[Advances in Marine Biology] Advances in Marine Biology Volume 15 Volume 15 || The Biology of Pseudocalanus

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  • Adv. mar. Biol., Vol. 16. 1978 pp. 1-231.


    CHRISTOPHER J. CORKETT and IAN A. MCLAREN Dalhousie University, Halifax, Nova Xcotia, Canada

    I. Introduction . . .. .. .. .. .. 11. Systematics . . .. .. .. .. ..

    A. Nomenclature . . .. .. .. B. " Physiological " Species . . .. .. C. Variations in DNA Content . . .. .. D. Retrospects and Prospects . . .. ..

    111. Distribution and Abundance. . . . . . .. A. Geographical Distribution . . .. . . B. Abundance . . . . .. .. .. C. Temporal Variations . . .. .. .. D. Vertical Distribution . . .. .. .. E. Sampling Problems and Microdistribution . . F. Physical-chemical Limits to Distribution . . G. Retrospects and Prospects . . .. ..

    IV. Morphology . . .. . . .. . . .. A. Embryo .. .. .. .. .. .. B. Nauplii . . .. .. .. .. .. C. Copepodids (C I-C V) . . . . . . .. D. Adults (C VI) . . .. .. .. .. E. Retrospects and Prospects . . .. ..

    v. ResDiration . . .. . . . . . . ..




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    A. Factors Influencing Rate of Oxygen Consumption. . B. Respiration and Food Requirements C. Retrospects and Prospects . . ..


    VI. Excretion . . .. .. .. A. Nitrogen .. .. .. B. Phosphorus . . .. .. C. Retrospects end Prospects . .

    VII. Locomotion . . .. .. .. A. Routine Swimming . . .. B. Escape Reaction . . . . C. Retrospects and Prospects . .

    VIII. Nutrition . . .. .. .. A. Feeding Mechanism . . .. B. FoodEaten . . . . .. C. Feeding Rate . . . . .. D. Die1 Feeding Rhythms .. E. Assimilation . . .. .. F. Food Requirements for Sustenance G. Retrospects and Prospects . .

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    IX. Reproduction .. I . .. .. .. .. .. A. SexRatio . . .. .. .. .. .. B. Oogenesis and Egg Laying . . .. . . . . C. Sperm and Spermatophore Production . . .. D. Mating . . .. . . . . .. .. . . E. Reproductive Rate . . .. . . .. . . F. Retrospects and Prospects . . .. . . . .

    X. Development and Growth . . .. . . .. .. A. Embryonic Development Rate . . .. .. R. Hatching . . . . .. . . . . . .

    D. Longevity of Adults . . .. .. .. .. E. Body Size . . . . . . . . . . .. F. Body Composition and Weights . . .. . . G. Oil Storage . . . . . . . . . . . . H. Growth Rates . . . . . . . . . . .. I. Rate of Production of Egg Matter . . . . .. J. The Balance Equation and Growth Efficiencies K. Retrospects and Prospects . . . . ..

    C. Development Rate of Nauplii and Copepodids . .

    XI. Life Cycles in Nature .. .. . . . . A. General Features, Terminology and Approaches


    B. Representative Life Cycles . . C. Retrospects and Prospects . .

    A. Ontogenetic Migrations . . XII. Vertical Migration . . .. ..

    B. Seasonal Migrations . . .. C. Die1 Migrations . . . . D. Retrospects and Prospects . .

    XIII. Production . . . . . . . . A. General Methods . . . . B. Production Estimates . . C. Retrospects and Prospects . .

    XIV. Parasites . . . . .. .. A. Dinoflagellates . . .. .. B. Gregarines . . . . . . C. Trematodes . . .. . . D. Nematodes . . .. .. E. Crustaceans . . . . . . F. Retrospects and Prospects . .

    XV. Role in the Food Web .. . . A. Effect on Phytoplankton . . B. Predators . . . . . . C. Significance in the Food Web. . D. Retrospects and Prospects . .

    XVI. Acknowledgemonts . . ,. .. XVII. References . . .. . . ..

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    Over forty years ago, at a conference sponsored by the National Research Council of Canada, Russell (1934) put our subject into context: intensive study of the plankton in northern waters . . . supplemented


    by recent observations on the food of plankton-feeding fish have all pointed to the economic importance of a few species only. In first rank can be placed Calanus Jinmarchicus, Temora longicornis, and Pseudocalanus elongatus . . , These three genera have all been extensively studied since, and Calanus has been admirably ( booked (Marshall and Orr, 1955). Perhaps because of its relatively large size, Calanus has been most favoured as an experimental animal and is much the best known copepod in a number of ways. Our knowledge of Pseudocalanus is somewhat complementary to that of Calanus. Out of an awareness, expressed even in the earliest copepod literature, of the extreme variability of size of PseudocaZanus in nature, has grown a rather precise set of ( rules concerning its development, growth, and reproductive rates. Perhaps it can also be said that there has been more concern with the mean response to environmental variables in studies of Calanus and more interest in individual variation in studies of Pseudocalanus.

    The reader should be aware that we have generally avoided using papers in the vast copepod literature that make no direct reference to Pseudocalanua. This may disappoint readers who feel that a more complete or deeper account might have been inferred from systematic relationships. For example, the swimming of Calanus nauplii has been well described, and there is no reason to suppose that the morpho- logically very similar nauplii of Pseudocalanus would behave differently. However, since we can find no description of swimming of Pseudoculanus nauplii, we do not cover the subject.

    We have attempted to be analytical and synthetical where possible in our review, and do not simply summarize the observations and conclusions of other authors. Some readers may feel that on occasion we have selected or even abused the writings of others in the search for patterns and regularities. However, we have reserved our most personal assessments of research on Pseudocalanus for the sections in each subsection that we call ( retrospects and prospects . Therein we broadly assess what has been done and suggest promising (and un- promising) lines for future investigation. Some of our suggestions for future research may seem a little vague ; perhaps they have to be since real discovery is by nature unpredictable.

    11. SYSTEMATICS A. Nomenclature

    1. The Genus The Genus was established by Boeck (1864) with the name Clausia,

    in honour of the late C. Claus. Later Boeck (1872) discovered that the


    name Glausia had been preoccupied by a parasitic copepod and there- fore substituted the name Glausia with the new name Pseudocalanus.

    2. Described species (a) Pseudocalanus minutus (Kreryer, 1845)

    The first description of a species of the genus was the publication of a plate by Kreryer (1842-45), on which the animal was given the binomen Calanus minutus. No description of the plate was pubIished a t the same time, but since the plate was published prior to 1931 the plate and accompanying binomen are sufficient to describe a new species (I.C.Z.N., Art. 16, a, vii). The original drawing is reproduced in Fig. 1 and is clearly a male copepodid V (see p. 30, Table I), although

    FIQ. 1 . Calanus minutus Kreyer, 1845, the type species of Pseudocalanus. A male copepodid V. ( x 2.6 from original plate 41 in Kreyer, 1842-46.)

    the diagram shows five thoracic segments and not the usual four. K r ~ y e r (1848) did publish, separate from the plate, a description of a male copepodid V of Calanus minutus in which he described the fifth thoracic segment as being rudimentary and free on its lateral and ventral sides. This evidence suggests that the fourth and fifth thoracic segments were incompletely fused or that the suture line of the fusion was still visible. This is not uncommon in Pseudocalanus and With (1915) illustrated copepodids V of both sexes showing small fifth thoracic segments.

    A problem arises since the date of publication of the binomen Calanus minutus is the date of publication of Kreryers plate, and we have been unable to obtain this exact date. It is known that the date must have been during or before 1845, when the last plates of this


    work were published (Sherborn and Woodward, 1901), and the date 1845 can therefore be used after the binomen (I.C.Z.N., Art. 21, f ) . According to de la Roquette (1842, p. 446), publication of the first plates had begun by 1842. We, therefore, cite both dates in our references except in purely nomenclatorial citations,

    K r ~ y e r preserved some specimens which were examined by With (1915), who described them as belonging all to the penultimate stage (18 + 29) , presumably meaning one male copepodid V and two female copepodids V. However, Dr B. Frost (personal communication) has recently examined the same material and reports that it consists of three female copepodids V and one male copepodid IV. This appears to exclude the possibility that the holotype is extant. I n view of other taxonomic problems to be documented below, great care should be taken in any future designation of a neotype.

    (b) Pseudocalanus elongatus (Boeck, 1864) P. elongatus was first given the binomen Clausia elongata by Boeck

    (1864) in a short description of adult males and females, with the observation that females were common and males rare in Christiana (Oslo) Fjord. Boeck made no reference to the earlier publications of K r ~ y e r (1 842-45, 1848).

    (c) Pseudocalanus clausii (Brady, 1865) Specimens of this species were originally found by Brady (1863)

    in the North Sea and erroneously ascribed by him to a quite different genus and species, Phadnna spinifera. Later Brady (1865) gave his specimens the new binomen Calanus Clausii, after the carcinologist C. Claus.

    (d) Pseudocalanus acuspes (Giesbrecht , 1 88 1 ) This species was originally described by Giesbrecht as Lucullus n.

    gen. acuspes, from the Bay of Kiel, and later given a very thorough description with excellent illustrations, by Giesbrecht (1 882).

    (e) Pseudocalanus major G. 0. Sars, 1900 This species was described by Sars (1900) as so very resembling

    the type species [by this he meant P. elongatus] that I should have been very much inclined to regard it as only a large variety if both forms were not found together in the very same samples, without exhibiting any transitions .

    Sars (1900) did not refer to the publications of Krayer (1842-45, 1848), but does refer to Boeck (1864) and, implicitly, Boeck (1872),


    so that clearly he assumed that prior to his work the genus contained only P. elongatus (Boeck, 1864).

    ( f ) Pseudocalanus gracilis G. 0. Sars, 1903 The classic work of Sars (1903) contains a description and figures of

    P. gracilis in the supplement at the end of the volume. He described the females of P. gracilis as being more slender than those of P. elongatus, as having a more conspicuously projecting frontal region and as having longer and narrower caudal rami. When females were placed on their side, the flexed first antenna was said to reach the end of the third urosome segment in P. gracilis, whereas in P. elongatus the first antenna reached only to the end of the genital segment.

    The male of P. gracilis was said by Sars (1 903) to resemble that of P. elongatus, the only distinction between them being the longer first antenna of the former.

    3. Subsequent delimitations of described species Pseudocalanus has been referred to under a variety of species names

    in the subsequent literature. Clearly the designation of at least some of the species has been less than satisfactory. We are concerned here with those papers that have attempted to clarify the status and characters of species.

    Much of the difficulty in subsequent work on the nomenclature of Pseudocalanus comes from the fact that Boeck, Brady, Giesbrecht, and G. 0. Sars did not mention the work of Krrayer in relation to the genus Pseudocalanus.

    Brady (1878) synonymizes his Calanus Clausii, 1865, with Pseudo- calanus elongatus (Boeck, 1864). Giesbrecht (1882, addendum p. 167) admits the synonymy of Lucullus acuspes Giesbrecht, 1881, with Pseudocalanus elongatus (Boeck, 1864) and P. clausii (Brady, 1865). Giesbrecht (1882) says that he had not previously been aware of the identity of the species he described due to the poor original accounts given by Boeck and Brady. Giesbrecht also lists in his bibliography Kraryers (1848) text description of P. minutus, but not Krayers (1842-45) plate. Giesbrecht was thus clearly aware of Krrayers work, but probably did not consider the description to be detailed enough to be worthy of comments in connection with the genus Pseudocalanus.

    It seems inconceivable that Sars did not know of the work of his compatriot, H. Kraryer, but since Kraryer described an immature specimen, Sars may not have viewed it as Pseudocalanus. Clearly the species name minutus is available for a species of Pseudocalanus, and


    the question arises: is the form that Krayer described synonymous with P. elongatus (Boeck), P. major, G. 0. Sam, or P. gracilis, G. 0. Saw?

    With (1915) considered this question in detail and examined what he referred to as Kraryers original specimens, and was of the opinion that the three species described by Boeck and G. 0. Sars were synonymous, since he found transition specimens in shape of head, length of first antenna, and size. With did, however, state that Krayers specimens ( were in shape of the head most like P. gracilis, and were of middle size ,. With (1915) therefore recognized only one species: Pseudocalanus minutus (Krcryer).

    Wiborg (1954) considered that G. 0. Sars was right in establishing three species and made use of the observations by With (1915) on Krcryers original specimens (see above) to designate P. gracilis as a synonym of P. minutus. He retained P. elongatus as a separate species and expressed some doubt about P. major, which he thought may be an independent species or a large-sized P. elongatus. He noted that P. minutus is normally larger than P. elongatus, but felt able to distinguish the two in samples from Norway, even when size showed considerable overlap, on the basis of body shape and length of second antennae.

    Although Brodskii (1948) indicated that two kinds of Pseudocalanus, differing in robustness of body, might be found in the Sea of Japan, he was content to follow Withs (1915) judgment of Sars species and to refer all his material to P. minutus. Later Brodskii (1950), in his major monograph on Calanoida of Soviet Far Eastern Seas and the Polar Basin, recognized three species : P. elongatus, P. major, and P. gracilis. In doing so he added to Sars (1900, 1903) criteria for separating the species, using relative lengths of the urosomes of adult females and the proportions of segments of the fifth legs of the adult males. However, in the synonomy of P. elongatus, Brodskii (1950) quotes Kraryers binomen, Calanus minutus, so that his three species should have been given as P. minutus, P. major, and P. gmcilis , according to the Law of Priority.

    Parran and Vervoort (1951) recognized three forms in one single species : Pseudocalanus minutus elongatus, P. minutus major, and P. minutus gracilis. Today, however, these forms should be con- sidered as subspecies (I.C.Z.N., Art. 45, d, i, and Art. 45, e, i) and one of the three subspecies should be a nominate subspecies and have the same name as the species, i.e. Pseudocalnnms minutus minutus (I.C.Z.N., Art. 47, a).

    Fontaine (1955) synonymized all the described species under Pseudocalanus minutus (Krayer) and attributed size variations (some-


    times continuous, sometimes polymodal) in her material from northern Canada to environmental influences.

    Kamshilov (1961) stressed the very great variation in size with no evidence of polymodalism, of Pseudocalanus in the White and Barents Seas and showed that the coefficient of variation (standard deviation/ mean) of size in his samples was twice that of Calanus (species not given). Furthermore, the ratio of cephalothorax length to length of urosome, which had been used (Brodskii, 1950) t o separate supposed species, had a continuous, unimodal distribution. He concluded that all his material should be referred to P. elongatus. However, here again, if this is done the name P. minutus has priority.

    Grice (1 962) stated that '' Pseudocalanus minutus was represented by two size groups ( P . minutus f. elongatus and f. gracilis) " in his collections from the Arctic Basin, but he did not routinely discriminate them.

    Cairns (1967) in his samples from the Canadian Arctic examined one criterion that had been used to define kinds of Pseudocalanus: there appeared to be two groups of females, not completely separated by size, but showing a possible discontinuity, on a graph, of urosome length against cephalothorax length. The regression coefficients of urosome length on cephalothorax length were 0.520 for the small and 0.376 for the large ones. Within the wide continuous size range (about 1.0-1-4 mm in cephalothorax length) of the large animals, the length of the urosome relative to the cephalothorax decreased with size. Cairns did not attempt to refer his specimens to any species of the genus Pseudocalanus, and suggested that the large and small females might represent reproductively isolated forms or have resulted from different environmental conditions.

    Lacroix and Filteau (1971) believed that two " forms ) ) (per Farran and Vervoort, 1951), the small elongatus and the large major of Pseudo- calanus minutus occur in the Baie-des-Chaleurs, off the Gulf of St. Lawrence. Adult females of the large form (cephalothorax mean - 1.4 mm) were common in spring, but the small form (- 0.9-1.0 mm) predominated in spring and summer. The large form predominated as copepodid V (1.2-1.3 mm) in the deep, cooler waters throughout the summer.

    Enough examples have been given to indicate that problems of nomenclature and of delimitation of named species pervade the literature on Pseudocalanus. A formal systematic revision would involve the examination of much new material. Since we cannot do this here, we follow the practice of McLaren (1965) and refer only to the generic name throughout this review on the biology of Pseudo-


    calanus. This is not to deny the certainty that different kinds of Pseudocalanus exist, but that these kinds may be difficult to accom- modate either in the formalities of nomenclature or in prevailing concepts of species (see p. 11).

    B. " Physiological '' species

    Even if morphological differences among geographically isolated populations of Pseudocalanus are elusive, physiological differences occur that may signify reproductive isolation (cf. Carrillo B.-G. et al., 1974).

    McLaren (1965, 1966) showed that the temperature response of adult female size and of embryonic development rate varied geographi- cally. For example, extrapolation of the size-temperature relationship (Fig. 26) for Loch Striven, Scotland, to 0C suggeststhat at this tempera- ture (normal for a female from the Canadian Arctic) a monster larger than any known species of copepod would result. Of course this is hypothetical, since development would simply not take place a t this low temperature, and furthermore the size-temperature relationship may break down a t excessively low temperatures (see p. 122). Clearly, however, there are inherent differences between populations in these two parts of the world. Regional differences in development rate, for example, expressed as time to reach various stages (Fig. 25), are less pronounced.

    C. Va&ations in DNA content

    I n recent years a novel source of variations within and between populations of Pseudocalanus has been discovered. McLaren (1 965) described a large form of Pseudocalanus that coexists with a more abundant small form in Ogac Lake, a partially landlocked fiord on Baffin Island, northern Canada. The small form was believed to be the same as the widespread Pseudoealanus of waters outside the fiord, the size of which had been reduced inside the fiord by elevated temperatures (see p. 117, Fig. 26).

    I n the large form embryonic duration (McLaren, 1966; see also p. 103, Fig. 22) and development times of older stages (McLaren, 1965 ; see also p. 113) are longer than those of the small form.

    McLaren (1965) speculated that the large form of Pseudocalanus was a polyploid. However, later work (McLaren et al., 1966) showed that both forms of Pseudocalanus from Ogac Lake contained the same chromosome number (n = IS), but that chromosomes in undivided


    eggs of the large form were much larger than those of the small form. The DNA content of nuclei a t the 32-cell stage was about seven times greater in the large form. This was attributed to polyteny, although today the whole question of repetitive or otherwise increased amounts of DNA tends to be discussed in different terms.

    Woods (1969) added more information, demonstrating that the large forms in Ogac Lake and also in another landlocked fiord, Winton Bay on Baffin Island, were morphologically very similar, except in size, to the small forms and to the phenotypically larger forms of the cold seas outside. Female cephalothorax lengths of the large forms were respectively (means f S.E.) 1.09 f 0.040 mm and 1-16 f 0.044 mm in Ogac Lake and Winton Bay, whereas the small forms were 0.85 & 0.009 mm and 0.84 f 0.007 mm. The small form is larger in cold waters outside the lakes, but its eggs are always smaller than those of the large form (see Table XVIII, and McLaren, 1965, his Fig. 1). Woods specu- lates on the adaptive meaning of these large forms. Noting that the effect of increased DNA per nucleus is probably an increase in cell size and a decrease in cell division rate, she suggests that this restores the normal size and cycle for an arctic population forced to exist in abnormally warm environments. Indeed, in Ogac Lake, McLaren (1969) showed that the small form may " waste '' much of its reproductive effort, since early broods matured and produced an unsuccessful second generation in summer. Under these conditions, there should be selective pressure for maturation later in the season, which would be thwarted by genetic exchange with the populations from outside the lakes, brought in by periodic high tides. Woods also notes arguments that larger size allows a greater range of food (see also p. 63). The large form during summer does show retarded maturation of the overwintered generation and slow progress of the new generation, compared with the small form (McLaren, 1969 ; Woods, 1969) thus restoring an essentially normal arctic life cycle (see p. 139).

    The large forms can be viewed as an " instant species ", almost certainly reproductively isolated from the coexisting small forms, in the manner of polyploid species among plants. It may be wondered if such discontinuous DNA variation is partly responsible for some of the size- polymodalisms in Pseudocalanus noted in the literature. Clearly this raises nomenclatural and systematic problems : how many of the described species are of this sort? Can such variants, morphologically identical to widespread forms except in size, spring up independently among different populations, and should they be classed together on the basis of size? To what extent does such a size change allow rapid morphological divergence to occur!


    Recently the whole question of DNA variation in Pseudocalanus has become more complex. Hart and McLaren (1978) have shown that there is continuous variation in body size, egg size, and attendant embryonic duration in populations of Pseudocalanus from Halifax, Nova Scotia (p. 105). McLaren (1976b) showed that the size of adult females is strongly heritable (p. 123) and that size of adult females is strongly related to DNA content of somatic nuclei (p. 124).

    D. Retrospects and prospects

    What started out as a rather classical nomenclatural muddle has led to a frontier problem in systematics. We feel that some of the nomenclatural confusion has been exacerbated by the attempts (e.g. Brodskii, 1950) to define species limits in terms of size and its correlates that are highly responsive to environmental influences and are also perhaps subjected to strong local differentiation under natural selection. We hope that the nomenclatural and systematic problems in Pseudo- calanus will be cleared up by a revision of the genus that takes into account these aspects of variability. Further investigation is clearly needed on the role of quantitative DNA variation at the ecological, evolutionary, and molecular level.

    The DNA content of nuclei, presumably by mediating cell size and cell division rates (Woods, 1969), may act as a basis for the quantitative inheritance of body size and durations of developmental stages. This genetic basis for maintaining phenotypic diversity may be aided by size-assortative mating (see p. 84). Not only is such a mechanism quite extraordinary but its consequences may defy simple systematic analysis. Consider the possibility, given the strong heritabilities of size together with assortative mating, that disruptive selection could very quickly lead to two reproductively isolated populations where once there was one. Indeed, it is possible that biological species (sensu Mayr, 1963) could come and go rather quickly in this widespread genus of copepods. The situation in Pseudocalanus may find its counterpart in other groups of copepods, including the sibling species of Calanus, as mooted by McLaren et al. (1966).


    A. Geographical distribution 1. General

    Fig. 2. Our survey of the distribution of Pseudocalanus is summarized in

    Although well known in broad terms, its precise limits are


    obscure in some places and its reported presence in some localities is dubious or in need of confirmation. Sewell (1948) collates virtually all earlier references to distributions of marine copepods, and it remains largely to update and correct his assessments. Sewell, like most previous and subsequent reviewers, concludes that Pseudocalanus is basically a neritic, northern genus, found in arctic seas extending southward along cooler coasts, and even beyond in deep waters.

    FIQ. 2. World distribution of Pseudocnlnnus. Open-ocean boundaries in Atlantic after Edinburgh Oceanographic Laboratory (1973) and in Pacific after Omori (1965). Other sources in text. We consider this t,o represent the distribution of normally reproducing populations, although there are deep-wster records outside these limits, and animals may not commonly breed in the mid-Arctic Ocean.

    I n considering the limits of the range of Pseudocalanus, Sewell cites records from as far south as Chesapeake Bay in the eastern U.S.A., from the North Atlantic Drift south of Iceland, from European waters as far south as Portugal, and from the Mediterranean. I n the North Pacific, he records it south to Japan and Vancouver Island. In addition, some anomalous records can be gleaned from Sewells review, and these must be examined.


    Sewell himself notes that supposed occurrences in the northern Gulf of Suez of Pseudocalanus and other North Atlantic forms are open to doubt. The samples in which these copepods occurred were from seawater taps draining tanks that were probably filled prior to passage of the ship through the Suez Canal.

    Sewell (p. 497) implies that Pseudocalanus reaches subantarctic or even antarctic waters through the deep Atlantic, but does not document this statement with references. Although he later (p. 499) lists the genus for deep Atlantic waters, he does not include it in his list (p. 513) of arctic or North Atlantic forms recorded from subantarctic or antarctic waters. Nor does it occur in the most extensive modern review of copepods of these waters (Vervoort, 1965).

    Sewells report of Pseudocalanus off western South America is based on the work of Wilson (1942). This very large work and a sub- sequent one by Wilson (1950) extended the distribution of Pseudocalanus over vast areas of the tropical and subtropical Pacific and Atlantic, far outside previously accepted limits. Some authors have corrected or expressed doubts about other records in Wilsons (1942, 1950) lists. His records of Pseudocalanus seem to have been evaluated simply by being ignored in a number of subsequent publications on copepods of the waters surveyed by him. Contrary to Wilsons claims, Pseudocalanus has not been found in extensive sampling of the California Current (Fleminger, 1967), off western South America (Bjornberg, 1973), in near-surface waters of the southern North Atlantic (Deevey, 1971), or in the tropical Pacific (Grice, 1961 ; Vinogradov and Voronina, 1963).

    A number of papers subsequent to Sewell (1948) give a more refined view of the distribution of Pseudocalanus. We cannot possibly consider more than a fraction of these, and confine our review to those that give a wide perspective or a more accurate assessment of the margins of its range.

    2. Arctic Basin

    Pseudocalanus is common in coastal arctic waters and has been recorded from many parts of the Arctic Ocean proper, generally in the upper 300 m (e.g. Dunbar and Harding, 1968). It is, however, evidently scarce and patchy in the more central parts of the basin, and has not been found in some surveys (e.g. Minoda, 1967). Harding (1966) found no subadults in his samples from the basin, and concludes that Pseudo- calanus there is an expatriate from surrounding neritic waters, especially the Chukchi Sea, where it is common (Grice, 1962).


    3. North Atlantic and adjacent waters An excellent overview of North Atlantic distributions of adult

    Pseudocalanus has been constructed from the Continuous Plankton Recorder surveys (Fig. 2 18 in Edinburgh Oceanographic Laboratory, 1973). The marked abundance in upper waters off eastern Canada and western Europe contrasts with its general scarcity in the open Atlantic, where scattered records are shown southward to about 41"N.

    I n the inshore waters of eastern North America, Pseudocalanus has been noted as far south as Beaufort, North Carolina, a t latitude 34'40" (Pearse, 1936). However, this and a number of other identifica- tions made by Wilson for Pearse's study must remain suspect, especially one reputed finding of Pseudocalanus innear-fresh water. Bowman (1 971) states that Pseudocalanus does not occur south of Cape Hatteras, a zoogeographical boundary for many northern forms. It penetrates the Gulf of St. Lawrence to at least 60"20'W (Prdfontaine and Brunel, 1962).

    I n the eastern North Atlantic it can be common in the Bay of Biscay and off northwest Spain, but it is not listed for the waters off southwest Portugal (Vives, 1970). I ts distribution in the Baltic region has been recently summarized by Ackefors (1969a) and Arndt and Stein (1973). It penetrates the Gulfs of Bothnia and Finland in small numbers, but is evidently not found in shallow waters even in the northern extremities of the Baltic proper (Eriksson, 1973b).

    4. Nediterranean and Black Xeas I n spite of the earlier accounts reviewed by Sewell (1948) the status

    of Pseudocalanus in the Mediterranean is uncertain a t best. Rose (in Trdgouboff and Rose, 1957) includes the genus in his taxonomic keys to Mediterranean copepods, but makes no mention of its occurrence in his text. Surveys and biological studies of copepods in the western Mediterranean by Gaudy (1962) and Vives (1967) fail to mention it or note its absence specifically. If it occurs a t all in the western Mediter- ranean, it must be as a rare expatriate from the Atlantic. I n the eastern Mediterranean, the thorough survey by Kimor and Wood (1975) failed to report it.

    However, Pseudocalanus does occur in the Adriatic. VuEeti6 (1957) states that " sporadic individuals '' occur all over the Adriatic, but Hure and Scotto di Carlo (1968, 1969) found it only in northern parts, where it was most common in May, although never dominant numerically. Recent work (Dr J. Hure, personal communication)


    indicates that it extends in some numbers down the coast of Italy, but not evidently beyond the Strait of Otranto.

    Pseudocalanus is also well known as a disjunct population in the Black Sea. Its distribution there is detailed by Afrikova (1975)) who maps its abundance by season and depth.

    5. North Paci$c and adjacent waters The best modern overview of the southern limits of distribution of

    PseudocaZanus in the North Pacific is supplied by Omori (1965, his Fig. 4). It is shown as most abundant in shallow waters of the Bering Sea and near the Aleutians, relatively abundant near the coasts of Hokkaido and southern British Columbia, less so in the open ocean in between. It was absent from some samples along the 43"N parallel between about 170"E and 175"W.

    On the Pacific coast of Japan, Pseudocalanus seems to be one of a number of boreal species that is not found west of the Bonin Ridge running south from the Tokyo region, although it occurs in Sagami Bay at the landward end of the ridge (Furuhashi, 1961). Furuhashi's southernmost records offshore are at 38"OO'N 145"23'E and (Furuhashi, 1966) a t 40"03'N 152'01'N. I n the Sea of Japan, Pseudocalanus occurs in the extreme southeast (Morioka, 1973) and off the coast of Korea (Mori, 1937).

    On the American coast, the southernmost reliable record appears to be at 38"52'N, just off the coast of northern California (Davis, 1949).

    6 . Expatriates in deep water The geographical limits outlined above can be considerably extended

    (and probably will continue to be) by scattered records from deep waters. These represent individuals carried from waters farther north, unable to rise to warmer surface waters, and presumably incapable of sustaining populations indefinitely. Ignoring problematical earlier records in Sewell (1948), we find records in deep water of two individuals off the Azores (Roe, 1972)) seven females a t 31"31'N 64"OO'W near Bermuda (Harding, 1972), and a southernmost recorded specimen a t 29'58% 22'58'W (Grice and Hulsemann, 1965).

    7. Distribution in relation to water masses Copepod distribution is frequently discussed in relation to water

    masses or marine biogeographic zones. Pseudocalanus often figures as one of many " indicator " forms in such studies, only a few of which will be reviewed here.

    In the North Atlantic (e.g., Edinburgh Oceanographic Laboratory,


    1973) Pseudocalanus is found in pure Atlantic as well as mixed arctic and Atlantic (subarctic, sensu Dunbar, 1947) waters. A sophisticated approach is found in Colebrook (1964), who used principal component analysis to group and classify copepods of the North Sea and North Atlantic. This results in an objective designation of " Para-Pseudo- calanus " as a member of the intermediate group with respect to north- south and neritic-oceanic gradients. Unfortunately, the lumping of Pseudocalanus with Paracalanus, a more southern form, makes the designation less useful.

    The southern limits of Pseudocalanus at about 42"N in the open waters of the western North Pacific (Omori, 1965) coincides quite well with the subarctic boundary, which is defined in strictly hydrographic terms (Dodimead et al., 1963). Pseudocalanus occurs in and is used in the definition of the North Pacijic temperate region of Brodskii (1956).

    8. Distribution ui th respect to distance offshore Pseudocalanus is generally reckoned as a neritic copepod. This is

    very evident in maps of late-summer distribution in the Barents Sea (Zelikman, 1966, his Fig. 7), and on a grand scale in the North Atlantic surveys of the Continuous Plankton Recorder (Figs. 217, 218, in Edinburgh Oceanographic Laboratory, 1973). All the areas with the highest abundance of Pseudocalanus are within about 400 km of land. Nevertheless, Pseudocalanus does occur abundantly further offshore in northern extensions of the North Atlantic (Ostvedt, 1955). Motoda and Minoda (1974) refer to it as " typically oceanic " as opposed to neritic in the Bering Sea. Possibly this is a matter of definition. It is at times most abundant in the central region of the Black Sea (Afrikova, 1975).

    On a smaller scale, a number of authors have stated that Pseudo- calanus is generally commoner away from the immediate vicinity of the coast. For example, Evans (1973) found that Pseudocalanus in 1969 was four times as common ten miles off the Northumberland coast as it was two miles offshore. However, Petipa et al. (1963) in a series of transects off the coast of the northern Black Sea found that regions of concentration varied, sometimes near shore and sometimes farther out. Furthermore, it may tend to become more abundant in enclosed bays than in the open waters outside. This is shown most clearly in a series of samples taken in summer 1960-62 from the Baie-des-Chaleurs, in the Gulf of St. Lawrence (Lacroix and Filteau, 1971).

    We conclude that Pseudocalanus is indeed predominantly a coastal form, but that the neritic-oceanic gradient is an unrefined one, allowing for many exceptions.


    B. Abundance 1. General abundance

    Pseudocalanus is not only widespread in northern seas, but is often said to be the most abundant form in many surveys of these waters. Perhaps the most impressive testimony to its numerical importance is from the long-term surveys with the Continuous Plankton Recorder around the British Isles (Fig. 3). Along with Calanus jnmarchicus (including C . helgolandicus, no doubt), Pseudocalanus (with a small admixture of Paracalanus) is found in virtually all the sampled areas. It is also numerically the most abundant form per sample.

    It ispossible, in our opinion, that Pseudocalanus is the most abundant metazoan in the world.

    2. '' Patches " and mms occurrences Pseudocalanus may be found in '' patches ", many kilometres in

    diameter, that may be treated as dynamical and productive units (e.g. Thompson, 1976). This may be of considerable significance to

    A B

    0.05 0.5 5 5OloO 5 1.6 0.4 02 0 0.01 0.1 I

    Pam-Reudacalanus rpp. Acartla a m .

    Cantrapagas hamatus

    Euchaob habas

    Houromamma rabusta Pareuchadta narvefica

    Rhincalanus nasutus Plauramamma banalis

    Ploummamma adominah8 Phuramamma gmcilis Labidocero wllastoni

    Sapphirina app. Candacia armata Euchaeta acuta hfstridia /onfu Calanus minor

    Astidius armatus Anoma/acwa patsrsoni

    Calanus amcilis Contrapagas bmdy!' i

    Plsummamma xiobias I i ).6 0.4 0.2 0 0.01 0.1

    0.05 0.5 ' 5 FIQ. 3. Histograms of A, the proportion of sampled area (vicinity of British Isles) in

    which the species occurred, and B, the abundance of each species during 1948-66, as revealed by the Continuous Plankton Recorder Survey. (From Colebrook el al., 1961.) A.M.B.-15 3


    fisheries (seep. 201). Fish (1936) interpreted such concentrations around the Gulf of Maine as " stocks " in the manner of fishery science. He felt that breeding occurred first in offshore areas and later inshore, where local concentrations were sustained by hydrographic circum- stances from areas of higher production offshore. The number of stations involved makes some of his isopleths of abundance open to question.

    Soviet researchers have shown particular interest in such con- centrations. Zelikman (1961) found mass occurrences of over 1oQ individuals per m3 near the mouth of the White Sea in midsummer 1956. Meshcheryakova (1964) describes less dense concentrations of Pseudocalanus and other copepods in the eastern Bering Sea. Explanations for this are vague, but a lack of coincidence with concen- trations of Calanus is of interest. Kamshilov (1961) describes abrupt increases in abundance at boundaries of sharp temperature changes in surface waters on transects through the Barents and White Seas, ascribed to concentration by hydrographic forces. Zelickman and Golovkin (1972) agree that hydrographic forces are responsible for concentrations of Pseudocalanus and other zooplankters near bird colonies on Novaya Zemlya, but stress that the concentration is due to productivity, not " mechanical " consequences of hydrography.

    C. Temporal variations 1. Seasonality of occurrence

    Throughout its range, Pseudocalanus shows seasonal fluctuations in abundance in relation to primary production and other factors. Where life cycles are annual, it is clear that a numerical peak must occur during the season of reproduction. But even where more or less continuous generations occur, there may be marked seasonality in abundance. Some authors have attempted to discern large-scale patterns in this seasonality.

    Pavshtiks and Timokhina (1972) summarized the annual cycle of Pseudocalanus in the Norwegian Sea, showing that the summer peak of abundance occurs in late June in Atlantic waters, mid-July in mixed waters, and late July in the East Icelandic Current.

    Colebrook (1969) has systematized data from surveys with the Continuous Plankton Recorder by using the centre of gravity on the time axis of the area included under seasonal curves of abundance. Geographical variation in this statistic for Pseudocalanw (his Fig. 8, probably including some Paracalanus, although this was not stated) shows a reasonable pattern of early peaks in southern and coastal waters


    and later ones in northern and oceanic parts. Analysis of covariance shows that seasonality is correlated with temperatnre, but of course causes may be indirect.

    In the southern parts of its range, Pseudocalanus is a winter-spring form, and may disappear altogether from sampling areas during summer. Since this disappearance seems clearly related to high temperatures, i t is discussed separately (p. 24).

    2. Year-to-year and long-term changes in abundance The whole subject of secular changes in the marine environment is

    of profound importance (Russell et al., 1971) and Pseudocalanus has figured in some of the discussions.





    - n E oc e" 212 P


    .x 119



    I u +0 50

    Ye0 r

    FIG. 4. Average numbers, per sample of 20 miles, of Pseudooalanua (including Para- calanua) from the east-central North Sea in monthly periods from January 1948 to December 1972, taken by the Continuous Plankton Recorder. (From Glover et al., 1974.)

    Pavshtiks and Timokhina (1 972) tabulate a five-fold variation in production of Pseudocalanus (p. 187) in the Norwegian Sea in seven seasons between 1959 and 1969. This is vaguely related by them to the temperature regime and the timing of the spring maxima.

    Lacroix and Filteau (1971) found that Pseudocalanus averaged two and a half times as common in the Baie-des-Chaleurs, Canada, in 1962 compared with 1960. They suggest that a warm hydrographic


    winter promoted strong vertical mixing and high production in the subsequent summer season in 1962.

    Meshcheryakova (1964) describes a roughly two-fold difference in abundance of Pseudocalanus and other forms in the eastern Bering Sea in 1958 and 1959. In the former year, an earlier warming led to a strong diatom bloom in summer, which in turn encouraged strong representa- tion of the copepods.

    Peterson and Miller (1975) found a marked reduction in abundance of Pseudocalanus off the coast of Oregon in 1971, evidently associated with reduced upwelling and warmer water than usual.

    In the Black Sea, annual production of Pseudocalanus (p. 183) varied almost two and a half fold during the period 1960-66 (Greze et al., 1968.)

    The remarkable summary of long-term changes in the east-central North Sea by Glover et al. (1974) is summarized on Fig. 4 (which includes Paracalanus; G. A. Robinson, personal communication). These authors conclude that the long-term reduction in mean annual abundance is related to retardation in the time of the spring phytoplankton bloom, from late March to mid-April in the Atlantic off the British Isles, and from mid-March to mid-April in the North Sea. This has led to a reduced length in season of sustained production by the zooplankton from slightly more than seven months in the fifties to about six months in the early seventies. Underlying the biological trends is said to be a climatic trend involving the withdrawal of Atlantic influence from the North Sea,

    D. Vertical distribution

    Pseudocalanus is generally found in the upper layers of the sea, although individuals have been taken as deep as 4 000-5 000 m (Grice and Hulsemann, 1965). Here we first outline briefly the main features of vertical distribution in the open sea, where the bottom may not set the deepest penetration. Then we consider inshore waters, where details of vertical distributions with respect to phydcal, chemical, and biological factors may be more evident than in the open sea. There is of course a dynamical aspect to this subject, which is dealt with at length elsewhere (Section XII). We refer throughout this section to daytime distributions of Pseudocalanus.

    The broad capabilities of Pseudocalanus are evident in vertical samples from deep, oceanic waters in various regions. In the Norwegian Sea, most individuals occur above 50 m in spring, but below 1 000 m at other times of the year (Ostvedt, 1965). In the southern Bering Sea,


    &oda (1971) found that most animals were between 0 and 50 m in a series of samples taken from 28 May to 19 June 1962. Only a tiny fraction (average 0.1%) occurred in the deepest hauls (between 707 and 1 350 m). Over the deep Kuril-Kamchatka trench, 98% of the biomass of Pseudocalanus occurs in the upper 50 m, according to Arashkevich (1969). Dunbar and Harding (1 968) found that almost all individuals were taken between 50 and 300 m under the ice of the Arctic Ocean ; at these depths, largely unmixed arctic waters are found. In offshore regions of the Black Sea, which is of course anoxic in deeper waters, Pseudocalanus is found down to at least 200 m but is generally more common above 50 m (Afrikova, 1975). We conclude from these studies that Pseudocalanus is capable of living in very deep waters (unless prevented by lethal conditions, as in the Black Sea), but may only be evident if seasonal samples are taken.

    Studies of vertical distributions in shallower, inshore waters give more insights into the physical, chemical, and biological factors, that might control such distributions. Minoda and Osawa (1967) found that Pseudocalanus and other small copepods were concentrated by day at depths of the sonic scattering layers in the Okhotsk Sea in summer, 1963, and this coincided with the thermocline at the time. In the Landsort Deep of the Baltic, Pseudocalanus was most abundant at 50-100 m, just below a thermal minimum, absent above 30 m, where temperature began to rise sharply, but present even down to 300-400 m, in spite of virtual absence of oxygen (Ackefors, 1966). At a shallower station south of Stockholm, Pseudocalanus always occurred below the thermocline at 20-30 m in spring and autumn, although a few were found near the surface in unstratified waters in winter (Ackefors, 1969b) ; salinities were low but varied only slightly with depth. In a semi-landlocked bay on the island of Split, Yugoslavia (VuEetiE, 1961), Pseudocalanus occurred at the surface only in January and November, when the water column was almost isothermal and


    wealth of information on the daytime vertical distributions of copepodids and adults (combined) at four stations a t several times of year, all accompanied by details of physical and chemical conditions in the water column. At the shallowest station (40 m) animals were generally commonest at mid-depths, whereas at another just slightly deeper (45 m) station they were more often found near the bottom. Both these stations had strong tidal currents and little thermal stratification. At a deeper station (100 m) there were single sharp peaks of concentration of three of the five sampling dates ; on each of these three dates there was distinct thermal stratification not present on the other two dates. The relative concentration at about 10 m on 22 January 1969 was more extreme than any other example depicted, and this concentration was in the middle of a sharp positive temperature gradient near the surface. Distributions at the deepest station (275 m) were remarkably uniform with depth at all times of year ; there was almost no thermal stratification. Lee and Williamson also depict the vertical distribution of NO,, NO,, PO,, and SiO,, which in some instances showed strong stratification when temperatures and salinities appeared uniform. Lee and Williamson single out two stations in March as showing chemical stratification in relation to copepod distribution. In the shallowest station a high NO, value near the bottom is correlated by them with smaller numbers there. On the other hand, in the deepest station a sharp maximum of NO,, NO,, and PO, occurred a t 100 m, which according to Lee and Williamson coincided with a peak of Pseudo- calanus; this peak appears to us to be unconvincing.

    E. Xampling problems and microdistribution

    Three different problems may thwart accurate estimates of the mean numbers of copepods living in a sampled unit of water : (1) the sampling gear may allow some individuals to slip through the net meshes ; (2) individuals may avoid being captured by the apparatus ; and (3) individuals may be arranged in a clumped manner in the water, and subject to being undersampled or oversampled in any one catch.

    It is obvious that many studies of copepods including Pseudocalanus have badly undersampled the young stages. The work of Carter (1965), McLaren (1969) and others indicates that a mesh of No. 20 (apertures 76 pm) is adequate for all stages (eggs being of the order of 100 pm at least). A formal study of size selectivity achieved by sampling Pseudo- culunus and other forms is offered by Sherman and Honey (1971).

    McLaren (1969) showed that a, 12.5 cm Clarke-Bumpus sampler towed vertically a t about 0.5 mls obtained on average about the same


    number of adult females (mean 5% more, range 29% less to 34% more) as predicted from parallel hauls with a net 0.5 m in diameter. The difference between the two nets was significant only on three of seven occasions during the season. There was thus no good evidence that females can escape a net as small as 12.5 cm in diameter towed at this speed. The superiority of vertical net hauls in dealing with vertically stratified zooplankton, including Pseudocalanus, is confirmed by samp- ling in enclosed experimental systems (Lawson and Grice, 1977).

    Of greater interest is the possibility of real horizontal variations in microdistribution. The parallel vertical net hauls of McLaren (1969) described above gave weak evidence that clumping on a horizontal scale of a few centimetres or metres did not occur in Ogac Lake,a peculiarly stable system hydrographically. Barnes and Marshall (1951) used a rapidly taken series of pump samples of about 6 1 each to test the distributions of various forms at 10 m off Millport, Scotland. In one series, nauplii of Pseudocalanus showed significantly non- random clumping, whereas nauplii of a number of other copepods did not show any such tendency. Barnes and Marshall suggest that such small scale clumping may result from the fact that Pseudocalanus, unlike the other species, carries its eggs until they hatch as nauplii.

    Recently Smith et al. (1976) have demonstrated marked aggregation of adult Pseudocalanus and other copepods in shallow waters off the coast of Oregon. They found that concentrations varied three- to ten-fold over horizontal scales of 30 to a few hundred metres. This variation was attributed to physical processes, largely related to vertical displacements of marked depth-peaks of concentration by internal waves in this near-shore setting. Presumably vertical net hauls, as opposed to the pump samples from fixed depths used by Smith et at., would have shown less variability on a horizontal scale.

    F. Physical-chemical limits to distribution 1. Temperature

    Psezldocalanus often tolerates great temperature variations through- out its range. However, temperature clearly is involved directly or indirectly in setting its limits of distribution.

    Although Kolosova (1975) concludes, from extensive field sampling, that Pseudocalanus in the White Sea has a temperature preference of 2-8C, this may reflect a wide variety of hydrological and biological causes rather than any debilitating effects of extreme temperatures.

    The limits for existence presumably exceed those for reproduction and development. McLaren (1966) lists for a number of localities experi-


    mental temperatures at which successful embryonic development occurred. A t 0C a t least some eggs hatched in all localities. The highest temperatures listed are 7.1 and 7~9C for two localities in the Canadian Arctic, 12-0C for Halifax, Nova Scotia; 13-1"C for Woods Hole, Massachusetts ; and 14.9OC for Loch Striven, Scotland. Corkett and Zillioux (1975) hatched eggs from Plymouth at 16-2"C. Thompson (1976) found that individuals from the southern North Sea could be reared at 3.7"C only up to NV, whereas those at 5-0"C could reach maturity. We shall indicate later (p. 108), that development below 8C may have been in other ways abnormal.

    It is expected that local populations will be adapted to local temperature extremes, but it is of some interest to consider the absolute thermal limits of Pseudocalanus in nature. Deevey (1960a) graphs the

    extreme range " as -1.8' to 24.5"C and the " breeding range " as -1.0" to 19C. However, these ranges must be looked at more critically.

    There is no doubt that Pseudocalanus exists and must a t times breed in the arctic a t the temperature of freezing of full sea water (ca. -1-8"C). The upper limit is less certain. Sampling techniques must take into account the fact that Pseudocalams may occupy the cooler parts of stratified water columns. The record of a few individuals at 20-21OC in the unstratijied Cape Cod Canal (Anraku, 1964a) must reflect its real potential for existence there. The occurrence (noted as " rare ") a t 23C in the Japan Sea (Morioka, 1973) also seems to have taken full account of vertical stratification of temperature (the species otherwise was found only at or below 13C). In the Black Sea, where surface temperatures in open water probably exceed those found in any other part of the range of Pseudocalanus, it stays in cooler depths in summer and autumn, but Porumb (1973) says that it almost disappears when surface waters warm to 23-26.5"C.

    We are unable to find any satisfactory upper temperature limit for breeding of Pseudocalanus in nature. Deevey (1960a) found eggs in samples from Delaware Bay in June, but only surface temperatures are given, and we have no indication that eggs were viable.

    2. Salinity There is limited laboratory information on the adaptability of

    Pseudocalanus to extreme salinities. McLaren (1966) found that mortality during embryonic development was equally high at salinities of 25.7 and 32-3%, for animals from Ogac Lake, Baffin Island, a brackish-water environment. McLaren et al. (1968) concluded that mortality of developing embryos was significantly higher only at the lowest experimental salinity of 2 5 ~ 2 % ~ for animals from full strength

    6 6


    sea water near Halifax, Nova Scotia. This seems to be weak evidence for local adaptation to low salinities of Ogac Lake.

    Certainly Pseudocalanus in nature is quite euryhaline or, properly " euryhaline-marine " (Jeffries, 1962). It is known from quite saline waters (37%,) in the Adriatic (VuEetid, 1961), but presumably does not have to contend with much greater hypersalinity. However, it is often found in highly freshened waters.

    Kuznetsov (1973) found that Pseudocalanus avoided the freshened (6-80/103) upper 6 m of the Laptev Sea in October. The lowest estimate of the limiting salinity appears to be that of Hessle and Vallin (1934), who state that it occurs at 4-5%, in the Baltic. However, this esti- mate may not have taken full account of stratification. The very accurate vertical sampling in the Baltic by Ackefors (1969b) revealed 6 ~ 0 % ~ as the lowest salinity where Pseudocalanus occurred. This is the lowest reliable estimate of which we are aware. Ackefors (1969b) and others have noted that Pseudocalanus is found in such low salinities only when the water is cold, in the depths in summer and near the surface only in winter. Ackefors also suggests that it does not spawn in the shallow waters near Asko, near Stockholm, where salinity does not exceed 7.5%,.

    3. Oxygen Pseudocalanus lives routinely in the Baltic at depths where the

    oxygen concentration is usually less than 2 ml OJl, and sometimes very near zero (Ackefors, 1969a). The lowest oxygen concentration where Pseudocalanus has occurred can be inferred from Ackefors (1966), who found some individuals between 400 and 500 m in the Baltic in August, when oxygen below 300 m was 1 ml/l and only 0.04 ml/l a t 440 m. A few individuals were taken at 31 m in Ogac Lake, Baffin Island, by McLaren (1969). At this depth oxygen was unmeasureable, but the very strong stratification on a small depth scale makes this record less reliable than those of Ackefors. Clearly, however, Pseudocalanus is capable of withstanding virtual anoxia.

    4. Pollutants Studies on the effects of pollutants on marine organisms are becom-

    ing commonplace, and a few published experimental studies deal with Pseudocalanus.

    Grice et al. (1973) found that acid waste sufficient to reduce sea- water pH to 6.7 (control 7.8) gave 30% mortalities of adults in 24 h. Lower pH gave lOOyo mortalities. They concluded that these effects were unlikely to be important in nature.


    Lee et al. (1977), using large polyethylene enclosures in the sea, found that initial fuel oil concentrations of about 40 p.p.b. (major non-volatile components) above the control concentration, had no measureable effect on zooplankton populations that were 44-91 % Pseudocalanus.

    Gibson and Grice (1977), again using large polyethylene enclosures in which Pseudocalanus was the predominant copepod, added concen- trations of copper. At the highest level of 50 pg Cull Pseudocalanm populations fell to 50% of their original levels at a rate 2.5-3 times faster than did controls. Reeve et aZ. (1977) studied rates of ingestion and production of faecal pellets by P~eudocaZ~n~s removed from these enclosures. Some depression in these rates when water samples from the enclosures were used was due to the reduction of food organisms by effects of enclosure or copper, so that rates determined on standard food (from outside the enclosures) give a more reliable indicator of effects of copper as a stress on the copepods. Ingestion rates on the standard food by control copepods (mean 14-2 pm3/cop./day) were below those that we believe to be saturation levels (see p. 68). There was no clear effect of copper by day 2, but by day 4 both ingestion rates and faecal production were reduced. By day 9, when populations in the enclosures had been severely depressed, these rates among animals exposed to 5 pg Cull were about half those of controls. In these enclos- ures, there was a shift to smaller phytoplankton species. Steele and Frost (1 977) speculate from their simulation models involving Pseudo- ca1anu.s (see p. 209) that this shift in phytoplankton size could have resulted because of depletion of their grazers, largely Pseudocalanus.

    G. Retrospects and prospects

    Although the overall distribution of Pseudocalanm is well docu- mented, we lack knowledge of its precise southern limits in offshore waters in particular. It would also be useful to have more refined information on the status of populations at the fringes of its range: whether they occur year-round or seasonally, in shallow or deep water, breeding or not.

    Pseudocalanus clearly adapts to a wide range of physical and chemi- cal conditions, and it should not be assumed that its geographical limits are set solely by physiological tolerances. We shall show later (Sections IX and X) that temperature has profound effects on size, development rate and reproductive rate, and therefore on population dynamics. It may be that extreme conditions limit a populations resistance to


    predation or ability to compete with other forms before the limits of physiological tolerance are reached.

    Lee and Williamson (1975) quite rightly point out that from their work I selected examples of vertical distributions . . . could be quoted as supporting nearly all the conflicting statements that have been in previous publications on the vertical distribution of P. elongatus . Yet vertical distribution in relation to temperature stratification often figure in such publications, with animals seeming to concentrate in, over, or under thermoclines. This seems to suggest that they may I choose not to enter warmer or colder waters even when this is well within physiological tolerances. Of course temperature is very often correlated with other variables : with salinity gradients, although these often seem slight by comparison ; with food, which may accumulate in or near thermoclines; and indeed with almost anything that varies vertically. We shall later discuss the possible significance of temperature in vertical migration (pp. 175-179).

    Long-term studies of Pseudocalanus and other marine organisms may tell us much about natural and man-caused changes in the bio- sphere (see Glover et al., 1974). The experiments discussed here deal largly with acute responses of Pseudocalanm to pollutants. Eriksson (1973a) has suggested that sex ratios of Pseudocalanus may be distorted in coastal waters by accelerated mortality of females. Steele and Frost (1977) have deduced from their simulation models that stresses like pollution may in general tend to favour small plant cells and therefore smaller copepods like Pseudocalanus. Although speculative, these arguments illustrate the kind of population information that may be required to understand future changes in distribution and abundance of P8eudocalan.u~.


    Pseudocalanus is typical of most crustaceans in that after hatching at an early stage of development it adds successively new segments and appendages.

    Pseudocalanus hatches as a nauplius, which is the most immature larval form among the arthropods. There are six naupliar stages (abbreviated N I-N VI) followed by six copepodid stages (abbreviated c! I--C VI), of which the last (C VI) is the adult.

    It is possible to divide the body from C I onwards into three regions or tagmata according to two different kinds of schemes. The first of these is based on theoretical considerations and we use the three terms,


    head, thorax and abdomen for all stages. The position of the border between thorax and abdomen is arbitrary, and is discussed later.

    The second scheme is practical and is based on the observable shape of the body. We use for the three tagmata of this scheme the terms cephalosome, metasome and urosome.

    N1 1


    N I P

    FIQ. 6. Characters of distal segment of first antenna and posterior end of body used to identify Pseudocalanus nauplii. (From Ogilvie, 1963.)


    A. Embryo

    The embryology of Pseudocalanus has not been investigated, but Corkett (1966) photographed the external features of eggs of Pseudo- &nus. After Marshall and Orr (1955) the following stages of Pseudo- calanw eggs were observed and photographed ; two-cell stage, segmentation-cavity stage, gastrulation stage. This is followed by a period when no detailed structure is visible until the developing nauplius can be seen, which occasionally twitches prior to hatching. The egg membranes are described in a later section (p. 107).

    B. Nauplii

    The naupliar stages I1 to VI of Pseudocalanus are illustrated by Oberg (1906). N I of Oberg (1906) is really N I1 (Ogilvie, 1963). The newly hatched nauplius (N I) is illustrated by Corkett (1968). Keys to the identification of Pseudocalanus nauplii are given by Ogilvie (1953) and Faber (1966). The most useful character for the identification of nauplii is the arrangement of the caudal armature as seen from a ventral view. Figure 5 gives a summary of the characters used in the identifica- tion of the six naupliar stages of Pseudocalanus. Ogilvie (1953) expresses some of these characters in tables useful for discriminating different genera and species.

    The first three naupliar stages contain only three pairs of append- ages, but in N IV the posterior portion of the body has lengthened and the rudiment of the first maxilla has appeared (Oberg, 1906). By the time N VI is reached there are rudiments of thoracic appendages. The appearance of rudiments of segments in N IV, N V, and N VI means they are sensu strict0 metanauplii (Snodgrass, 1956), but the term metanauplius is not normally used and Pseudocalanus is universally referred to as having six naupliar stages.

    C. Copepodids (CI-C V ) 1. Structure

    The basic structure of copepodids (along with adults) is summarized in Table I . The cephalosome is the observable large, anterior division of the body ; it is not divided into observable segments. The metasome consists of those observable segments between the cephalosome and the main body articulation with the urosome. The urosome consists of the narrow observable segments behind the main body articulation.


    TABLE I. NUMBERS AND ARRANGEMENTS OB SEUMENTS AND SWIMMINU FEET IN Pseudocalanus (modifiod after Corkett, 1968)

    No. NO. No. No. No. observable observable observable observable pairs of

    segments segments segments segments feet

    Stage sex thoracic abdominal meta-some urosome swimming

    - I I1 -

    I11 - IV ? IV d V ? V s

    VI (Ad.) 9 VI (Ad.) d

    4b 5 b 6 5 5 5 5 3 4

    l b

    l b

    1 2 2 3 3 3c 4

    2 3 4 4 5 4 5 4 5=

    ~ ~~~~~~~

    Fifth highly modified. After Oberg (1906). Plus genital segment (see text p. 34).

    The basic structure of the five immature copepodid stages are given in Table 1, and we do not repeat all this information below. Corkett (1968, his Table I) used the term segments thoracique libres instead of metasome.

    2. C I This stage has three metasome and two urosome segments as in all

    copepod species (Gurney, 1942). Oberg (1 906) states that in the early copepodid stages the small anterior segment of the urosome was separated from the metasome during moult and therefore belongs to the thorax. We therefore place the border between thorax and abdomen between the first and second urosome segment (Table I). C I has two pairs of swimming feet and the rudiments of the third (Oberg, 1906).

    3. C I I We consider (as in C I ) that the border between the thorax and

    abdomen lies between the first and second urosome segment (Oberg, 1906). C I1 has the rudiments of an additional fourth pair of swimming feet.

    4. C I I I It is not clear where the border between the thorax and abdomen

    lies (either at the main body articulation or between the first and second


    urosome segment), but the latter is likely by analogy with C I , C 11, C V 9, and C VI.

    6. C I V Sexual dimorphism appears at this stage. The fifth pair of swimming

    feet in the male is small and uniramous (Kraefft, 1910). The fourth metasome segment is the result of the fusion of the fourth and fifth thoracic segments, but this fusion is occasionally incomplete. It is again not clear where the border between the thorax and abdomen lies (see above) : probably between the fist and second urosome segments.

    6. C V As above (C IV) the fifth pair of swimming feet in the male is small

    and uniramous (Kraefft, 1910). Here again the fourth metasome seg- ment is the result of the fusion of the fourth and fifth thoracic segments with occasional cases of incomplete fusion as in the C V 8 illustrated in Fig. 1. From the side views of the female urosome of C V in Kraefft (1910) it seems clear to us that the border between thorax and abdomen lies between the first two urosome segments, which are swollen at this stage prior to fusion to form the genital segment in C VI. When young female stages of Pseudocalanus are parasitized, sometimes this fusion does not take place (see p. 194).

    D. Adults (C V I )

    1. Arrangement of somites and appendages into tagmata Within the arthropods somites are grouped into tagmata, such as

    head, thorax, and abdomen. Use of such a term does not necessarily mean that a structure by this name contains the same homologous somites in different groups of Crustacea. In the adult of Pseudocalanus the first thoracic segment is fused with the head (unlike all previous copepodid stages) to form the cephalosome; this leaves three metasome segments (Table I).

    The theoretical and practical arrangements of somites and the names for tagmata useful for adult Pseudocalanus are given in Table I1 and some are illustrated in Fig. 6. Column 1 in Table I1 shows the basic theoretical number of somites which are homologous to those of other Crustacea (Borradaile et al., 1961, their Table 7).

    In column 2 of Table I1 we show the theoretical distribution of somites into the three previously mentioned tagmata. We adopt the position of Owre and Foyo (1967) and consider the maxillipeds as being the last pair of head appendages and for convenience consider the


    1 2 3 4 5 G

    Theoretical Theoretical arrangement Observable tagmala Observable tagmata Appendages somites of somites into tagmata in male. in female

    1 2 3 4 5 6 7 8 9

    10 11 12 13 14 15 16


    1 2 3 4 5 6 1 2 3 4 5 6 1 2 3

    Anal segment



    Abdomen I J


    Metasome fused

    genital segment

    I First ant,enna Second antenna Mandible First maxilla Second maxilla Maxilliped 1st swimming foot J 2nd swimming foot 3rd swimming foot 4th swimming foot 5th swimming foot Genital operculiim ($2)




    Jfused genital segment




    First antenna

    Second antenna


    First maxilla

    Maxii I iped

    First swimming foot

    Second swimming foot thoracic somite

    Third swimming foot thoracic somite

    Fourth and f i f th thoracic sornites Fourth swimming foot

    Genital operculum Genital segment

    (sixth thoracic somite and first abdominal somite)

    Second abdominal somite

    Third abdominal somite

    Fro. 6. Diagrammatic representation of an adult female P8eudocatanus (see Table I1 and text). The abdominal and thoracic somites are numbered in theoretical sequence and the anterior observable tagma is the cephalosome. (After Sam, 1903, and Owre and Foyo, 1967.)

    somite bearing the first antenna as being the first somite, thus giving rise to six head somites. We further adopt the position of Owre and Foyo (1967) and consider the next six somites as belonging to the thorax. Owre and Foyo (1967) state that the abdomen, as defined by them, contains " one to five somites " ; this statement is misleading as there are only four possible somites behind the thorax as they define it. We


    therefore consider the abdomen as containing three somites followed by the telson or anal segment.

    Column 3 shows the well-known sequence of appendages. Columns 4 and 5 show the practical subdivisions of the body for

    both sexes in Pseudocalanus according to the system of Owre and Foyo (1967). The fourth and fifth thoracic somites are fused to form the third metasome segment. In the male the genital segment corresponds to the sixth thoracic somite only. In the female the genital segment is formed by the fusion of the sixth thoracic somite and first abdominal somite. The genital operculum of the genital segment represents rudiments of the sixth thoracic appendages.

    Finally a useful division is the cephalothorax (column 6) which contains all the main body apart from the urosome and is that part of the body measured in biometric studies (cephalothorax length).

    2. Appendages (a) Structure

    With the exception of the first antenna the appendages of the Crustacea may be reduced to one or other of two types : the biramous limb, which in copepods includes the second antenna, mandible, maxilliped and thoracic legs, and the phyllopodium, to which belong the first and second maxillae. For the purpose of this review the two branches of the biramous limbs will be referred to as an internal endo- pod and an external exopod. On the phyllopodium type of limb projections occur and these will be referred to as endites when internal and exites when external. A more detailed account of the structure of copepod limbs is given by Gurney (1931).

    (b) First antenna The first antenna is a structure sui generis. It does not belong to the

    biramous or phyllopodium type and is not comparable in detail with the structure of any other crustacean limbs (Borradaile et al., 1961).

    The first antenna in the Calanoida never has more than 25 segments, and this number is frequently reduced by fusion of segments 1 and 2, 8 and 9 and more often 24 and 25 (Gurney, 1931). Griffiths and Frost (1976) illustrate the first antenna of male and female Pseudomlanus with the female first antenna possessing 23 free segments of which the first and second, eighth and ninth appear fused (Fig. 7B).

    The male first antenna has further fusions of segments especially at the base where there are well developed aesthetes (Fig. 7A). The aesthetes are chemo-sensory in function and are probably used to detect







    ex '


    r l

    FIQ. 7. Appendages of adult Pseudocalamzca. A, first antenna of 3. B, first antenna of 9. C, second antenna of $2. D, mandible of 9. E, first maxilla of 9. F, second maxilla of 9. G, second maxilla of 6. H, maxilliped of 9. I, first left thoracic (swim- ming) leg of ?. J, second left thoracic (swimming) leg of ?. K, fifth pair of thoracic legs of 3. Symbols are: a aesthetes; b blade; en endite; end endopod; ex exite; exp exopod; 11 left leg; rl right leg; s stout seta; sb serrated blade; t teeth. (A and B from Griffiths and Frost, 1976; C, D, E and H from Schnack, 1976; F from Marshall and Om, 1966; G, I, J and K from Sam, 1903.)


    a pheromone produced by freshly moulted females prior to mating (Pa 84).

    (c) Second antenna The second antenna contains an exopod and endopod with well

    developed terminal fans of setae (Fig. 7C). The second antenna is used by Pseudocalanus in locomotion (see p. 52) and in filter feeding (see p. 54).

    (d) Mandible The mandible consists of a blade used for mastication of the food

    (the morphology of the blade is considered in connection with feeding mechanism, see p. 57). On the mandibular blade is situated a biramous palp (Fig. 7D) which is used with the second antenna to create water currents used in locomotion and feeding.

    (e) Pirst maxilla The first maxilla is a flattened phyllopodiuin type of appendage

    with a well developed endite and exite that play a part in feeding (Fig. 7E). The long flexible setae on the exite help maintain the feeding current (see p. 54) and the teeth on the endite (or gnathobase) are used to comb food from the setae and setules of the second maxilla before the food is passed to the mouth.

    (f) Second maxilla The second maxilla (Fig. 7F) is the appendage used to filter food

    from the feeding current. This phyllopodinm type of appendage has a number of endites with well developed setae on which are situated setules. The arrangement of setae and setules and their use in filter feeding is considered later (p. 54) as is the possible use of the terminal " stout seta " (p. 58).

    The second maxilla in the adult male is vestigial (Fig. 7G) showing that filter feeding cannot take place in the adult of this sex.

    (g) Maxilliped The maxilliped consists of a single endopod (Fig. 7H) with well

    developed setae. The setation is not reduced, unlike that found in carnivorous copepods (Anraku and Omori, 1963 ; Arashkevich, 1969 ; Schnack, 1975). Rotation of the maxillipeds is used to enhance the feeding eddies (see p. 54).


    (h) Thoracic appendages The first four thoracic appendages or swimming feet are flattened

    biramous appendages (Fig. 71, J) probably used in the escape reaction to avoid predators (see p. 53). It is possible the shape of these appen- dages are responsible for the name copepod ( K W T ~ , oar ; TOVS, foot), a name first used by Milne-Edwards in 1830 (Russell, 1934). The exopod on the second, third and fourth swimming feet of the female has a terminal serrated blade (Fig. 7J). The adult female has no fifth thoracic legs but the adult male has a highly modified fifth pair of legs consisting of a three-segmented right leg, and a five-segmented left. Sam illustration (Fig. 7K) hints at fusion of two segments in the first basal segment of the right leg.

    E . Retrospects and prospects Although its external anatomy can be satisfactorily described in

    general terms, little is known of details that might serve to separate different kinds of Pseudocalanus (see Section 11). Furthermore, virtually nothing is known (except by inference) about the internal structure of Pseudocalanus.

    For purposes of description and exposition, we have found it useful to compare theoretical and practical arrangements of the series of segments and appendages (Table 11). There is still considerable con- fusion in published accounts of such series, and we hope our approach will find more general use among copepodologists and others.

    Future work on the morphology of Pseudocabnus in relation to function should certainly include studies of the fine structure of the first antenna1 aesthetes with which males are so richly endowed. It would also be useful to have insights into the ways in which the fifth legs of the males function in mating.


    Respiration of Pseudocalanus has been quite extensively docu- mented, generally as one of a number of forms in comparative studies. The ultimate aim of such studies has generally been to supply one component of the balance equation of growth or production (see p. 181). Respiration is measured as oxygen consumption. Little appears to have been done using more biochemical approaches to metabolic rate, although Muhammad (1965) has demonstrated a strong correlation between oxygen consumption and succinic dehydrogenase activity in a variety of mixed zooplankton, including Pseudocalanus.


    A. Factors injuencing rate of oxygen consumption

    Our survey of the determinants of respiration rate deals with variables that are expected to be important in nature. Little appears to have been done on certain more methodological questions. Pavlova (1975) has shown that degree of crowding may be important in Pseudocalanus. Rates of 0, consumption (means & 95% c.1. in pg/cop./h) by un- crowded (3-4 cop./l6 ml) adults were 0.225 f 0.032 for males and 0.190 f 0.223 for females; for crowded (10-12 cop./l5 ml) adults, they were 0.092 & 0.030 and 0.086 f 0.037 respectively. Generally speak- ing, however, authors have standardized such matters for comparisons between experiments.

    1. Body size Conover (1959) was evidently the first to include PseudocaZanzcs

    in a relationship between rate of oxygen consumption (R, in p.1 O,/cop./ day) and body weight (W, in mg dry wt) for a number of copepod species:

    Log R = 2.068 + 0.856 log W. The relationship for four experiments using adult female Pseudocabnus alone, with a length range of 0-80-0.91 mm, at 20C (probably an exces- sive temperature for the animaIs from Southampton, England), gave a regression coefficient of 0.433 which was less reliable than the value of 0.856 for all species (see above).

    Because weight of an organism may be variously made up of meta- bolically inactive material, such as stored oil, ripe ova (as opposed to rapidly growing oocytes) or gut contents, cephalothorax length might be a better predictor of respiration rate of like-shaped animals. Raymont (1959) assumed that respiration followed a " surface law ", and that it would be proportional to the square of length, and therefore corrected respiration rates of copepods accordingly. However, within the size range of Pseudocalanus used by him (adults of both sexes 0-94-1.13 mm) no correlation of respiration rate and length was noted. Conover (1959) fitted a relationship of respiration rate (R, as above) to cephalothorax length (L, in mm) for a variety of copepods:

    log R = 0.353 + 2.713 log L. The less reliable regression coefficient for PseucEocalanus alone was 1.645. We do not have data for respiration of nauplii and copepodids of Pseudocalanus from which to derive an intraspecific relationship, and such experiments as conducted by Conover (1959) demonstrate that i t is difficult to use adults or copepodids of a narrow size range to derive an accurate relationship between respiration and body size of


    Pseudocalanus. It is better to use a general, interspecific relationship, making use of a wide size range of animals. Probably the best available interspecific relationship to date is that fitted by Ikeda (1974) to " boreal " zooplankton, including Pseudocalanus:

    log R = 1.437 + 0.783 log W. Again R is pl O,/cop./day and W is dry wt in mg. We can transform this for cephalothorax length (L in mm) by using the length-weight relationship given on p. 127.

    The mean habitat temperature for the " boreal " species in this relation- ship was 8.6"C and, although Ikeda (1974) did not attempt to correct for experimental temperature, most of his respiration rates were determined at temperatures close to this habitat temperature. The literature provides a few estimates for temperatures near 8.6"C of respiration rates of Pseudocalanus of known weights or lengths (Table 111). Agreement with the rates predicted from Ikeda's equation is quite good, with the overall mean of predicted values about 5% higher than that observed.

    Polyakova and Perueva (1976) give another series of respiration values a t 8.5 and 10C. Unfortunately, they give total lengths and wet weights of their animals. Using the conversion factor of dry wt = 0.15 wet wt, which they use to transform dry weights in Conover (1969) to

    log R = 2.850 log L - 0.070.


    Experimental Size Respiration, p~o,lcop.lday Source temperature ___

    "0 mm pg dry wt Obeerved Predicted

    8 29.6a 1.61 1.73 Anraku (1964b) 8 26-7a 1.25 1.61 Anraku (1964b) 8 14.Sa 0.41 1.00 Anraku (1964b) 8 13.7= 0.55 0.96 Anraku (1964b)

    N 6-8 13.5 0.94 0.94 Ikeda (1974) N 6.8 13.3 0.79 0.94 Ikeda (1974)

    N 11.2 12.0 1.12 0.86 Ikeda (1970)

    10 0.98 1.56 0.80 Marshall and Om

    10 0.87 0.74 0.67 Marshall and On: (1966)


    Estimated from graph.


    wet weights tabulated by them, we find that their observed values of R in p1 O,/cop./day (ten estimates) average 22% lower than those predicted from Ikeda's equation.

    2. Temperature Evidently only Anraku (1 96413) has systematically examined

    effects of temperature on respiration rates of Pseudocalanus (Fig. 8). Animals were kept at experimental temperatures for 24 h before 0, consumption was measured. Clearly temperature has the usual positive

    Temperature ("C)

    Fro. 8. Respiration at different seasons of adult female Pseudocalanus from near Cape Cod, Massachusetts, expressed per copepod and per unit dry weight. Approximate habitat temperatures are shown as H on each curve in the righthand graph. (After Anraku, 1964b.)

    effect a t the lower end of the temperature scale, and use of rateldry wt appears to give more comparable results. It is worth noting, as well, that Raymont's (1959) estimates for both sexes of Pseudocalanus from Woods Hole a t 15" in April-May (mean 2.45 p1 O,/cop./day) were similar to those found by Anraku in the same locality and season some years later (ca. 1.9 p1 O,/cop./day, from Fig. 8). However, Raymont's cope- pods averaged 0.99 mm in length, or about 11-5 pg dry wt (from equa- tion p. 127), so that respiration on a per weight basis was about 200 pl O,/mgldryLwt/day, which is much in excess of that found by Anraku (ca. 75 p1 O,/mg dry wt/day, from Fig. 8). The dry weights of the copepods used by Anraku can be deduced from Fig. 8 to be about 27 pg in May, which seems excessively large for lean animals (p. 127), and they may have had much stored oil. For these reasons we believe that


    Anrakus results can only be used in a relative way for comparisons of temperature response.

    There are obvious seasonal differences in temperature response (Fig. 8). In the cool months (February and December) rates were lower at 22.5 than at 15C) so that the animals were beyond the optimum ) a t the highest temperature. On the other hand, rates at the lower temperatures were inversely related to habitat temperature (indicated by H in Fig. 8) ; that is, copepods taken in cooler waters were better able to maintain high respiration rates at cold temperatures in the laboratory. Anraku describes such seasonal differences in terms of lower Qlo (ca. 1.3 in Feb. and 1.7 in Dec., v. 3.7 in Aug.) for copepods from the cooler months, but this is merely descriptive of the higher rates at lower temperatures in the monotonic parts of the curves on Fig. 8. The differences between seasons may have resulted from long- term acclimation (i.e., reversible changes in physiology or activity that take longer than the 24-h adjustment period used by Anraku). Differences could also have resulted from permanent developmental differences between cold-water and warm-water generations (in the manner of size, see p. 116), or even from genetic differences (cf. Bradley, 1975).

    Whatever the cause of seasonal differences, we may agree with Anraku (196413) that his results indicate an adaptation to cold by Pseudocalanus. This may lead to maintenance of similar respiration rates in nature regardless of season. Anraku tabulates habitat tempera- tures of 7-1, 14.1, and 6.7C for animals collected in May, August, and September respectively, and we assume 2C for February. At these temperatures the weight-specific respiration rates were quite similar (- 38-60 pl O,/dry wt/day ; Fig. 8).

    The falling off a t high temperatures of respiration for animals collected in the cooler months may be more pathological than physio- logical, and is of little interest in the context of natural conditions. Anraku (196413) noted that animals died or behaved abnormally a t 22.5C even in August, and that Pseudocalanus disappeared from the Woods Hole region when temperatures were above 20C (see p. 24). Raymont (1959) found, in experiments conducted on the adults of both sexes, an elevated respiration in Pseudocabnus from Woods Hole in April-May in one experiment a t 20C compared with the mean rate of several experiments a t 15C. However, he noted that repeated runs showed a drop in the rate at 20C. Conover (1959) estimated that at 20C adult female Pseudocalanus from Southampton respired 196-256 (mean 234) p1 O,/mg dry wt/day, much in excess of the rate for Woods f Hole (Fig. 8). Conovers experiments were short-term (4-8 h) and his


    animals may not have become physiologically damaged while those of Anraku were 24 h in duration. However, Conovers results may also have had little relevance for natural conditions, since habitat tempera- tures a t the time of his study were said to be 11.5OC.

    3. Light Although light could influence the activity and therefore oxygen

    consumption of copepods, only Pavlova (1975) appears to have examined its effect on adult Pseudocalanus from the Black Sea. She standardized animal sizes and degree of crowding for experiments being compared. Rates of oxygen consumption (means f 95% c.1. in pg/cop./h) by males at 3 cop./l5 ml were 0.101 f 0.078 in the dark and 0.450 f 0.351 in diffuse light ; for males at 4 cop./l5 ml, rates were 0.360 & 0.181 in the dark and 0.710 f 0.425 in diffuse light; for females a t 4 cop./l5 ml, rates were 0.190 f 0.118 in the dark and 0.490 f 0.380 in diffuse light.

    Thus it appears that respiration is higher (and more variable) in the light. The animals may simply be more active, trying to escape light conditions that obtain by day near the surface (see Section XII). Pavlova (1975) found that respiration rates of females suspended by day in containers at depths of 50-100 m in the sea were similar to rates in the dark in the laboratory. Unfortunately, containers were larger, animals more crowded, and temperatures considerably lower than those of laboratory experiments, so we do not feel that her results give a meaningful indication of the natural rates obtaining under very low light levels.

    B. Respiration and food requirements

    Anraku (1964b), Marshall and Orr (1966), and Hargrave and Geen (1970) have calculated minimum food requirements or proportions of food used for respiration by Pseudocalanus. Some of these experiments were with feeding animals, others with starved animals, and it may be noted parenthetically that Raymont (1959) found no significant difference between the results of two experiments with unfed and seven with fed Pseudocalnnus. In view of the variability of conditions and results, we do not feel it worthwhile to list the food requirements calcu- lated by the above authors, nor to convert other individual respiration estimates. Furthermore, we feel that caIculations that use RQ values for carbohydrate, fat, and protein separately or in some chosen mixture give an unwarranted air of precision. Instead, we shall here assume an RQ of 1, so that 1 pg of dry body tissue or food requires 1 pl of 0, to be


    metabolized. If we take Ikeda's (1974) formula (p. 39) as an adequate predictor of 0, consumption, and assume a seasonal temperature com- pensation (as implied in Fig. 8) then minimal food (F) expressed as a percentage of body weight (W in mg) can be given by :

    log F = 0.437 - 0.217 log W.

    An adult copepod of 10 pg might thus need about 7% of its weight daily as food to compensate for respiration, while a nauplius of 1 pg might need about 12%.

    C . Retrospects and prospects

    No doubt much has been left undone in the study of respiration of Pseudocalanus. Nothing appears to be known of the effects of salinity, oxygen tension, and other such variables. Studies of the effects of food concentration deserve expanding, and the effects of temperature and light have not been fully explored. We feel that the use of dry weight as a measure of size has made it difficult to compare results from different seasons and localities, and make a plea for use of a better measure of metabolic size, perhaps length. However, whatever measure- ments might be made, the experimental violence done to such tiny animals by crowding them into small volumes of sea water and perhaps forcing them to be abnormally active may make any results somewhat unnatural.

    Our conclusion that respiration might involve expenditures of the order of 10% of body weight each day might not be worth refining through further respiration measurements. It is possible that weight losses can be determined more directly in starving animals, or perhaps by reductions in the size of the oil store (see p. 129). If the strategy of respiration studies is to forge links between food availability, growth, and production, then this can probably be done more directly without use of a " balance-equation " approach (see p. 132).


    Excretion has been extensively studied in zooplankton, including copepods. Although excretion may be of interest as a phenomenon in its own right, there have been two main strategies in such studies : (1) rates of excretion supply one component in the " balance equation " of growth or production, and (2) excretion supplies nutrients to phyto- plankton. The elements of interest in excretion are nitrogen and phosphorus.


    A. Nitrogen

    Although amino acids and especially urea are produced by copepods, the current view (Conover, in press; Smith, 1975; Ikeda, 1974) is that NH, is the predominant form of excreted nitrogen by non-feeding copepods. Only NH, excretion has been measured in Pseudocalanus. Butler et al. (1969) and Ikeda (1974) have made a few measurements, but Christiansen (1968) has made extensive analyses of NH, excretion by Pseu,docaZanus from Bras dOr Lake, a landlocked arm of the Atlantic in Nova Scotia. Some of the factors influencing NH, excretion are of interest in the context of experimental design, but of little significance in nature. We will detail some of these methodological matters first, since Christiansens (1968) work is not readily available.

    1. Methodology Christiansen (1 968) determined concentrations of NH, coloro-

    metrically, standardizing to a salinity of 25%,. It is important to realize that, unlike for respiration experiments, food conditions during the experiment are of crucial importance. It is expected that a copepod that is feeding or has a gut full of food would excrete a t a higher rate than a copepod that was not fed and had an empty gut, both because of increased metabolic production of waste products and because the methods used to measure excretion may include the leaching of un- assimilated nutrients from faeces. Christiansen (1 968) placed actively swimming animals in unfiltered sea water (containing any food present in nature) in 140 or 450 ml bottles during the experimental period when excretion rates were measured. Ikeda (1974) kept his animals in natural raw sea water for one day prior to the experiment and then placed animals in filtered sea water during the experimental period. He even removed faecal pellets produced during the experimental period in an effort to measure basal levels of excretion. Size of bottle was found by Christiansen to have no significant effect on excretion rate separate from the effect of concentration of copepods (see below). Experimental and control bottles were placed on plankton wheels in the dark at controlled temperatures.

    Experiments with antibiotics and mixtures of copepodids of Temora longicornis and Pseudocalanus indicated no significant effect of bacteria in experiments lasting up to 14 h a t 2C. Christiansen concludes that corrections for bacterial uptake of NH, are unimportant in short-term experiments, a t least.

    Crowding of animals had a powerful effect on reducing production of NH,. Unspecified mixtures of copepodids of T . longicornis and


    Pseudocalanus were used to demonstrate this. Copepods were placed in 450 ml containers at concentrations from 50 to 600 per container. This crowding effect is most likely an artifact of experimental conditions and is discussed in more detail below. The log-log regression given by Christiansen for the relationship had a regression coefficient of -1.04 which was close to unity (P < 0-001). A regression coefficient of unity would mean an inverse proportional relationship which clearly cannot apply to very low concentrations of copepods since it would imply indehitely high excretion rates.

    Excretion rate also declined more or less exponentially with time in experiments with mixed copepodids in unfiltered seawater, so that rates were about five times as high at 2 h after the commencement of experiments compared with 12 h later.

    Although Christiansen ( 1968) suggested that quiescence and perhaps metabolic shifts would explain reductions in excretion rates, both when the copepods were crowded and when experiments were conducted over longer periods of time, he also concluded that food may become depleted in the darkened bottles. The importance of behavioural quiescence was not supported by his demonstration that excretion rates of C V Pseudocalanus (20 cop./l30 ml) were unaffected by different amounts of time animals were kept prior to the conduct of experiments. We conclude that experiments with fed animals under crowded conditions and of long duration are likely to give reduced excretion rates due to depletion of food. We can therefore readily agree with Christiansen that short term (2-4 h) experiments with uncrowded (


    and for several stages of Psezldocalanus. The interspecific and intra- specific relationships were very similar (Fig. 9). The regression coeffi- cients of near unity imply that excretion rate per individual is virtually the same for a tiny nauplius (about 0.6 pg in Fig. 9) and a full-grown

    NP-PI \

    Ooo 1 \ ,a sirnilis \

    - I

    log E = O

    ti 1-u

    ,066 -

    20 t- \ \




    G u 0.001 0-01 (

    Mg dry wt . (W)

    FIQ. 9. Weight-specific excretion rate for adults of different species of copepods (open circles, broken line) and for different stages of Pseudocalanw (closed circles, un- broken lines). (After Christiansen, 1968, who included in his analysis the point for Calanus Jinnaarchicus from Corner ct al., 1966.)

    adult (ca. 14 pg): about 0.68 and 0.86 pg NH,-N/individual/day res- pectively. This is hardly likely to be a natural state of affairs. We suggest that this anomalous finding of Christiansen ; t ~ well as similar results in Corner et al. (1965, their Table 4) are related to the crowding effect described earlier (p. 45). The crowding effect was inversely related to excretion and gave a log-log regression coefficient close to unity, like the effect of body weight. The effect of crowding together numbers of animals of a given biomass may have the same effect in


    reducing excretion rate (through depletion of food or whatever mech- anisms) as occurs when the biomass of individuals increases and the numbers are held constant, sts in Fig. 9.

    Rather than attempting to correct for the crowding effect in the relationship between excretion rate and body size, we turn to the work of Ikeda (1974), who fitted the following expression to non-feeding " boreal " zooplankton (terms as in Fig. 9) :

    log E = 0.182 - 0.21 log W. This expression (which includes values for Pseudocalanus) gives an excretion rate for a 14 pg animal (full-grown adult) of 0.052 pg NH,- N/individual/day and for a 0.6 pg animal (nauplius) of 0.004 pg NH,- N/individual/day. Since Ikeda (1974) measured excretion by unfed animals we would expect these values to be lower than those calculated from Christiansen (Fig. 9). More important, however, is the fact that the excretion rate calculated from Ikeda (1974) for the biomass of a nauplius is an order of magnitude smaller than that calculated for an adult. This seems to us to be a more realistic result although we are fully aware that it has yet to be demonstrated that extrapolation may be made from the interspecific relationship of Ikeda to the intra- specific relationship implied in the above calculations.

    4. EfSect of temperature Unfortunately, Christiansen (1968) once again used mixtures of

    copepodids of Temora longicornis and Pseudocalanus to test effects of temperature (T, in "C) on excretion rates (E, in pg NH,-N/cop./day) a t varied densities (C, in No./450 ml) :

    log E = -1.59 - 0.585 log C + 0.0137 T. Effects of crowding (C) and temperature (T) were highly significant ( P < 0.001) and the use of a multiple regression enables the effect of temperature on the release of nitrogen to be determined after the effect of crowding has been removed. The regression coefficient of 0.0137 implies that, whatever the density, a 10C rise in temperature will increase the excretion by 37%, i.e. a low Qlo of 1.37. Support for this low Qlo comes from the work of Ikeda (1974) who gave measure- ments of excretion rates by non-feeding Pseudocalanus in two experi- ments a t about 7C (4-3 and 5.0 pg NH,-N/mg dry wt/day) and one experiment at 12C (4.1 pg), again implying a low Qlo. Nival et al. (1974) also suggest that a low Qlo of excretion rate for non-feeding copepods is characteristic.


    5. Effect of salinity Christiansen (1968) again used mixtures of copepodids of T.

    longicornis and Pseudocalanus at 10C to test the effect of salinity on excretion rates at varied densities. Christiansen gives a multiple regression in which both crowding ( P < 0.001) and salinity (P < 0.01) are highly significant. Unlike temperature the effect of salinity was found to be quite pronounced, doubling the rate of excretion between lo%, and 32%,. Excretion in the more euryhaline Acartia tonsa was not significantly affected by salinity. Presumably the acute effect shown by Christiansen could have some importance in highly stratified waters, but acclimation or adaptation may well occur in persistently brackish waters occupied by Pseudocalanus.

    6. Effect of oxygen concentration As already noted (p. 25), Pseudocalanus can be found at very low

    oxygen concentrations in nature. Christiansen (1 968) carried out 4-h experiments at 10C with C V Pseudocalanus, 20 cop./l30 ml a t 20 different oxygen concentrations between 1.3 and 6.9 ml 02/l.

    The effect of excretion rate was we11 fitted by a negative exponential expression (exponent N -0.3) such that there was an approximate doubling of the rate at 1 ml O,/I compared with that near 0, saturation.

    7. Nitrogen requirements We suggest elsewhere that a value of 7% N might be found in

    lean Pseudocalanus and discuss the possibility that even higher values in Christiansen (1968) may include gut contents (p. 126).

    Christiansens equations (Fig. 9) suggest that a feeding adult animal of 10 pg dry wt might excrete about 0.8 pg of NH,-N daily (and perhaps more as organic N). If we assume that its food is also 7% N by dry weight, this implies a production of NH,-N in excreta (and possibly leached from faeces) in excess of the body nitrogen per day. This is a higher value than any listed by Corner and Davies (1971, Table VIII). However, it may be reasonable, as rations of up to 140% of body weight per day have been observed (Paffenhbfer and Harris, 1976, see p. 63).

    Ikedas (1974) formula for non-feeding animals gives a better indication of basal requirements, indicating that an adult Pseudo- calanus (10 pg) might excrete about 0.040 pg NH,-N/day, or about 5.6% of its N content (if N is 7% of dry wt). This estimate agrees with that of Butler et al. (1969), who found that mixed small copepods (in fact over 90% C I V and C V Pseudocalanus) in filtered seawater


    excreted (mean and 95% c.1.) 3.98 & 0.61 pg NH,-N/mg dry wtlday. Mean dry weight was 11.7 pg, and contained 7.8% N, so that this rate represents about 5% of body nitrogen per day.

    B . Phosphorus Hargrave (1966) and Hargrave and Geen (1968) present information

    on phosphorus excretion by Pseudocalanus from Bras dOr Lake, Nova Scotia. Both dissolved inorganic phosphorus (DIP) and dissolved organic phosphorus (DOP) were measured. Again we deal briefly with methodology to the extent that it may influence whether the estimates being sought are representative of those occurring in nature. As was the case for excretion of NH,, food conditions in these experiments are important and again may be implicated (although the evidence is less complete) in reducing DIP under crowded conditions and in experiments of long duration. Unfortunately, the authors did not consider Pseudo- calanua in all their experiments.

    1. Methodology Hargrave (1966) showed that both DIP and DOP declined sig-

    nificantly in brackish water without zooplankton held for 24 h in the dark. Thus it is not surprising that both DIP and DOP increased more in laboratory experiments with copepods when antibiotics were added, which they were routinely.

    About 67% of dissolved phosphorus was DOP in one set of experi- ments with C V and adult Pseudocalanus described by Hargrave and Geen (1968). Thus measurements of DIP alone (which was the measure- ment usually made in experiments) should be corrected if they are to be used as estimates of rate of release of total dissolved phosphorus.

    Copepodids of Temora longicornis and Pseudocalanus in experiments with unfiltered seawater were observed to concentrate in the lower half of unstirred experimental bottles and produced significantly less ( .P < 0.05) DIP than did those in stirred bottles (Hargrave and Geen, 1968). However, no direct measurements of the effect of crowding were made.

    Hargrave (1966) also found significant declines in production of DIP after about 10 h in unfiltered seawater by a mixture of copepodids of T . longicornis and Pseuducalanua. However, the high temperatures (18-20C) in the experiment could have been a factor.

    2. Effect of food concentration Mixed copepodids of T . longicornis and Pseudocalanus released

    significantly less DIP in membrane-filtered seawater than in natural sea A.M.B.--15 4


    water at in situ temperatures. Means, 95% c.I., and ranges in pg DIP/cop./day were : 0.0075 f 0.0007 (0-0030-0.0160) and 0.0210 f 0.0055 (0.01 11-0.0551) respectively (data from Hargrave, 1966). The former may be taken as a non-feeding excretion rate.

    Hargrave also showed that release by copepodids of Pseudocalanus of DIP and DOP was reduced by passage of the medium through filters of different pore sizes smaller than 3-5 pm. These presumably removed food which can be used by Pseudocalanus (see p. 63). Cope- podid concentrations (650-1 000/1) and temperatures (1 7-1 9C) were rather high in these experiments.

    3. Effect of body weight Hargrave and Geen (1968) include Pseudocalanus in a graph of rate

    of DIP excretion (E, in pg DIP/mg dry wt/day) as a function of body size (W, in mg dry wt) for nine species which can be written from Hargrave (1966) as :

    log E = -0.663 - 0.296 log W.

    The authors do not state whether filtered water was used or not, but the rate predicted from this equation for a 10 pg Pseudocalanus is 0.0085 pg DIP/cop./day, which is close to the non-feeding rate (0.0075 pg DIP/cop./day) noted above. Certainly the larger animals (Mysis, Gummarus, Crungon) in their regression could not have been feeding much from the sea water. We take it that the regression illustrated by Hargrave and Geen represents some sort of physiological relationship uninfluenced by much faecal production. TO support this, Hargrave (1966) shows a close proportionality between oxygen uptake and phosphoros excretion by seven of the nine species used in the regression of DIP excretion on size.

    4. Effect of salinity No significant correlation was found between excretion rate and

    salinity of a mixture of copepods, including Pseudocalanus, from Bras dOr Lake (Hargrave, 1966). However, details of the experiment and results are not given.

    5 . Phosphorus requirements Hargrave ( 1966) conducted experiments on non-feeding copepodids

    or Pseudocalanus with empty guts. By including direct estimates of loss of body P, he calculated that 18.2% of total body phosphorus could be released as faecal particulate P per day. In addition the copepodids released some 7.7% of total body phosphorus per day in dissolved form


    (DIP and DOP). This estimate agrees with that of Butler et al. (1969) who calculated the excretion of total P in membrane filtered water, They found that " mixed small zooplankton " (almost all Pseudo- calanus) excreted (mean f 95% c.1.) 0.77 & 0.07 pg P/mg dry wt/day. Their animals weighed about 11.7 pg each and were 0.61% P, so that about 11 % of their body P was excreted daily.

    The regression of DIP on body weight suggests that higher values may be attained by feeding Pseudocalanus. Assuming (from the inter- specific relationship of Hargrave and Geen; see p. 50) that a 10 pg Paeudoealanus, containing 0 . 6 1 ~ 0 P, produces 0.0085 pg DIP per day, this will be about 14% of the body Plday. This could be as little as one- third of the total dissolved P produced, since DOP was not measured (see methodology, p. 49).

    C. Retrospects and prospects The evidence seems clear in these studies on Pseudocalanus that

    " starvation ') rates of excretion are much lower than excretion rates found during feeding. Experimental and technical difficulties of work- ing with a tiny animal under fed conditions make it unlikely, in our opinion, that precise estimates of excretion rates can be obtained that are representative of those found in nature. Moreover, the role of such an animal in replenishing nutrients probably depends as much on system qualities of the animal's environment-the amounts and kinds of food available-as on the character of the excreting animal.

    If basal excretion estimates are required it is probably better for purposes of calculation to assume general functions of the sort derived by Ikeda (1974) relating body size, temperature, and excretion rate of different species, rather than to try and estimate such rates directly with such a small animal as Pseudocalunus.

    While there have been attempts t o use excretion rates in balance equations of growth of copepods (e.g., Corner and Davies, 1971), the most that can be said for the rates available for Pseudocalanus is that they are compatible with feeding rates and with the direct and accurate estimates of growth rate that can be made (see p. 132).

    Altogether, we conclude that further detailed studies of excretion in Pseudocalanus might be of intrinsic interest, but would have little strategic value for biological oceanography.

    VII. LOCOMOTION A. Routine swimming

    Gauld (1966) examined several genera of calanoids, including Pseudocalanus, and observed that they usually swim in a smooth,


    gliding fashion, using principally the second antennae for propulsion, in the manner described by Lowndes (1935). Urry (1964) used strobo- scopic illumination to determine that the second antennae of adult Pseudocalanus vibrated at 1 890-2 580 cycles/min, a rate considerably higher than the 1 200 cycles/min reported for Calanus by Lowndes (1935).

    The movement of the second antennae in copepods is complicated (Gauld, 1966), but evidently the endopod provides propulsion when the exopod is in a recovery stroke and vice versa, so that continuous propulsion is maintained. Giesbrecht (1 882) illustrates the second antennae of both male and female Pseudocalanus. The setae of the male

    f ? 1


    J I cm

    FIQ. 10. Swimming excursions of adult female Pseudocalanus during seven-second paths. The sequences of positions (each straight portion an excursion) from which the scatter diagrams were based are shown on a reduced scale on the right. Each excur- sion (dot on graph) is plotted as an absolute value, and the average horizontal and vertical components of movement are given by dark bars on the axes. (After Anderson, 1974.)

    are longer than those of the female and completely setulated, suggesting a more efficient swimming potential, which is probably used in hunting for a mate during the short life of an adult male.

    In addition to the second antennae, the mandibular palps are involved. The palps rotate a t their base, presumably to reduce resistance on the recovery stroke, since Gauld (1966) states that the effective thrust must be mainly during the backward stroke of the palps. The action of these two pairs of appendages gives the slow gliding motion and in producing this forward motion also creates a broad, U-shaped vortex or swimming swirl (this should not be confused with the feeding current, p. 54).


    Cushing (1959) uses a calculated 24-h swimming rate for Pseudo- calanus of about 0.2 cmlsec but this is based on slender data.

    Anderson ( 1974) has analysed the routine swimming of Pseudocalanus in spatial terms. He observed that, although it occasionally swims in loops (see mating, p. 84, for a possible explanation), its undisturbed movement is usually similar t o the " hop-and-sink " motion described by Bainbridge (1952) for Calanus. Periods of vertical ascent often alternate with periods of passive sinking. I n photographic records of this motion, this appears as " J "-shaped paths (Fig. 10). Anderson analysed photographs of swimming Pseudocalanus to measure the vertical and horizontal component of each straight excursion during seven-second paths. The horizontal displacement was assumed to be equally distributed in all directions. The distribution of the vertical and horizontal components of velocity is summarized on Fig. 10. The vertical component of 0.061 & 0.010 cm/s considerably exceeds the horizontal component of 0.031 f 0.006 cm/s (means f 95% c.1.). This confirms in a quantitative way the " hop-and-sink " motion.

    B. Escape reaction

    As Gauld (1 966) pointed out, most calanoid copepods, including Pseudocalanus, can make large leaps or jerks to avoid contact or capture. Rapid movement makes it difficult t o see exactly what limb movements are involved, but there seems little doubt that the swim- ming feet in particular are brought into play.

    Although Anderson (1974) does not describe an escape reaction for Pseudocalanus he postulates that its small-scale motion, doubling back on itself vertically, makes it less vulnerable to predation by ctenophores than are some of the other species of copepods he studied.

    C. Retrospects and prospects

    Slow swimming is reasonably well understood, but it would be useful to clarify the mechanism used in the escape reaction. Perhaps more important would be a hydrodynamic study of the sort that have tentatively been developed for other species of copepods. Certainly the work of Anderson (1974) implies that the routine swimming rates could be readily documented, and it would be of some value in con- nection with " energy-balance " approaches t o growth and production (p. 181) to estimate the energetic costs of such motion.



    A. Feediny mechanism 1. Filter feeding (a) Feeding current

    Esterley (1916) and Cannon (1928) have given an account of the feeding current in Calanus and Gauld (1966) confirmed that these observations on the way particles are filtered and ingested in Calanus also apply to Pseudocalanus.

    The feeding current is primarily a pair of eddies flowing round the bases of the maxillipeds. The pair of eddies are formed from the swimming swirl or vortex and are enhanced by the rotation of the maxilliped and by the movement of the f i s t maxilla. The exite on the first maxilla carries long flexible setae (Fig. 7E) which suck water forward through the setae of the second maxilla and then sweep it away outwards.

    (b) Filtration The setae and setules on the second maxilla (Fig. 7F) are used to

    filter food organisms from the feeding current. The second maxilla in female Pseudocalanus has been studied in detail by Schnack (1975).

    We are interested in three basic measurements : (1) length of setae, (2) length of setules, and (3) distance between setules; and how these measurements vary for: (a) different setae along the maxilla, (b) different setules along a given sets, and (c) different seasons of the year.

    The length of the setae along the second maxilla showed no general trend to increase or decrease, but varied in length from about 90 pm to 110 pm with a few smaller setae of 50 pm (Schnack, 1975).

    The length of the setules varies both among and on setae and Schnack (1975, her Appendix B) showed that setule length varied from 3.0 to 9.0 pm on a few selected setae.


    Position 95% c.1. Average distan,ce

    between setules (pm) Month

    tip December 1970 8.2 7.9-8.5 6'7-7.2 tip July 1971 7.0

    base December 1970 4.0 3.8-4.1 base July 1971 3.0 2.8-3.1


    The distance between setules varied both for different setae along the second maxilla and for different positions along given setae. At the base of the appendage the setules on the seta were closer together than at the tip (Table IV).

    Seasonal variation is also encountered and the average distance between setules in July is significantly smaller than that found in December (Table IV). We suggest that this is related to seasonal variation in body size in response to temperature (p. 116). Schnack (1975) considered the minimum distance between setules in female Pseudocalanus to be 3.0 pm (95% c.1. 2.8-3.1) which was the smallest value in the seven species she studied, leading her to conclude that Pseudocalanus was specialized for filter feeding and therefore essentially a herbivore. The detailed measurements on the second maxilla are not easily used to reconstruct an effective mesh size to determine the efficiency of removal of small food organisms, since the mesh size must vary with the distance between setae. This distance must vary with position of the second maxillae, presumably under control of the animal. However, the means of distances between setules on setae from about 3 to 8 pm (Table IV), do suggest that Pseudocalanus would be more efficient in filtering particles larger than about 8 pm.

    Poulet (1977) tabulates differences in number of setae, size and vibra- tion rates of feeding appendages of adult female and C I11 animals. He also calculates the hypothetical volume swept by the stroke of these appendages. Naturally enough, relative mesh size (number of setae per appendage length) is smaller, vibration rate of appendages faster, and the hypothetical volume swept by each appendage is smaller among younger animals. Although these data do not give direct estimates of minimal sizes of potential food (see above) they show clearly that younger animals could secure smaller food particles more efficiently.

    Once food particles have been filtered from the feeding current by the second maxilla the particles are combed off the setae and setules of the second maxilla by the teeth on the endite of the first maxilla (Fig. 7E) and passed to the mouth.

    (c) Mastication Before food particles are passed through the mouth into the oeso-

    phagus they undergo mastication by the mandibular blades. Anraliu and Omori (1963) found that filter-feeding copepods had short and rounded teeth whereas predatory copepods had teeth that were few and pointed. Petipa (1 975), in a recent study of the origin and classification of feeding types of calanoid copepods, suggests that the ( ( Pseudo- calanus type can be derived by reduction of the masticatory function

  • B FIG. 11. Scanning electron micrographs of the right adult female mandible of Pseudo-

    cnlanus. A, chewing surface. B, detail of dorsal teeth. Symbols are; c1-c4, central teeth; cli, diastema; d,-d,, dorsal teeth; v,, ventral tooth. (From Sullivao et al., 1976.)


    from the " Calanus type ", and can lead by further reduction to a " Paracalanus type '' of feeding. Earlier Itoh (1970) tried to quantify such differences by calculating an " edge index " ( E L ) which took into account the length and distance between teeth relative to the total width of the mandible blade. Schnack (1975) using Itoh's E.I. (with some modification) found she could identify three groups of copepods : (1) E.I. < 500, continuous filtering herbivorous copepods; (2) E.I. 500-900, omnivorous copepods ; (3) E.I. > 900, carnivorous copepods. Schnack (1975) found Pseudocalanus females had an E.I. of 365 and they were placed with Paracalanus parvus females (E.I. of 265) in the first category.

    Sullivan et al. (1975) examined the teeth on the mandibular blades of eleven species of copepod in detail using a scanning electron micro- scope. They confirmed the work of Beklemishev (1 954a) that the teeth had siliceous crowns set in a chitinous mandibular blade. They also showed that the right and left blades were not identical. The sharp projections on the teeth of one mandible fit into the grooves on the teeth of the opposite mandible, suggesting a cracking rather than a grinding action. In the herbivorous copepods such teeth would be well suited for breaking diatoms, and Sullivan et al. (1975) comment that " possession of glass teeth for eating food in glass cases is surely one of the lyrical symmetries of nature ".

    Based on the work of Beklemishev (1954a), Sullivan et al. (1975) have divided the teeth into three groups. Starting with the ventral edge of the blade and progressing to the dorsal edge these groups are : ventral, central, and dorsal.

    The right mandibular blade of PseudocaZanus has a single large ventral tooth separated by a diastema from the rest (Fig. 11A). The left mandibular blade of Pseudocalanus was not studied but based on work on other species of copepods, the left blade probably has two ventral teeth into which the single ventral tooth on the right blade would fit. The ventral tooth on the right blade of Pseudocalanus is followed by four central teeth (Fig. 11A) which are followed by three dorsal teeth of a complex nature (Fig. 11B) and Sullivan et al. (1975) suggest that these dorsal teeth can " tightly grip food of a softer nature ".

    2. Peeding on large particles Cushing (1955) states : " I have Been a Psedocalanus take a

    Biddulphia sinensis almost as big as itself, break it and filter off some of the contents ". This is an important observation because it suggests that, despite evidence given above that Pseudocalanus is basically a


    continuous filter feeder it is, nevertheless, able to feed by another mechanism, evidently involving selection of larger particles.

    Gauld (1964) suggests that larger particles are captured by Pseudo- calanus as in other copepods, by use of a sweeping movement of the second maxillae. He also pointed out that the second maxilla of Pseudocalanus has at its tip a long stout sets (Fig. 7F) which would be a very effective seizing and holding weapon . The maxillipeds may be involved in this feeding process as well since they are known to play an important part in the grasping of food by carnivores such as Euchaeta norvegica (Gauld, 1964) and Oithona similis (Schnack, 1975).

    B. Food eaten 1. Xpecies eaten in nature

    Pseudocalanus is capable of ingesting a wide variety of food. Corkett (1966) has shown that individuals in the laboratory will take in fine sand and produce faecal pellets and Schnack (1975) finds sand (fine mineral particles) in guts in nature. Pavlovskaya and Pechen- Finenko (1975) have shown that Pseudocalanus in the laboratory will ingest and assimilate algal detritus, humus particles, and even melanin. These and other such experiments are reviewed later, but they tell us nothing about the food available to and chosen by animals in nature.

    Until recently, the gut contents of wild-caught Pseudocalanus had not been extensively studied. Lebour (1922) concluded that diatoms formed the main food, especially Coscinodiscus and Thalassiosira. Flagellates were also thought to be eaten although indistinguishable in the guts. Later, Lebour (1 923) found coccoliths in guts, as evidence that coccolithophorids are eaten.

    Marshall (1949) examined guts of over 100 live Pseudocalanus from off Millport, Scotland, and found that 73 were empty or had indistinguishable remains, 18 had diatoms, 4 had radiolarians, 1 had a flagellate, and 10 had crustacean remains. Although the crustacean remains show that Pseudocalanus can be carnivorous (and we have found that females will eat their own nauplii) the morphological evidence of the previous section and other studies in nature (below) imply that they are overwhelmingly herbivorous. Beklemishev (195413) stresses this, and found only the diatoms Chaetoceros and Thalassiosira in guts of adult females from the Bering Sea.

    Schnack (1 975) presents a great amount of information on food and feeding of copepods off Kiel Bay, near the mouth of the Baltic. She determined the kinds and amounts of food in guts of adult female Pseudocalanus taken in November and December 1970, and in July,


    September and October 1971. These contents were compared with food in the water column, sampled by a net with mesh of 54 pm and by plankton pump which sampled particles too small to be caught by the net. She found that the spiny diatoms Chaetoceros spp. were almost uneaten. Xkeletonema costatum was common in the water but scarce in guts, possibly due to its fragility. I n general, she concludes that Pseudocalanus is a herbivore, that individuals favour small food species, that they remove only a fraction of the range available in the plankton, that they favoured centric over pennate diatoms, and that small forms like Exuviaella baltica and Heterocapsa triquetra were a t times important. These conclusions do not take into account the possibility of local concentrations of food or copepods in the water column (which would complicate conclusions about selection of one sort of food or another), and they are unsupported by statistical analysis.

    Zagorodnyaya (1 974) has produced by far the most detailed assess- ment of food in guts of Pseudocalanus from samples taken in the Black Sea off Sevastopol in January and March 1973. She identified and tabulated some 50 food species, predominantly diatoms and dino- flagellates, with some chrysophytes. No animal food was found. The three most regular species were the dinoflagellate Exuviaella cordata, the diatom Cyclotella caspia and the chrysophyte Coccolithus huxleyi. Diatoms were selected in excess of their proportionate representation in the water column, and the reverse was generally true of dinoflagel- lates (depth distributions of copepods and food species were taken into account). However, she concludes that species selection was generally based on size. This and other aspects of Zagorodnyayas important work are dealt with elsewhere.

    Feeding experiments conducted in the laboratory using natural seawater and its contained food give some indication of the food species used in nature, even with the reduced options in time and space. Curl and McLeod (1961) give anecdotal observations on the selective removal of Skeletonema sp. from stored plankton samples by Pseudocalanus and Acartia tonsa. Parsons et al. (1967) also noted use of Xkeletonema in more formal experiments. Geen and Hargrave (1966) found that Pseudocalanus did not eat many of the long-spined Ceratium sp. nor the spiny, chain-forming diatom Chaetoceros, but rather favoured larger flagellates in natural seawater samples. Parsons et al. (1967) also indicated that Pseudocalanus was unable to derive much value from samples of a bloom of Chaetoceros socialis and C. debilis. In contrast, Poulet (1974) observed chains of Chaetoceros sp. being devoured by females kept in unfiltered seawater.

    A species by species account of the food of Pseudocalanus in nature


    could in principle become almost endless. A number of the above authors have indicated that size is a chief determinant of suitability of a food species. This subject is dealt with next.

    2. Xixe of food Clearly there must be some lower limit to the size of food particles

    that can be filtered and some upper limit to the size of organisms that Pseudocalanus can handle . Observations on the maxilla, show that. the smallest distance between setules on the setae is - 3 pm (p. 55) and individuals can evidently contend with food almost as large as themselves (p. 57). However, much effort has been expended on the search for size-selective feeding within these limits. As shall be seen the evidence for size-selective feeding by filter-feeding animals is by no means conclusive.

    Evidently the first formal consideration of size-selective feeding by Pseudocalanus was by Hargrave and Geen (1970). They showed that filtration rate was significantly higher for cells about 10 pm in maximum diameter than for cells of about 0.5, 5, and 7 pm (about 12 v. 4-5 ml/cop./day respectively). Their results are marred by being based on experiments with a mixture of C I V and C V of Pseudocalanus and Temora longicornis feeding in water from which particles > 35 pm had been removed by filtration.

    Zagorodnyayas (1974) analysis of gut contents of Pseudocalanus in the Black Sea is especially valuable for its information on several stages of copepodids and on adult females (Table V). Counts and measurements are based on unspecified standard methods , and unfortunately there is no clear indication in her paper that the percent- age values in Table V are for cell numbers or total cell volumes, although


    COLUMN. (After Zagorodnyaya, 1974.)

    Size January March group ( rm)

    < 10 10-20 20-30 30-40 40-50 > 50

    C I I I C I V C V

    43 59 38 50 34 37

    7 6 19 - 1 -

    1 1

    _ _ _ _

    Ad. Q Water C IIf

    16 25 50 38 41 7 31 23 36

    8 4 7 5 3 - 2 4 -

    ~ _ _ _


    C I V

    53 21 21

    3 2

    C V Ad.?

    61 54 16 15 13 20 8 8 1 2 1 1


    14 66 17 1.6 1-4


    one can infer the former. Formal statistical analyses of the data as presented in Table V cannot be made, but they support Zagorody- nyayas conclusions that the copepods consumed mostly cells < 10 pm (which were especially Cyclotella caspia and Coccolithus huxleyi) and that older stages and adults were more competent with larger cells.

    Extensive studies by Poulet (1973, 1974, 1976, 1977), and Poulet and Chanut (1 975) have advanced the whole subject of grazing by copepods to new levels of sophistication. The recurrent theme in Poulets work is size-selective feeding.

    For each grazing experiment, Poulet placed 50 or 100 lively adult female Pseudocalanus in a liter beaker containing seawater screened through a 160 pm mesh. Duplicate containers filled with screened seawater served as controls. All experiments were carried out for 19-20 h a t temperatures close to those of the water from which the sampies were removed. The experimental and control samples were analysed with an electronic particle counter set for particles between 1.58 and 114 pm (earlier work) and up to 144 pm (later experiments). This produced data on concentrations (volume in p.p.m.) versus particle diameter (spherical equivalent).

    Poulet (1973) studied grazing in samples from 5 m a t five stations in a transect from the head of Bedford Basin, a highly enriched environ- ment, to beyond the entrance of Halifax Harbour, Nova Xcotia. He also used a vertical series of samples from five depths between 0-60 m from the middle of Bedford Basin. From his analyses of the changes in the concentration-size distribution of particles after grazing, he con- cluded that the copepods were well able to consume particles from 1.58-114 pm (although not readily if < 4 pm). Poulet (1973) found, however, that grazing occurred on smaller particles (< 25 pm) when these were more than about half of the total concentration and occurred on larger particles when these were equally concentrated as or more concentrated than the smalIer ones. That is, the heterogeneity of particle distribution in time and space can be overcome by copepods by shifting their grazing pressure from one size of food to another .

    Poulet (1974) expanded his work to a two-year study using water samples from 5 m in Bedford Basin. He described the seasonal cycles of particles in six size categories : 1.6-3-6 pm, 4-0-9-0 pm, 10-1-22-6 pm, 254-57.Opm, and 64-1 14 (or 64-144) pm. The seasonality of abundance of particles in nature is of course a property of the environment he studied, and is not reviewed here. Against this background of seasonal availability, Poulet studied possible selection of particles using elec- tivity indices for all but the smallest of the above six size categories. I n agreement with his earlier conclusions (Poulet, 1973), he argued that


    " in general, and within certain limits, Pseudocalanus minutus consumed those particles that were present in the greatest concentration ',.. This evidently need not be understood as indicating selection of those that are most concentra,ted. Poulet (1974) is somewhat equivocal on this question. Although he applies no statistical tests, he discusses seasonal variations in electivity indices a t some length, in this sense endowing the indices with " reality ". Finally, however, he concludes that Pseudocalanus is " unselective ') in its feeding.

    There is, however, no doubt that electivity varies with particle size. The numbers of positive and negative electivity indices can be esti- mated for each of his five particle-size groups from Poulet's (1973) text and his Fig. 5 . The indices were positive in la%, 33%, SOY0, 68%) and 59% of experiments for the smallest through largest particle size categories respectively (heterogeneity x2 = 45.3, d.f. 4, P < 0.01). This would seem to suggest that smaller particles ( < l o pm) are less readily removed by the animals. Poulet also presents a series of graphs with regressions of rate of consumption against particle concentration, which we summarize in Table VI. He concludes that " the highest


    y = a + b x __ Particle size n r

    PS a b

    1.6-3.8 60 -0.413 0.214 0.17 4.0-9.0 80 - 0'093 0.707 0.54

    10.1-22.6 89 0.365 0.991 0.63 25.4-57.0 84 0.430 0.932 0.83 64.0- 144.0 73 0.341 0.636 0.62


    z = particle concentration (In of mg/l). y = food consumption (In of mg/h/cop. x Given as log in original, but In meant,

    and with corrigendum from author (regression and correlation coefficients reversed in original).

    [correlation] coefficients were computed in size group 3 and 4, showing a good feeding response towards particles in the 10 to 50 pm range ". This conclusion cannot be inferred from correlation coefficients. More interesting questions might be asked using analysis of covariance, but this cannot be done from the data given. However, the elevations (a) of the regressions for the two smallest particle sizes (1.6-3.6 pm and 4.0-9.0 pm) in Table V I are lower than for larger particles. Except for the smallest particles, for which the variance of estimate must be very


    large (r not significant a t P = 0.05), the slopes (b in Table VI) are similar for each regression. The value of a for particles < 4 pm is about -0.4, and for particles > 10 pm is about 0.4. The difference suggests that the smallest particles are retained about half as efficiently (i.e., eO.8

    Poulet and Chanut (1975) come to somewhat different conclusions by using two non-parametric tests to detect possible differences in the size-frequency distributions of particles in diets and in controls. The more sensitive Kolmogorov-Smirnov test for the maximum difference between the cumulative frequency curves in controls and diets showed significant differences ( P < 0.05) in 16 of 42 experiments. However, in each of these experiments the difference was due to the increase in particles over control level, either substantiaIly (5-25% over control) or grouped in a narrow size-range. Poulet and Chanut conclude that statistically significant examples of apparent selective feeding are due to the formation of smaller particles from larger ones by the activities of the copepods-for example by the breakup of chains of diatoms. Certainly this may partly explain the low electivity of the smallest particles and the differences in the regressions of consumption rate on particle concentration between large and small particles.

    The general conclusion to be reached from Poulets earlier work does not altogether agree with the observations of Zagorodnyaya (1974) who found that Pseudocalanus favoured cells < 10 pm (Table V). Her experiments cannot be considered as well controlled as Poulets, but her observations that the diets of older copepodids and adults may include larger food particles is an amplification rather than a contra- diction of Poulets work. It seems that Pseudocalanus may make use indiscriminately of a wide range of food, but that the upper limit of that range may increase with body size. We have given anatomical evidence (p. 5 5 ) that seasonally smaller females may be able to filter smaller particles. Finally, in his most recent paper, Poulet (1977) concludes that copepodids (C I-C IV, mostly C 111) consume food particles


    humus particles, melanin) to varying degrees by Pavlovskaya and Pechen-Fenenko (1 975). Since a substantial fraction of particulate organic matter in coastal waters is non-living, the work of Poulet (1976) adds an important refinement to his studies of particle grazing by Pseudocalanus.

    Using measurements of adenosine triphosphate (ATP) he estimated the proportions of living and non-living particulate carbon in control and grazed samples of seawater between 29 February, 1972, and 24 January, 1973. (Other features of his grazing experiments are noted in the previous section.) The living fraction in the sea (control samples) varied from 7 to 42%, with a mean of only 21% of total particulate carbon. He estimated that on average about 29% of the ingested carbon was living.

    Poulet found that selectivity [sic] indices for the living fraction were positive in 56% of experiments. However, a sign test and a runs test indicated that the selectivity values for living and non-living particles did not differ.

    Poulet concludes that seasonal variation of the body size and the number of eggs laid per female , . . give indirect evidence that the assimilation of a diet composed mainly of non-living particles occurs and is channelled into growth and reproduction . However, food probably has little effect on body size (p. 122), and there is in fact no direct indication that the non-living fraction is either assimilated or nutritious.

    C. Feeding rate

    The aim of observations and experiments on Pseudocalanus as a consumer of food is presumably to establish for individuals of a given stage, sex, and size, the rate of removal of food of a particular kind at a particular density in the water. Temperature and perhaps salinity can be assumed to be important in determining this rate. Such data tell us nothing about the assimilation of food nor of its subsequent utilization.

    Although they are in principle interconvertible, rates of food consumption by copepods have traditionally been expressed in two ways: ( 1 ) as Jiltering rate and (2) as feeding rate, or, more precisely, ingestion rate. Filtering rate measures volume of water swept clear of food (or other particles). The dimensions of filtering rate are volume of water per animal per unit time, and the expression of food consumption in this manner has a hopeful ring ; it was once believed that copepods could be treated as automata that swept the water at rates independent of the character and abundance of the food therein. This contention


    has to be demonstrated, and some support for this view is found in the work reviewed in the previous sections. We consider, however, the expression of food consumption in terms of filtering rate to be a need- lessly abstract way to express the intake of food and prefer to use ingestion rates.

    Ingestion rates can be expressed in a number of ways. Although often given as rates per individual or as rates per unit of body weight, rates given as a percentage of body weight (wet, dry, carbon, etc., as appro- priate to the technique) are perhaps the most useful. The appropriate time unit is one 24-h period (we will follow the convention of using per day ) in a priori recognition of the possibility of die1 rhythms. We refer to the total ingestion per day as the daily ration.

    The vast literature on consumption of food by copepods (reviewed recently by Marshall, 1973) is full of observations and experiments that do not seem to supply useful information on any of the above topics ; we make no attempt to be exhaustive in our review of matters other than those specified above as they relate to Pseudocalanw.

    1. Effect of food concentration Much of the earlier literature on feeding by copepods argued or

    assumed that filtration rate was independent of concentration, and this was proposed for Pseudocalanus as well (Gauld, 1951). The extensive experiments by Marshall and Orr (1966), using uptake of 32P from algal cells, allow some inferences to be made about the suitability of certain food species. However, their variable and very low estimates of filtering rates give no information on effects of food density. They used small concentrations of cells, and losses of 32P in faeces and excretion were not accounted for.

    The first indication of the seemingly obvious possibility that Pseudocalanus could be satiated a t high food concentrations comes from the work of Anraku (1964~) . He showed that females in (evi- dently) 6-h experiments did not ingest more than about 5 x lo4 cells/day of the diatom Thalassiosiru Jluviatilis or filter more than about 40 ml/day of the medium (Fig. 12A).

    Urry (1965) found that rate of production of faecal pellets diminished but was not asymptotic a t concentrations of lo6 cells/ml of the flagellate Isochrysis galbana. Corkett (1966) extended these studies to higher concentrations. Although rate of faecal pellet production cannot be used to estimate feeding rates, it indicates the shape of response to density of two food species (Fig. 12D, E). Corkett also found that at concentrations of I . galbana less than 4 x lo4, faecal pellets were about

    A.M.B.-15 5


    half as long but the same width (and therefore about half the volume) of those pellets produced at higher concentrations.

    Parsons et al. (1 967) estimated concentrations of food organisms in control and grazed samples of seawater with an electronic particle counter, and found that ingestion rate levelled off at high concentra. tions (Fig. 12B). Furthermore, they found that feeding virtually ceased

    p 3

    L l I " 0 I 2 3 4 5 2 4 G 5 10 I5 20

    Celts x103/rnl Concentration (pm3 x 106/rnl)


    Cells x ro3/rnl 119 C/ ( FIU. 12. Evidence of saturation of feeding rates of Pseudocalanue. A, ingestion rate of

    the diatom !z'halassioaira Juuiatilk (after Anraku, 1964~). B, ingestion rate of mixed natural phytoplankton (after Parsons et a2.. 1967). C, ingestion rate of II mixture of the diatom flkeletonema sp. and '' p-flagellates " (after Parsons et al., 1969). D, number of fmcal pellets produced with the diatom Laudetia boreal& as food (after Corkett, 1966). E, number of faecal pellets with the chrysomonad 180- chry8i8 galbana (after Corkett, 1966). F, ingestion rate (mean of all stages) of Pseudo. caEanua feeding on Thatassiosira rotula as a function of nominal food densities (after Paffenhofer and Harris, 1976).

    in Pseudocalanus and other species at low food concentrations. Accord- ingly, they felt that daily ration r could be given as a function of food density p by the modified Ivlev equation :

    r = R [ 1 - e - k ( P - P d ] .

    Here R is the maximum (asymptotic) ration, po is the level a t which feeding ceases, and k is the proportionality constant applying to the particuIar feeding species or food type. Unfortunately, the alga Chaetoceros sp . that predominated in their seawater samples was thought to have been almost uneaten, so the relationship between food density and ingestion rate is open to question.

    Parsons et al. (1969) confirmed the utility of their modified Ivlev equation in describing feeding rate of Pseudocalanus (with a small


    admixture of Oithona sp.) on food consisting of a mixture of Skeletonemu sp. and p-flagellates (Fig. 12C).

    Frost (1974) graphs ingestion rate of cells of Thalassiosira JEuviatilis by Pseudocalanus as a function of cell density. He shows an abrupt threshold of ingestion rate of about 1 400 cells/cop./h beginning at a cell density of about 1 100 cells/ml. Because he does not give data points on his graph, we do not include it in Fig. 12. A later paper (Robertson and Frost, 1977), also without data for Psezdocalanus, gives a maximum daily ration of 1-13 times body weight in carbon.

    We turn to the work of Paffenhafer and Harris (1976) for the most complete study of ingestion rates as a function of food density. They showed that filtering rate and ingestion rate were roughly proportional to body weight between stages C I and C V, so that the amount ingested per unit body weight at any given food level is constant for these stages. We use their nominal values of food density (actual values deviated little) in Fig. 12F.

    We have choaen to fit by eye more-or-less asymptotic curves to the examples of satiated feeding in Fig. 12, although we are aware of alternatives (e.g. Frost, 1974). A lower limit of food density a t which feeding ceases, as indicated in the work of Parsons et al. (1967, 1969) is not always evident in Fig. 12.

    Because the relationships have been assumed to be asymptotic, we have chosen to estimate the levels of food supply that lead to 90% of the maximal ingestion rate. We have used original estimates of cell volume and carbon content where given. The size and carbon content of T. Jlzlviatilis are from means in Mullin et al. (1966). Corkett and McLaren (1969) give the volume of Isochrysis galbana. Corkett and Urry (1968) give disc diameter of Lauderia borealis, whose volume is estimated from published illustrations by assuming that discs are twice as broad as high. Carbon contents for these two species are estimated from the carbon/volume regression in Mullin et al. (1966).

    There are startling variations in the results of this comparison (Table VII). The very high value for L. borealis is almost certainly due to the fact that it did not stay well in suspension in the static cultures used by Corkett (1966). The motile I . galbum is probably too small (4-8 pm) to be efficiently filtered; the work of Poulet (p. 63) suggests that it might be removed at about half the rate applicable for larger cells. Although Chuetoceros appears to be saturating a t high levels, it was hardly ingested at all. Even between the two species of Thalassiosira there appear to be differences (Frosts estimate, cited above, for T. jluviatilis gives an abrupt threshold level at about 1 100 cella/ml or 0.21 pg C/ml). Clearly all these experiments give evidence



    Phytoplankton concentration at 90% of Cell volume rnazimum ingestion rate

    Food species p m 3

    cells/ml pm3/m1 pLgClml

    Thalassiosira fluviatilia 1370 1700 3.9 x 106 0.32 Isochrysis galbana 100 160000 16.0 x loG 2.72 Lauderia borealis 27 000 4300 116.0 X 10" 5.14 Chaetoceros sp. - - 5-2 X lo6 0.27 Skeletonema sp. and

    Thalassiosira rotula - - 1.1 x 106 0.09 " p-flagellates " - - 11.5 X lo6 1.09

    for satiation of feeding rates, but tell us little about the food levels at which this may be achieved in nature. Paffenhofer and Harris (1976) argue that their food densities match those found in nature, and that their use of large, rotating culture-vessels contributed to their low estimates of satiation food densities using T . rotula.

    It is also possible to calculate the maximal rates of ingestion from the experiments summarized above. Table VIII assumes the same


    Daily ration Food species

    llm3 PFLS c Thalassiosira fluviatilis 110 x lo6 8.14 Chaetoceros sp. 0.8 x 106 0.04 SkeZetonerna sp. and

    Thalamiosira rotula 195 X loG 16-1 " p-flagellates " 40 x 40G 3.8

    conversion factors used in Table VII. The estimate for Chaetoceros sp. is clearly not comparable with those for the other food species, and supports the contention of Parson's et al. (1967) that it is hardly eaten because of its spines; the maximum ingestion rate is clearly not set by satisfaction of " hunger ". Although the estimates of ingestion rates in Table VII I otherwise show considerable variation, this is not as extreme as the differences among saturation levels of food supply (see Table VII). It should be noted that the high estimates of ingestion


    rates (up to 140% of body weight per day, see Fig. 12F) of Paffenhofer and Harris (1976) are for growing copepodids, and the rest are based on adult females.

    There is clear evidence of high variability in feeding rates of individuals. In a small series of week-long experiments with one or two copepods per vessel, Corkett (1966) found that one female consumed as much as 330 x lo6 pm3 Isochrysis/day for a week, whereas another took as little as 60 x 106 pm3/day. Similarly, the experiments of Delalo (1964) indicate that individuals varied greatly (see p. 73).

    We can now consider the relationship between food density and feeding rate in natural seawater as found in the two-year study by Poulet (1974). We have shown (Table VI) that the regression coeffi- cients of logarithms of ingestion rates of particle concentrations are somewhat less than unity when each size group of particles is con- sidered separately. This is a suggestion that saturation might occur at higher food levels. However, the overall regression of ingestion rate (Y in mg X 10-4/h) on food concentration (X in mg/l) is given by Poulet (1974, with his corrigendum and correction as in our Table VI) as: In Y = 1.29 In X -0.33 ( r = 0.80, d.f. 93). The value of r after transformation to z and calculation of S.E., implies that the regression coefficient (1.29) is significantly greater than 1.0. Thus there is no evi- dence for levelling off of feeding rate with increased concentration of particles : quite the contrary. This non-proportionality is probably an artifact of grouping particles of different sizes, since smaller particles, for which regression elevations were lower, were also present in lower average concentrations (Poulet, 1974, his Fig. 9). In his later study of feeding by copepodids (Poulet, 1977) there is a weak positive correlation (weighted r = 0.61, d.f.8, p N 0-06, from his Table 1) between feeding rate and monthly mean food concentrations. There is also no evident leveling off of rates at higher concentrations.

    The particle concentrations measured by Poulet (1 974) averaged 5.2 p.p.m. or 0.27 pg C/ml, using his conversion factor. In spring they frequently exceeded 10 p.p.m. or 0.52 pg C/ml. In his study of cope- podid feeding, Poulet (1 977) tabulates food concentrations averaging 3.80 p.p.m. (0.20 pg C/ml). These values are close to or exceed those Bhat have been found to saturate feeding rates in some laboratory experiments (Table VII), especially the critical ones of Paffenhofer and Harris (1976). An explanation might be sought in the fact that on average some 79% of the particulate carbon in Poulets (1976) experi- ments was non-living . It this is relatively non-assimilable or otherwise unnutritious (contrary to Poulets suppositions) the copepods might continue filtering a t maximal rates in spite of very high food concen-


    trations. This, however, does not explain the low ingestion rates exhibited by the copepods in Poulet's experiments (see p. 72).

    2. Effect of temperature Although temperature certainly has a profound effect on the

    growth and development of Pseudocalartus (Section X), its effect on feeding rate has apparently been examined only by Anraku (1964b). His results are somewhat difficult to interpret. It should be borne in mind that only five females were used to determine each experimental point in Fig. 13. Anraku (1964b) does not report the concentrations of

    L 50

    111111111111 '0 4 8 12 16 20 :

    Temperature ("C)

    FIG. 13. Filtering rates at different seasons of adult female Pseudocalunua from near Approximate habitat temperatures, H, are shown on Cape Cod, Massachusetts.

    each curve of the right-hand graph. (After Anraku, 1964b.)

    Thlassiosira Jluviatilis he used, and it is worth noting that filtering rates were in other experiments about 30 ml/cop./day a t 1 000 cells/ml and only about 10 ml/cop./day a t 5 000 cells/ml (Fig. 12A). Further- more, dry weight may be an inappropriate measure of filtering capacity, especially since it includes '' inert " materials like stored oil.

    Although the effects of temperature have by no means been fully explored in Anraku's experiments, it seems possible to conclude that high temperatures, even 15"C, depress feeding rates. The feeding rates per unit weight a t " in situ " temperatures (after Anraku, 1964b) are interpolated in Fig. 13B. There is a suggestion that the " optimum " rate lies near these habitat temperatures. The fact that filtering rate in August at 15C is almost as high as that a t 8C might be taken as a hint of acclimation to warm summer temperatures. However, there remains a great difference between rates at habitat temperatures, suggesting that no seasonal adjustment has occurred.

    However, let us suppose for the purpose of exposition that the size of


    the copepods were as indicated in the length-temperature relationship for nearby Long Island Sound (Fig. 26, p. 118): 1-00 mm in May, 0.98 mm in December, and 0.81 mm in August. Assume further that the filtering capacity of a copepod is proportional to the square of its length: 1.00, 0.96, and 0.66 respectively for the above months. It can be seen that the similar filtering rates per copepod in May and December and the muchlower rate per copepod in August (Fig. 13A) make sense in terms of this approximation of filtering capacity. We do not offer this as a serious analysis, but as a plea for more thoughtful considerations of copepod size in design of such experiments.

    3. Daily rationns in nature We have given several estimates of the maximal daily ingestion by

    copepods in the laboratory (Table VIII). Here we will summarize attempts to estimate the daily ration of Pseudocalanus in nature.

    Zagorodnyaya (1 974) derived a mean daily index of fullness of guts (as a percentage of body volume) from observations on sampIes collected over 24-h periods in the Black Sea during January and March, 1973. Translating these indices into amounts of food consumed during 24 h required a measure of the rate of passage of food through the guts of the copepods. Zagorodnyays quotes a symposium paper by Pavlovskaya and Pechen-Finenko (see also the same authors, 1975, for more details), who carried out experiments to determine the time required for clearance of radioactive food (Gynmodinium kowalevskii) from guts of adult females. Pavlovskaya and Peehen-Finenko (1975) conclude that food passes through the gut at 8C in 30 min. This seems to be somewhat arbitrary : their Fig. 2 indicates that almost all the radioactivity was evacuated from guts a t 20 min, and they choose to use an asymptotic curve to describe the series of points, which allows no real estimate of time for complete evacuation. However, their estimate (20 or 30 min) compares closely with direct observations by Delalo (1964) that identifiable remains of Prorocentrum micans appeared in faeces on average about 40 min after commencement of feeding.

    Using 0.5 h as an estimate of time for passage through the gut the daily ration of Pseudocalanus was calculated by Zagorodnyaya (1 974) from mean daily indices of fullness: 24 multiplied by (index of full- ness)/O-5. No trace of food was found in adult males. Table IX indicates that C V and adult females in March had the highest daily rations. These stages showed most marked diurnal vertical migration, and Zagorodnyayas work is considered later in that context (p. 165;).

    Poulet (1974) summarized his extensive experiments on grazing by female Pseudocalanus on natural food particles as monthly estimates


    TABLE IX. DAILY RATION OF BLACK SEA Pseudocalanus. (From Zagorodnyaya, 1974.)

    Ration, yo of wet body weight

    C I I I G I V C V Ad.? Month

    January March

    7.1 6.0 7.0 5.7 2.6 5.0 11.8 12.1

    of mean food concentrations and mean daily rations. Rations were also expressed as a percentage of body weight, assuming that each adult female weighed 6.7 pg carbon (in a later paper, Poulet, 1976, he uses a value of 7.14 pg C). In fact, if Pseudocalanus near Halifax vary seasonally as they do in other localities (Fig. 26, p. 118), a three- ta four-fold seasonal variation in body weight (from the relationship on p. 127) may be involved. Bearing in mind these possible sources oj error, the work of Poulet (1974, his Table 1) implies an essentially lineal relationship between food supply and ration. In his study of feeding bj copepodids, Poulet (1977) shows (his Table 1) that they ingested ar average ration of 0.18 pgC/cop./day using his estimate of body weigh1 for copepodids (3-26 pg dry wt) and assuming them to be 50% carbor (see p. 126), we estimate that they consumed on average only 11% of their body weight per day (seasonal range, 3-16%).

    The estimates of daily rations as a percentage of body weight in nature of 2.6-12.1% (Table IX) by Zagorodnyaya (1974) and of 2 . 2 4 5 5 % by Poulet (1975, 1977) are in general much smaller than those that can be gained at saturation feeding levels in laboratory experiments (Table VIII, assuming body weight of 6.7 pg C, as for Poulets work, above). The estimate by Poulet (1976) that only an average of 21% of the food of Pseudocabnus is living does nothing to explain this discrepancy. Non-living food is unlikely to be more nutri- tious than living food, and thus be equally satisfying as living food at lower densities.

    In conclusion, there remain major questions about the amount of food consumed by Pseudocalanus in nature. These can only be resolved after a consideration of the amounts of food required by Pseudocalanus.

    D. Die1 feeding rhythm

    It is probable that vertical migrations of Pseudocalanus routinely take it into depths where food is scarce, and some authors have assumed in their calculations that feeding only occurs at night (McLaren, 1963;


    Parsons et al., 1969). It is of interest to know if there is a feeding rhythm that is independent of this behaviour ; the evidence is equivocal.

    Anrakus (1 964c) 53-h feeding experiments revealed initial acclima- tion of rates, but no evidence of die1 rhythmicity. Sharp changes could conceivably have occurred during the night, when no observations were made, but the amount of food eaten by morning was about as predicted from the rates prevailing during the previous day. Lock and McLaren (1970) found food present in guts of Pseudoculanus at all times of day and night (artificial light cycle) in rearing experiments. These experiments were with animals that had spent varying amounts

    1 ;z 0a700 1100

    \ \#



    /P\ el-- ...* ..-- --- _..- ..*-

    1500 1900

    :a- -

    Time of day

    Fro. 14. Number of cells of tho dinoflagcllate Prorocentrum micans eaten by recently captured adult female Psedocalanus during 4 hour intervals. (After Delalo, 1964.)

    of time in the laboratory. Possibly any natural rhythm had been lost. He placed freshly

    caught individuals in 15-20 ml receptacles and fed them the large (40-50 pm) dinoflagellate Prorocentrum micans at 200-400 cells/ml. The medium was changed every 4 h and the number of tests (indigest- able) of P. micans were counted in the preserved faecal pellets. Strong feeding peaks were evident (Fig. 14). He found considerable individual variation among females in intensity of feeding, but peak times coin- cided in all individuals in February and in 3 of the 4 in March (when one peaked 1900-2300 h). Delalo compared mean consumption during the period of 6 h on either side of the peak time with that during the remaining 12 h and found significant differences by t-test in both February and March. Although this test is formally questionable in view of the small samples and inhomogeneity of variances, the coinci- dence of peaks is in itself clear evidence of cycling (9 out of 10 ; binomial

    Delalo (1964) attacked the question directly.


    expectation 115, P < 0.01). Delalo also attempts to analyse the difference between the February and March curves using x2 (method unclear), and concludes that the difference is non-significant. However, the fact that all four March peaks are later than all six February peaks is significant (runs test, P < 0.05).

    Delalo allowed one individual in March to continue feeding for a further 24 h, and found that the feeding rhythm persisted, although at reduced amplitude (maximum 34 cells v. 81 cells consumed, at 1500-1900 h rather than 1900-2300 h, and total intake during the 24 h 143 v. 192 cells, estimated from his Fig. 2). Although it is unwise to

    O O E 80


    .- f 40



    c Jan.

    L t I

    0- 1200 2000 0400 1200

    l i m e of sample FIG. 15. Observations on fullness of guts of copepodid and adult stages of Pseurlocalanua

    captured at various times of day in the upper 150 m of the Black Sea. (After Zagorodnyaya, 1974.)

    read too much into the performance of one individual, there is thus a suggestion that behaviour changed after a period in the laboratory.

    Delalo speculates about the relationship of his results to feeding rhythms of vertical migration. This subject has been examined extensively by Zagorodnyaya (1 974, 1975), using samples taken in January and March (dates not given) in the northern Black Sea. She dissected out guts of copepodids and adults (20 of each stage in each sample where possible) to estimate volumes of compact food masses. For present purposes it is enough to illustrate the clear evidence for rhythmic feeding in nature (Fig. 15).

    Most recently, Mackas and Bohrer (1 976) have used a fluorometric technique for detecting chlorophyll in gut contents to illustrate a moderate die1 rhythmicity in the intake of food by Pseudocalanus in waters near Halifax, Nova Scotia.


    Our general conclusion is that Pseudocalanus may show strong diel feeding rhythms in nature that can perhaps only be demonstrated in freshly caught individuals. Certainly short-term observations on feeding behaviour and feeding rates must a priori be considered suspect. Prudence might also suggest that only freshly caught individuals should be used if natural rates are being sought.

    E. Assimilation

    The only attempts to measure assimilation by Pseudocalanus are evidently those of Pavlovskaya and Pechen-Finenko (1975), who worked with C V and adult females (numbers in each experiment unspecified) from the Black Sea. These authors used a wide variety of radiocarbon-labelled foods-living dinoflagellates, diatoms, and infusoria, freshly prepared detritus of single-celled and multicellular algae, humus of plant origin, and melanin.

    One set of experiments was run in triplicate at 8C for 8-17 h, during different times of the 24-h period to accommodate possible diel irregularities. The amounts of food assimilated were measured by radioactivity of the copepods, which were dried for weighing after their guts were evacuated of unlabelled food. The amount of food assimilated by the copepods was very low in these experiments : maxi- mally 3% of body weight in the case of the diatom Skeletonema costatum, followed by melanin (1.8%). The large dinoflagellate Peridinium trochideum, detritus from the multicellular alga Cystoseira barbata and humus of plant origin were all taken very little: 0-1-0.2% of body weight during the experimental period.

    By using 15-min exposures to labelled food, collecting all faeces, and measuring labelled CO, as respiration, Pavlovskaya and Pechen- Finenko were able to estimate assimilation efficiencies (percentage of ingested food appearing in bodies or respired). They used corrections for changes in feeding rates during the 24-h period in order to express results in percentages of copepod body weight per day, but the relative distributions of ingested food among faeces, body, and respiration are unaffected by this mode of presentation (Table X).

    Clearly there are marked differences in the amounts ingested of the different foods and the extent to which they are assimilated and used in respiration. Much of the assimilated food appeared to be lost in respiration during the experimental period. The two dinoflagellates were evidently relatively undigestible, while detritus of Ulva regida was little ingested. Other results by Pavlovskaya and Peched-Finenko are expressed by them only as assimilation eficiencies: Uronemu


    TABLE X. ASSIMILATION OF FOOD BY C V AND ADULT FEMALE Pseudocalanus. (After Pavlovskaya and Pechen-Finenko, 1975.)

    yo of body wtjday

    Unassimilated Respired Remaining Assimilation (infaeces) (in CO,) in body eficiency (%)

    Kind of food

    Gymnodinium kowalevskii 8.86 4.90 0.57 38 Peridinium trochoideum 17.36 4.59 0.85 24 Detritus, Platymonas viridis 8-19 10.32 9-26 71 Detritus, Ulva rigida 1.69 2.23 0.45 61

    marinum 68% ; detritus, Cystoseira barbata 53% ; humus 82%; melanin 7 3 yo.

    Thus, with the exception of the two species of dinoflagellates (Table X), most foods were digested relatively efficiently. However, 8s noted above, some of these were not readily ingested (detritus of the two multicellular algae, plant humus).

    It may be concluded from this work, that ingested food is generally assimilated with high efficiency ; but, in the absence of statistical analysis, it is not possible to conclude that the efficiencies ranging from 53 to 82% really differ significantly. Furthermore, the rather startling difference in the distribution of assimilated matter between the body and respiration pools (Table X) raises questions about the validity of the approaches and techniques (cf. Conover and Francis, 1973). Finally, in view of the enormous variability in rates of ingestion of food by Pseudocalanus shown in previous sections, minor differences in assimilability may be of little consequence.

    F. Food requirements for sustenance 1. Amount of food

    The amount of food required by Pseudocalanus, like the amount consumed, is a matter of definition. Later sections consider the food requirement for growth (p. 133). Here the concern is with food require- ment for sustenance of the adult and is measured by the survival of adult female Pseudocalanus kept in the laboratory.

    Urry (1 965) demonstrated, as a prelude to determining food require- ments for survival, that starved females from the overwintered generation off Plymouth (see p. 145) survived longer than the females from the f i s t spring generation. Corkett and Urry (1968) demon- strated that growth medium (Erdschreiber medium) alone could not be


    used as a food, and that varying culture volumes between 10 ml (1 copepod present) and 500 ml (2 copepods present) had no effect on survival if food supply was adequate. Corkett and Urry (1 968) showed that antibiotics did not prolong life of starved animals, but that small amounts of penicillin and streptomycin increased survival when the copepods were fed. Large amounts of antibiotics (more than 100 i.u. of each per ml) were clearly toxic. Antibiotics were not used by Urry (1965) and Corkett and Urry (1968) in their tests of food requirements, but the adults were placed in fresh culture medium every week.

    Two algal species have been tested a t varied concentrations. Isochrysis galbana at 30 000 cellslml promotes an almost full length of life (Table XI), although this level may supply only 60% of the food that Pseudocalanus is capable of ingesting (see Fig. 12E). Corkett and Urry (1968) found that much smaller quantities of the large diatom Lauderia borealis are needed-500 cells/ml being sufficient (Table XI) which is a level of only about 30% of that which can be ingested (see Fig. 12D).

    TABLE XI. SURVIVAL OF ADULT FEMALE Pseudocalanua AT VARYING FOOD CONCENTRATIONS. (From Urry, 1965, and Corkett and Urry, 1968.)

    Algal species Lauderia borealis Isochrysis galbana

    Con- Con- centration centration copepods (days) (cells/ml) (cells/ml)

    Average life No. of Average l i fe (days)

    No. of copepods

    20 0 17 18 0 14 20 1000 23 18 500 41 20 5 000 26 18 2 000 53 20 30 000 58 18 4 000 46 20 100 000 83

    2 . Quality of food Urry (1964, 1965) tested the quality of a number of species of

    algae in sustaining adult females. Each species was fed to a group of copepods (taken from the same samples from nature) at 30 000 cells/ml and compared with a control group of copepods fed Isochrysis galbana at 30 000 cellslml (Table XII). Clearly a wide variety of food species permit the survival of adult females.

    It is of interest to look at those species that seem nutritionally inadequate (Table XII). Urry (1964, 1965) does not explain the


    inadequacies of Nitzschia gotlandica or Hemiselmis virescens. He does suggest that, although Gymnodinium veneJicum has been known to produce poisonous exocrines, his cultures had evidently lost their toxicity.


    (After Urry, 1964, 1965.)

    Relative No. of length of life copepods Rood apeciesa

    Diatoms Phaeodactylum tricornutum Nitzsohia gotlandica

    Cryrnnodkium veneficum

    Arnphidinium sp .

    Hemiaelmis virescens

    Chlorella stigmatophora Dunaliella tertiolecta Chlamydomonaa coccoides Chlarnydomow sp.

    Dicrateria inornata


    a. vitiligo




    0.93 0.37

    1.14 0.59 0-51


    0.57 0-61 0.98 0.89

    < 0.36

    48 40

    48 61 20


    - 48 20 20


    a Both food species and control (Zsochlyais galbantc) at 30 000 cells/ml, replenished weekly.

    G. vitiligo is not known to be toxic, but Amphidinium spp. have this reputation. Some Chlorella spp. are toxic, and Urry (1965) showed that Pseudocalanus survived poorly (0.56 of control) when fed Isochrysis galbana in a cell-free extract of C. stigmatophora. Urry also found undigested cells of this species in the faeces. No such toxicity effects were noted in the other relatively unsuitable chlorophyte, Dunaliella tertiobcta.

    Corner and Cowey (1968) compared amino acid contents of the chrysophyte Dicrateria inorwta with that of the diatom Phaeodactylum tricornutum, taking (from Urry, 1965) the former as a " poor " and the latter as a " good " food. There was little difference in amino acid contents, and we suggest that the former is probably " poor " because of its small size (3-6 pm) compared to the Isochrysis control ( P 8 pm).


    Although these experiments on food quality are of some intrinsic interest, they probably tell us little of the nutritional problems faced by Pseudocalanw in nature. None of the toxic or unsuitable species are widespread or dominant members of the open-water coastal plankton. PseUd0calanu.s may more often face food shortage, or refractory or unnutritional non-living food, than with unsuitable food species within the suitable size-range.

    G. Retrospects and Prospects

    We are left somewhat unsatisfied by published work on feeding of Pseudocalanus and, by inference, of other copepods. We are uncertain whether the low selection of small ((10 pm) particles is because of poor I sieving or a result of creation of small particles from large. It is possible that seasonal differences in the temperature response of feeding rate would not be found if a more appropriate measure of size of individuals were used. We are not really sure whether Pseudocalanw clears its gut in half an hour, twenty minutes, or even less.

    However, the most serious questions seem to us to concern the great variability of estimates of feeding rates, whether calculated from fullness of guts in nature, from rates of removal of natural food in seawater samples, or from removal of defined food species in laboratory experiments. The work of Paffenhafer and Harris (1 976) stands apart in revealing that very high feeding rates at low, natural food concentra- tions can be shown by copepods reared in the laboratory. We think it is quite probable that wild-caught animals (generally adult females) may fail under most conditions to show meaningful feeding rates. More attention should be given to residual die1 rhythms. Experiments should clearly be conducted with uncrowded animals, preferably with some sort of mixing of the medium. Consideration should be given to the character of individuals in grazing experiments; are they fat or lean, recently moulted or not, gravid or infertile, or are they even in some sort of resting stage?

    Recently Conover (1978) has made the bold suggestion, using ex- amples of unsaturated feeding rates shown by Poulet (p. 69) for Pseudo- &nw, that copepods adapt in nature by producing more digestive enzymes in response to increased food levels. Clearly this ability could underline the great variability shown by Pseudocalanw under various experimental conditions, and we look forward to further explorations of Conovers hypothesis.

    We will show later that maximal, temperature-dependent rates of


    reproduction (p. 98), development of stages (p. 156) and production (p. 189) may occur during a substantial part of the year in temperate waters. Further, it seems that Pseudocalanus can suspend development and enter an overwintering, resting phase even when food is plentiful (p. 157). Studies of food choice and feeding rates, plagued with inaccuracies and uncertainties, may be irrelevant when Pseudocalanus is so seldom food-limited in nature. Altogether, we conclude that more extensive studies of nutrition in Pseudocalanus may not be the most revealing approach to finding out how it works in nature.


    A. Sex ratio Although sex ratio is also an aspect of development or demography

    and could be considered in the section on development and growth or life cycles, we include it here because of its clear relationship to repro- duction. Sex ratios of adult Pseudocalanus, like those of many other copepods, are strongly distorted in favour of females. Many authors give sex ratios in relation to localities and seasons, and some speculate on the differences. It would not be profitable to quote many of these, since it is quite clear that the shortage of adult males in nature is due to their restricted life span relative to that of females, and not to markedly unbalanced primary sex ratios. We will quote some of the evidence for this conclusion from field samples and laboratory studies.

    The short life of adult males is most obvious in seasonal samples from high latitudes. In the far north, adult males may appear in numbers only around the time when overwintered copepodids begin to mature and then evidently disappear, whereas adult females may be found through the year (e.g. Ussing, 1938; Grainger, 1959). Ostvedt (1955) found that males reached maturity and fertilized females in the depths below 600 m in the Norwegian Sea, but failed to ascend with the females to the surface in spring.

    A number of authors have shown that males and females in plankton samples are roughly equal in abundance among C IV and C V, which show secondary sex characters (e.g. Ussing, 1938 ; Bogorov, 1939 ; Marshall, 1949 ; Fontaine, 1955 ; McLaren, 1969). The small deviations from unitary sex ratios that are discussed by some of these authors are probably due to different rates of development of males and females in these copepodid stages (McLaren, 1969).

    Laboratory evidence indicates clearly that adult males have shorter lives than females (p. 114), but rearing experiments are somewhat equivocal. Thompson (1976) used I . galbana and reared 87 adult


    females and 29 adult males at a range of temperatures ; no trend in sex ratio was evident in relation to temperature. On the other hand, Paffenhijfer and Harris (1976) obtained 73 adult females and 74 adult males on a diet of Thalassiosira rotula. There thus appears to be some trophic factor in determining adult sex ratio, but whether this operated in these experiments through differential mortality of males or through primary sex determination is unknown. We think it very unlikely that a trophic factor was responsible for the different sex ratios in samples from the North Sea and White Sea as speculated by Mednikov (1961). The diatom T. rotula is also better than the flagellate I . galbana in efficiency of feeding (Table VII), and for growth and development (p. 113).

    We consider that the short life of adult males is related to the fact that females are fertilized only once during their lifetime, shortly after they mature (see p. 83). Under these circumstances early reproductive efficiency of the males is important, even a t the possible cost of a long life.

    B. Oogenesis and egg laying

    The oogenetic cycle of Pseudoculunus has not been studied, but the superficial appearance of developing eggs has been described by Corkett (1966), who distinguished three stages (Fig. 16). The immature stage containing small developing eggs in the ovary, but not in the oviduct, is found in C III- C V, and in newly matured adult females (Fig. 16A, B). The semi-ripe stage contains some large eggs that may extrude into, but not fill, the oviduct and its diverticula (Fig. l6C). The eggs in the ripe stage (Fig. 16D) may fill the oviduct and its large anterior diverticula. After laying, the animal reverts to a semi-ripe condition. Corkett also found a few females with a degenerating ovary; these females were more abundant at the beginning of the year and perhaps came from the overwintered generation.

    Egg laying has not been described, but as in Calanus (Marshall and Orr, 1952) the eggs are extruded in a soft condition and become round and firm only after they are attached to the genital segment. The structure of egg masses and sacs and their membranes is considered elsewhere (p. 85) .

    C. Sperm and spevmatophore production

    The spermatogenetic cycle has not been described, nor is it known how many spermatophores can be produced by a male during its short


    life (see p. 114), although a single male has been known to fertilize up to three females in the laboratory (Hart and McLaren, 1978).

    Giesbrechts (1882) illustration of a spermatophore shows suggestion of layering of the masses of sperms within (Fig. 17A), and

    Sixth thoracic segment


    Fiith thoracic segment


    G e n h opercufum


    7 i v e r t i c u l u m Egg mass

    Left oviduct

    FIQ. 16. Development of the ovary of Pseudocalartus. A, C V. B, adult female with immature ovary. C, adult female With semi-ripe OVV. D, adult female with ripe ovary. (After Corkett, 1966.)

    Hirschfeld (1974) indicated that the tightly packed sperms are arranged in a helical manner. She counted about 360 sperms in an acetocarmine squash of one such spermatophore. We will see that these would be enough to fertilize the eggs produced by a large (1.1 mm or so) female


    A B Fro. 17. Spermatophores of Pseudocalanua. A, spermatophore extruded from mele

    B, unusually large number of spermatophores attached to a single gonopore. (abnormal, see text) female. (From Giesbreoht, 1882.)

    during her lifetime: about 35 eggs per clutch (Fig. 19A) for a total of 10 clutches or so (p, 93).

    D. Mating

    Some authors have commented on the fact that the elongated spermatophores are rarely found in nature. Adult males are also short- lived (see p. 80). These facts in themselves suggest that mating is normally a once-in-a-lifetime act for each female. Giesbrechts (1882) report of up to 70 spermatophores attached to single females is extraordinary. Giesbrechts illustration (Fig. 17B) is of interest in indicating what appears to be a rudimentary fifth leg. This can be


    associated with parasitic sterilization or intersexuality (p. 194) and pos- sibly the mechanism of mate attraction (see below) could be badly distorted.

    Unlike some species (e.g., Eurytemora herdmani ; McLaren, 1976a) Pseudocalanus seems difficult to mate in the laboratory. In one experiment about four C V females were allowed in the presence of a single adult male in 54 individual 125 ml bottles with adequate food; mating success was less than 10% (Hart and McLaren, 1978). Increas- ing size of culture vessels beyond 100 ml seemed to have no effect on mating success (Hirschfeld, 1974). Hart and McLaren (1978) found that there was evidence for size-assortative mating ; i.e. large males chose large females and vice versa, when given a choice in the laboratory. The evident sexual fastidiousness of Pseudocalanus may be in part related to this size-assortative mating.

    Some of the events leading up to mating have recently been clarified by Griffiths and Frost (1976). They found that males placed in filtered seawater with recently matured females exhibited swimming behaviour similar to that described for other species by Katona (1973) : rapid zig-zags alternating with slow figure-eights and loops. Ten experimental beakers, with five males in each, were subjected to 20 min with male- conditioned, 20 min with female-conditioned, and 20 min with control (freshly filtered) water. The frequency of occurrence of the three kinds of male behaviour is given in Table XIII. Clearly these elaborate patterns of swimming have a sexual connotation and are probably evoked by substances produced by freshly moulted females.


    (After Griffiths and Frost, 1976.)

    Conditioned water

    Male Female Control Behaviour

    zig-zag 1 10 1 looping 5 10 4 figure -eight 4 8 3

    Griffiths and Frost obtained further evidence for such a pheromone in Calanus by demonstrating that there was a significant accumulation of radioactivity in adult males exposed to seawater conditioned by labelled males or females. They showed that this radioactivity was concentrated around the positions of aesthetes on the antennules of


    Calanus males. Their drawing of the first antenna of the Pseudocalanus male (Fig. 7A) shows a rich endowment of aesthetes.

    Griffiths and Frost suggest that the function of the elaborate swim- ming behaviour of males may be to bring widely spaced individuals together. However, we can find no published observations on the way in which the male approaches and attaches the spermatophore to the female, presumably using the remarkable fifth legs (Fig. 7K) during what must bc a very ephemeral coupling.

    E. Reproductive rate 1. General pattern of egg production

    The following terminology (Corkett and McLaren, 1969) is used throughout this review. A true egg sac is a group of eggs clearly sur- rounded by an outer membrane and attached to a female. An egg mass is a similar group of eggs attached 60 a female, such eggs adhering to one another by the outer egg membrane, with no further surrounding membrane. The general term clutch. is used for the eggs contained within a sac or mass.

    The eggs are generally carried by the female until they hatch, although the clutches may in some populations under some circum- stances break up before hatching (Corkett and Zillioux, 1975). When clutches break up they often leave a mass of eggs attached to the female and the rest of the eggs become detached singly or in groups. We assume that eggs are always laid in sacs which can be recognized by the symmetry imparted to them by the outer membrane. In plankton hauls these egg sacs are often disrupted and leave only a fcw eggs (i.e. masses) clinging to the genital segment.

    It is not possible to establish patterns of egg production in nature as observations have to be made over a period of time on individual females. We believe that the normal potential production of eggs by females (not reduced by food limitation) is illustrated by the examples in Fig. 18. These individual females, captured as adults in nature, were among those producing the largest number of egg sacs in their respective experiments, and perhaps had only recently been fertilized in nature.

    The reproductive life of these females can be divided into two phases. First there is a reproductive period of sustained production of clutches of more-or-less similar size (horizontal lines in Fig. 18). This may be followed by a period during which clutches are smaller or even entirely inviable (eggs disintegrate soon after being extruded and were presumably infertile). It is not known if this apparent infertility is due



    to shortages or inadequacies of stored sperm or to physiological short- comings of the females. Death in any case may follow after a quite long, essentially post-reproductive period (after horizontal lines, Fig. 18).

    Reproductive rate per female can be analysed in terms of five variables : (a) the number of eggs in clutches ; (b) the rate of production of clutches; (c) the total number of clutches produced during the reproductive period ; (d) length of post-reproductive period ; and (e) the proportion of eggs in these. clutches that hatch as nauplii.

    Fertile clutch o Inferti18 sac 20-

    - .. t Death of female -..*,-I

    $30; . I

    Time (doys)

    FIQ. 18. Production of successive clutches in the laboratory by female Pseudocalanw captured in nature. A, female from off Plymouth, England, kept at 844OC in excess laochrysis galbuna, replenished weekly (after Corkett and Zillioux, 1976). B and C, females from off Halifax, Nova Scotia, kept at 6-7"C, at 3 X lo4 cells/ml (B) and 3 x 105 cells/ml (C) of I . gulbanu replenished weekly (after Corkett and McLaren, 1969).

    (a) Number of eggs in clutches Figure 18 indicates that, although there is little evidence for trends

    during the full reproductive period of females, the size of individual clutches may be quite variable. There is some suggestion in Fig. 18 (and in other examples depicted by Corkett and McLaren, 1969) that exceptionally small clutches are often followed by exceptionally large ones, and vice versa. Perhaps this involves withholding eggs between oogenetic cycles.

    Although a variety of explanations have been offered for clutch size in Pseudocalanus, the importance of female size was first explicitly recognized by Marshall (1 949). McLaren (1 963) showed that her data from Loch Striven on number of eggs (E) as a function of cephalothorax length (L, in mm) were closely described by E = 19.36.LB.g4.


    Subsequently McLaren (1965) and Corkett and McLaren (1969) concluded that this same function described egg numbers in unbroken sacs from Long Island Sound, Nova Scotia, and the Canadian arctic, provided local difference in egg size were taken into account. Re- analysis of these data shows that clutch volume is indeed more closely related to length than is the number of eggs in the clutch (Fig. 19).

    Loch Striven, Scollond 0 Halifax.Nova Scatia A Ogac Lake,Baffin lslond eFoxe Basin OSouthwes? Baffin Island

    Long Island Sound *Unpam Bay


    O n

    A A 0 . 0



    0 / E = 0.0201 L449



    Cephalolhorox length(L1 in mm

    FIQ. 19. Clutch sizes in number (A) and calculated volumes (B) as functions of cephalo- thorax length of adult female Pseudoculunw. (After McLaren, 1966, and Corkett and MoLaren, 1969.)


    The relationship between clutch volume and length is significantly greater than cubic (95% c.1. of the exponent in Fig. 19B are 3.44-4.94). This relationship can be compared with that describing body weight as a function of length, which is also significantly greater than cubic (exponent 3.40-3.88, see p. 127). Although an upper limit to clutch volume may be imposed by space within the body, as suggested by McLaren (1965), the fact that mean clutch volume in a female is smaller than the largest clutch volumes (Fig. 18A, C) suggests that some other adaptive control is operating. Perhaps sizes of clutches are controlled due to hydrodynamic restrictions required for swimming, especially for escape.

    Corkett and McLaren (1969) found that mean numbers of eggs in a sac were uninfluenced by wide variations of food supply (Fig. 20). Five females kept by them a t an even lower food supply of 3 000 cells 1. galbanalml failed to produce any sacs in 5-7 days.

    The coincidence of large clutches and spring diatom outbursts (Marshall, 1949) is a consequence of large female size in the first new generation developed at spring temperatures (see Section XI for many examples).

    Corkett and Zillioux (1975) found that temperatures had no effect on clutch size of females captured off Plymouth, but that those produced at higher temperatures tended to release more of their eggs prior to hatching times (Table XIV).

    It seems possible to conclude from the above work that mean clutch size during the reproductive period of the female is determined by her size, and is influenced little if a t all by circumstances surrounding her during this time. Next we examine work on Pseudocslanus against this conclusion.

    TABLE XIV. EFFECTS OF TENPERATURE ON EGG PRODUCTION B Y Psetl,doca~anus FROM OFF .PLYMOUTH. (After Corkett and Zillioux, 1975.)

    1.3 2 12.3 4 0-7 24.5 11-38 4.0 7 11.3 & 2.2 5 1.1 35-4 9-57 8.4 13 13.8 f 2.1 12 2.3 38.2 7-88

    16.2 7 11.5 -J= 1.7 42 3.4 36.9 3-71


    Paffenhofer and Harris (1976) measured reproduction performance of a number of females reared at 1 2 O C . Average clutch size was 16-26, but there was variation within and between experiments. Apparently they included small clutches produced late in life in determining mean clutch sizes. This is perhaps reflected in the smaller mean clutch sizes in an experiment started with 10 " older '' females. Since no data are given on the sizes of individual females, it is not possible to explore their observations further.

    Thompson (1976) found in extensive experiments that females from North Sea stock produced on average about half as many " viable eggs " per clutch as might be expected from the relationship indicated in Fig. 19A. Her estimates are actually based on counts of nauplii, and will be considered later (p. 94).

    Sazhina (1971) gives a clutch size of 27 for Pseudocalanus from the Black Sea. Elsewhere (Sazhina, 1968, 1974) she lists values of 27-30 eggs at ZO"C, 16 a t 15-17"c, and 9-11 at 18-22C. The trend within this (elevated) temperature range is interesting, but we are given no details on sizes of fernales (tabulated simply as 1.2 mm) or the conditions of capture or rearing.

    We conclude by emphasizing the importance of specifying body size (and egg size if possible) in any experiments or analyses on egg produc- tion by Pseudocalunus.

    fb) Rate of production of clwtches A female obviously cannot produce a new sac while one is being

    carried on her genital segment. Even if the egg sac is dropped pre- maturely, a new one does not usually appear until nauplii in the detached sac are hatching; Corkett and Zillioux (1975) noted a single exception.

    The rate of production of sacs is determined by the time taken for embryos to develop to hatching and by the time between hatching of one clutch and appearance of the next. Embryonic duration is controlled by temperature but time between clutches can be subject to other influences, of which food supply can be assumed to be important.

    In a high food supply, a new sac can appear within an hour of hatching of the previous one. This lapse of time was determined pre- cisely for a few females from Halifax, Nova Scotia by Corkett and McLaren (1969) and can also be estimated from the numbers of sacs produced by females at various food concentrations (Corkett and McLaren, 1969, their Fig. 2). To estimate this time, it is assumed that the first and last sac during the reproductive period (i.e. at the ends of the horizontal lines in Fig. 18) were discovered a t random with respect


    p z

    to their stage of embryonic development. The proper estimate of num- ber of clutches during this period is then one less than the number observed. Each of these clutches can be assumed to have taken about 4.7 days at the given experimental temperature of 6 7 C (see Fig. 22). The remaining time can be allotted to periods between clutches. Evidently little time is lost between clutches at high food densities,

    015,000 Cclls/ml 5 - mo 30,000 Cellr/ml

    ~ IS0 .000 Celb/ml


    (After Corkett and McLaren, 1969 ; see text.)

    Isochrysis galbanaa celEs/ml

    600 000 300 000 150 000 30 000 15 000

    Days between clutches

    Number of females Mean. Range

    3 0.6 0.3-0.8 9 0.8 04-4.1

    6 3.7 1.0-5.1 3 4.6 3.2-6.1

    3 1.2 0.1-2.4

    ~ ~~~~

    Food level replenished weekly.

    although a few individuals may show longer delays than most (Table XV). The average time between hatching of successive egg sacs is about 20% longer than the time of embryonic duration when food is adequate (>30 000 cells/ml, replenished weekly ; Table XV). Produc- tion rate of clutches begins to drop at levels below 150 000 cells/ml, but probably not much above 30 000 cells/ml, when Iaochryaia galbana is


    used. It is interesting to note that a t only 15 000 cells/ml the number of eggs in a clutch is not reduced (Fig. 20).

    Now we may examine other, less extensive estimates of rate of production of clutches against the observations given above.

    Sazhina (1971) assumed an interval of 3-5 days and later (Sazhina, 1974) 3-5 days between successive clutches for Pseudocdanus from the Black Sea. She did not consider possible effects of temperature on the interval but these estimates refer to 8-10C (see Fig. 22).

    Corkett and Zillioux (1 975) derive an estimate of the maximal rate of production of sacs for well fed animals from Plymouth by dividing 12-6 (the mean number of eggs in a sac) by the time taken for develop- ment to hatching at their four experimental temperatures. They found that the observed rates of egg production were only about 50-70y0 of these maximal rates (compared with 83% for Halifax females, above). However, they based their estimates on rate of egg production during the whole laboratory life of the female, including the post-reproductive period.

    The extensive work of Thompson (1976) allows us to estimate the time between hatching and sac formation for seven females reared and mated in the laboratory. Here the reproductive period was explicitly designated, as time of appearance of last clutch was noted. It is possible, however, that females could have slowed down rate of production of sacs before this in some cases (cf. Fig. 18). From Thomp- son's data, we estimate that there was generally a mean lapse of a day or so between clutches of females (Table XVI). Longer periods occurred


    Temp. "G

    Est.a time

    to hatching

    Total no. of sacs

    Obs.b Obs. time Obs. time mating to first to carrying of post-


    Eat. time between

    first clutch, laet clutch, clutch,es, day8 days time, days


    6.1 8.6

    10.8 13.5 13.5 14.5 14.5

    5.2 4.0 3.2 2.5 2.5 2-3 2-3

    7 10 5

    16 6

    16 3

    4 43 1.9 38 3 40 0.5 10 4 24 2-8 3

    16 54 1.3 70 16 16 0.7 64 2 44 0.6 67 2 6 0.2 41

    From Fig. 22. Time between appearance of last clutoh and death of female.


    between clutches of the female at 10*8"C, which died shortly after her fifth clutch appeared and may have been abnormal. Excluding this female, the times between appearance of successive clutches averaged about 28% longer than the times for development to hatching of eggs of the various temperatures. This is a good match for the 20% estimate for females from Halifax (above).

    Paffenhofer and Harris (1976) tabulate the means in four experi- ments of number of sacs produced by females, numbers of eggs per sac, and periods of nauplii production in days. If the last are to be inter- preted as mean times between hatching of first eggs and hatching of last, then an estimate of times between successive clutches can be made, as above, by subtracting one sac from the mean number produced, In the one experiment with Thalassiosira rotula as food, four clutches (five minus one) were produced in 14.33 days. It is assumed that this experiment was carried out at 12-5'C like their rearing experiments and that embryonic duration is about 2.8 days (Fig. 22). This implies a mean period between appearance of successive clutches about 24% longer than the time for development to hatching. In three other experiments using Peridinium trochoideum, (concentration?) the mean delays between hatching of one clutch and appearance of the next were 3.3, 4.7 and 6-0 days. This seems to confirm the conclusion of Paffenhofer and Harris (1976) that P. trochoideum is a poor food for Pseudocalanus.

    From all these sources, we conclude that successive clutches of well fed, fully reproductive females should appear at intervals equal to about 1.25 multiplied by the duration of embryonic development for the given temperatures.

    The lapse of time between mating and the first clutch has been estimated for seven laboratory-reared females by Thompson (Table XVI). If we exclude the two females at 13.5"C as abnormally retarded, the first clutch in Pseudocalanus may appear in about the time taken t o hatch a clutch. Since the female is fertilized very soon after moulting to adulthood (see p. 83), a period between maturation and first clutch similar to that between hatching of successive clutches might be assumed for demographic or productivity studies.

    (c) Total number of clutches We have shown that females in the laboratory produce a number of

    normal or complete egg sacs, and then may produce smaller or infertile ones during an essentially post-reproductive period (Fig. 18).

    Among females captured in nature, some will have already


    expended part of their reproductive potential. Those females producing maximal numbers of egg sacs are more revealing of reproductive potential. Of 33 females whose reproductive histories are depicted by Corkett and McLaren (1969), eight produced between 8 and 11 full-sized clutches and between 0 and 3 small, late ones. This strongly suggests that the normal reproductive potential for females off Nova Scotia is about 10 successive clutches.

    Sazhina (1971) suggests that Pseudocalanus in the Black Sea may produce 21 clutches, but this estimate is based on an assumed interval of 3.5 days (embryonic duration at 10C) and an unsupported estimate of 75 days for the length of the reproductive period.

    The largest number of clutches produced by an individual captured off Plymouth was 9 (see Fig. 18A), all of which hatched successfully (Corkett and Zillioux, 1975).

    Laboratory raised and fertilized females can, in principle, give more precise estimates of potential number of egg sacs. Results of three such experiments are tabulated by Paffenhofer and Harris (1976). In one experiment using Peridinium trochoideum as food, 15 females produced an average of only 2.27 (range 2-4) egg sacs. In another experiment three females produced only one, two, and two sacs respectively. This is good reason (along with the delays between sacs noted on p. 90) for thinking that P. trochoideum is an unsuitable food. In another experi- ment using Thalassiosira rotula as food, six females produced an average of five clutches (range 2-9), which is lower than might be expected from the maximal performances of wild-caught females. Paffenhofer and Harris state that unfertilized eggs were colIected when females were about to finish egg production, but it is possible that some of their females did not fulfil their reproductive lives. The experiments were carried out in bowls, in which T . rotula may not have stayed in suspension. Another experiment with 12 females in a rotating beaker prolonged the period of reproduction, but no data are given on total numbers of clutches.

    The seven females fertilized in the laboratory in Thompson's (1976) study (Table XVI) produced an average of 8.9 egg sacs, close to the potential indicated for wild females. The variation in number of sacs in her experiments may be " natural ", whether related to pre- mature death (female at l0-S"C) or to premature infertility (females at 13.5, 14-5OC). We are given no information on whether the late clutches of the females producing 15 and 16 sacs were full sized.

    For purposes of calculating demographic or production parameters, it may be perfectly acceptable to assume a potential of 8-10 clutches. In fact, observed or assumed mortality rates will ensure that very few


    females will reach this potential, or food may become seasonally scarce long before this potential is reached.

    (d) The length of the post-reproductive period Evidently females can live for some time after reproduction has

    essentially ceased. We have suggested above that the eight out of 33 females that carried 8-11 successive complete clutches in the experi- ments of Corkett and McLaren (1969), had been captured soon after maturity. The mean reproductive span of these eight females was 51 days, and they lived an average 41 days beyond this.

    The seven females reared and mated in the laboratory by Thompson (1976) had mean reproductive periods (mating to last clutch) of 39 days and post-reproductive periods of 40 days (TableXVI). Elsewhere we suggest that the potential length of life may be set physiologically by temperature (p. 115), and the post-reproductive period would accordingly be shorter in females that have been thwarted from sus- tained reproduction by food shortages. However, for females producing a full complement of about ten clutches at a maximal temperature- dependent rate, the evidence suggests that an essentially post- reproductive period can occupy the second half of adult life; however, given natural mortality rates this post-reproductive life is unlikely to be expressed in nature (but see work of Martens, 1975, discussed on p. 208).

    (e) Proportion of eggs hatching Corkett and McLaren (1969) and Paffenhofer and Harris (1976)

    found that infertile or otherwise unviable eggs are normally produced only when females approach the end of their reproductive lives. Death of some embryos at other times does occur, and might be expected among females confined to small experimental vessels. It would seem unlikely that infertility or embryonic death are frequent in natural populations. Therefore, it is a little surprising that Thompson (1 976) found that the rate of production of viable eggs by females from the North Sea was considerably lower than might be expected.

    Thompson gives estimates of average numbers of viable eggs per sac for a very large sample of females of known cephalothorax lengths. Those between 0.72 and 0.78 mm produced on average 5.1 such eggs and those 1.00-1.12 mm on average 9.3 eggs, or about half the mean number carried in sacs of females from Nova Scotia or Scot- land (Fig. 19A). Her estimates of viable eggs for females mated in the laboratory and for females captured seasonally are also substantially below expected levels.


    Thompsons counts of viable eggs were based on counts of nauplii found on periodic examination of females. We have found (unpublished observations) that females may eat some and on occasion all their nauplii, often very soon after they have hatched. This is presumably the major source of discrepancy between Thompsons results and those summarized in Fig. 19. A useful study of viability of eggs of Psezcdocalanus could be made with containers adequately large for females to oxygenate their eggs by swimming, and by removal of sacs shortly before they hatch, so that no eggs are lost.

    2. Theoretical rates of reproduction Embryonic durations can be established accurately, and we have

    suggested that the time between successive clutches (or hatchings) might be about 25% longer than these durations when food is adequate. We have also shown that numbers of eggs in a clutch can be predicted for local populations, and that inviable eggs can probably be ignored. Thus estimating the maximal potential rates of reproduction per individual female might seem straightforward : simply divide the observed or calculated mean egg number in clutches by 1-25 multiplied by embryonic duration at the given temperature. This is in effect what is suggested by Sazhina (1974).

    However, this needs further refinement, as some females may not have produced their fist clutches and others may be post-reproductive. In populations with continuous, overlapping generations the relative abundance of fully reproductive females will depend on the age structure of the adult female population. If mortality rates or recruitment of new adults are high, the pre-breeding females will be relatively common. Post-reproductive females will be more prevalent if mortality or recruit- ment rates are low.

    We have suggested for purposes of approximation that the pre- reproductive phase might on average last as long as the interval between appearance of successive clutches and that the post-reproductive phase might occupy the second half of a females life. We have used these approximations to estimate the proportion of females that might be fully reproductive in populations of various age structures. For simplicity we assume that the number in each successive age-group is a constant fraction of the preceding one (which is the same as assuming that constant mortality and recruitment rates have prevailed for some time). For a series of such populations, in which the oldest reproducing females (tenth clutch) ranged between 1% and 50% as common as the newly matured ones, elementary analysis shows that reproducing females constitute between 59% and 73% of the population.


    We suggest that it might be assumed that an average of 65% of females in populations with continuous, overlapping generations are fully reproductive. It is on this basis along with the assumption that 25% of fully reproductive females will be between clutches a t any given time that we have calculated the potential rates of reproduction depicted in Fig. 21.

    Temperature PC)

    FIG. 21. Average number of eggs produced per day by populations of food-satiated females of various lengths as functions of temperature. Unbroken curves are for females from off Halifax, Nova Scotia, and broken curves for females from south- west Ba6n Island (see Fig. 19).

    3. Reproductive rates in nature Although there are a number of published observations on the

    number of eggs borne by females in nature, these generally fail to account for inevitable disruption of sacs and masses in preserved samples. To ensure accurate estimates, free and attached eggs must be counted in samples taken with suitably fine-meshed nets. There are numbers of estimates of egg numbers in the literature for which no such information on methods is given.

    Reproductive rates have been estimated for one population in which egg production was highly discontinuous. From counts of adults, nauplii and free and attached eggs in successive fine-mesh samples from Ogac Lake, Baffin Island, McLaren (1969) estimated that clutch size was 19.6 f 5.0 (mean and 95% confidence limits from his Table 2) . The wide confidence limits for this estimate from 14 " broods '' (eggs or young from roughly synchronous clutches ; see p. 135) are not surpris- ing considering the many possible sources of error, but the mean


    estimate is gratifyingly close to the expected clutch size of about 18 eggs for females of about 0.85 mm (mean for the season from McLaren's Fig. 6) as suggested in Fig. 19A. McLaren (1969) also estimated that the time between successive broods was approximately a week, which is about as expected at the temperature of 2-7C that prevailed in the

    2 4 6 8 10 12 14

    Temperature ( T I in "C

    FIG. 22. Embryonic durations of Pseudocalanus from three localities. BBlehrQdelr's temperature function for Halifax animals from McLaren et a2. (1969). Function with b = -2.06 fitted to data in McLaren (1966) for the large form from Ogac Lake and to data for North Sea animals from Thompson (1976).

    upper waters of Ogac Lake at the time of his studies (i.e. 1.25 x 4-5 to 8 days, the times taken for embryonic development a t 7 O C and 2C; Fig. 22, Table XVIII). After two or three successive broods in early summer in Ogac Lake, the food supply diminished rapidly, and the consequence was evidently not simply reduced reproductive rate, but

    A.Y.B.-15 6


    virtual cessation of reproduction, and finally death of the overwintered females (see p. 138).

    In continuously breeding populations, it should be possible to use egg counts (free and attached) and temperatures to estimate repro- ductive rates, in the manner suggested by Edmondson et 02. (1962). This has not evidently been done for Pseudocalanue. However, Marshall (1949) lists total numbers of free and attached eggs in fine-meshed samples taken weekly from Loch Striven, Scotland, along with mean numbers of eggs on those females that were carrying full, unbroken egg sacs. This allows us to estimate the proportion of females that were carrying egg sacs at the time of sampling. This has been done for the purpose of understanding life cycles (see later, p. 143). On average about 40% of females in the population bore egg sacs during the season of sustained reproduction, in March through August (Fig. 29, p. 142). From laboratory evidence (previous section), we have estimated that about 65% of females should be in full reproductive condition and that a further 25% of these should be between clutches, so that we expect that some 50% of females should be bearing egg sacs in any given sample. The slightly lower estimate from animals from Loch Striven suggests that the pre-reproductive period or the period between clutches has been underestimated in laboratory experiments, or possibly that predation takes a toll of eggs from prematurely broken sacs.

    Preliminary observations by Corkett (1 969) suggest that egg numbers may at times indicate near maximal reproductive rates for a population of females in which there are no pre-reproductive or post- reproductive individuals (i.e. 1.25 multiplied by the observed number of eggs per female in Table XVII, close to the predicted numbers on April


    (After Corkett, 1969.)

    Number of eggs per female Predicteda 0 bse~ved


    25 March 15.2 6.0 3 April 18.5 13.9 9 April 19.5 14.6

    15 April 24.5 9.5

    Relative size of

    oil sacb (mean f 95% c.1.)

    0.01 f 0.003 0.02 & 0.006. 0.03 f 0.005 0.04 f 0.008

    a Based on mean size of 99, from Fig. 19A. Determined as by Corkett and McLaren (1969).


    3 and 9). However, on March 25 and April 15, observed numbers were less than expected even for a population composed in part of non- reproductive females (i.e. 25% non-reproductive on average, as esti- mated in previous section). On March 25 some females had no visible stored oil, and 88% of oil sacs were less than 0.02 in relative volume (Table XVII). However, on April 15 oil sacs were relatively large and 17% of females had oil sacs less than 0.02 in relative volume. This suggests that the presence of stored oil in these females reflected a level of food in excess of that required to support maximal reproductive rates.

    TABLE XVIII. PARAMETERS OF B~LEHRADEKS TEMPERATURE FUNCTION, WITH b = -2.05, DESCRIBINQ EMBRYONIC DURATIONS OF Pseudocalanw. (Data from McLaren, 1966; McLaren et al. 1969; and, for the North Sea, from Thompson,


    Temp. at

    pm f. 95% c.l. sampling

    Parameters Mean egg

    a Locality diameter time of a

    Halifax, N.S. 121.6 & 1.8 0.1 2 144 - 13.40 Woods Hole, Mass. 127-4 & 3.7 -0.7 2 312 - 13.87 Frobisher, N.W.T. 130.4 &- 3.3 - 1.7 2 280 -13.84 Ogac Lake, N.W.T.

    Ogac Lake, N.W.T. (small form) 108.5 & 2.3 4.6 2 105 - 13.00

    (large) 155.3 & 2.6 4-6 3 467 -13.17 Millport, Scotland 123.6 f 1-8 8.9 2 290 - 13.63 North Sea - 1 o a 1 845 -11.45

    Approximate annual mean temperature of southern North Sea; not given in Thompson (1976).

    F . Retrospects and prospects

    A number of mysteries remain concerning reproduction by Pseudo- calanus. The nature of the mating act and the reasons for low mating success in the laboratory are unknown. The reasons for unbalanced sex ratios in some laboratory rearings (Thompson, 1976) are obscure. Perhaps qualitatively or quantitatively inadequate food promotes a tendency for a greater proportion of females to be produced. This strategy could be adaptive for Pseudocalanus, since females live longer (p. 114) and, even ifthey mature at a time when foodis inadequate for their young, they need not waste all their reproductive efforts then.


    Because of the evidently simple rules governing clutch size and clutch frequency in Pseudocalanus, control of its potential reproductive rate is well understood. Evidently these potential rates may at times apply in nature. We need more studies from nature to investigate this supposition using frequent sampling with fine-meshed nets, like that of Marshall (1949). Possible indicators of maximal reproductive rate such as presence of adult males a t a certain frequency or sizes of the oil store in adult females, should be explored.

    Pseudocalanus has been noted as having a generally lower reproduc- tive rate than that found in some other common copepod genera such as Acartia, Centropages and Temora (Corkett and Zillioux, 1975; Dagg, 1977). After demonstrating that Pseudocalanus females (unlike those of Acartia tonsa and Centropages typicus) did not show reduced repro- ductive rate when fed intermittantly (12h/day), Dagg (1977) concluded that Pseudocalanus is adapted to patchy and irregular food availability. Since we have already shown (p. 73) that Pseudocalanus has a marked die1 feeding rhythm, Daggs laboratory feeding schedule may not have been altogether appropriate as a model of such patchiness. However, clearly the restrained reproductive rate of Pseudocalanus does require more exploration in the comparative manner begun by Dagg.


    Readers will find this section of our review perhaps the most difficult and condensed, but we believe that it is through the observa- tions and analyses outlined here that the role of Pseudocalanus as an important producer in the food web of northern seas may be best understood.

    It is possible to describe rates of development in terms of the moult into successively different morphological stages (Egg, N I-C VI). Growth is a conceptually separate phenomenon from development, and indeed some authors have expressed growth rates of copepods directly as a continuous increase in weight (wet or dry, or of some element). However, if the weight of particular stages can be determined, then growth rates can be estimated by using the times taken to reach these stages. We therefore pay considerable attention in this review to the determinants of development rates and body sizes as separate processes.

    We will show that temperature is of profound significance in determining development rates and sizes, and therefore growth rates, of Pseudocalanus. I n considering these matters, we make some use of BBlehrBdeks (1 935) temperature function. Empirical justification for the use of this function has been given by McLaren (1963). We use it in


    this review partly because it has already been used in publications about Pseudocaianus, and partly because of the need of some analytical function for interpolation and prediction. Since the use of BBlehrAdeks function has recently been subjected to some criticism (Bottrell, 1975), we describe its properties briefly here.

    BBlehrBdeks equation is one of several three-parameter equations that can adequately describe responses of physiological rates to temperature. The development time (D) in days of a development stage or stages (eggs, N I-C VI), of Pseudocalanus is represented as a function of temperature (T) in C by: D = a(T-u)b, where a , u and b are fitted parameters.

    On a linear plot the constant u (often called the biological zero since it is the theoretical temperature a t which development time is infinite) describes the position or origin on the temperature scale. D = a when T = 1 + u and therefore the constant a is the theoretical development time one degree above u ; log a is also the intercept on the y-axis of a plot of the log of development time against the log (T-u), the para- meter b is the slope of this line.

    The parameter b in this equation can be assigned a constant value. The assignment of a constant value to b is arbitrary; however, as pointed out by McLaren et ai. (1969) when b is made a constant then a for embryonic duration among closely related animals is related to egg size. Furthermore, they show that a is strongly correlated with habitat temperature among more distantly related copepods.

    A. Embryonic development rate 1. Zffects of temperature

    Figure 22 shows that BBlehrBdeks temperature functions with b = -2.05 (from McLaren et al., 1969) describes quite well the differ- ences between three geographically separate populations of Pseudo- calanus. The wide 95% confidence limits for means of North Sea animals in Fig. 22 generally exceed the ranges in development times for individual clutches given by McLaren (1966) and McLaren et al. (1969). These wide intervals and the anomalous duration at 8.6C probably result from less frequent experimental observations (Dr B. Thompson, personal communication). However, this also illustrates the usefulness of having a general temperature function, like BBlehrQ- deks, for interpolation with such data.

    The assumed value of b = -2-05 (see above) has been used to fit the parameters of BBlehrAdeks function to development times of different populations of Peeudocalanzcs (Table XVIII). Clearly, the great


    difference of the large form from Ogac Lake (Table XVIII, Fig. 22) from all other populations is its proportionately slower development at all temperatures. If curvature ( b ) is held constant, the position on the Celsius scale (x) of its temperature response does not differ palpably from that of the small form, but the value of a is substantially greater (Table XVIII). The regression of a on egg size for the populations of Pseudocalanus given in Table XVIII, even when the large form from Ogac Lake is excluded, is significant at p = 0.05.

    McLaren et al. (1969) showed that with b = -2-05 the parameter u for 11 species of copepods from the arctic to the tropics was related to average environmental temperature and suggested that u may be used in this manner to indicate temperature adaptation. The regression of u on the temperature at time of sampling for populations of Pseudo- calanus given in Table XVIII is not significant (p - 0.09).

    Other estimates of development time in the literature (Marshall, 1963; Katona and Moodie, 1969; Sazhina, 1971, 1974) are not sdE- ciently accurate (usually given to the nearest whole day) to express possible regional differences. The earlier work of McLaren (1965) gives estimates of the relative times taken to hatch at different temperatures of embryos of Pseudocdanus that had undergone partial development, and has been superseded by the subsequent work cited above.

    2. Effects of salinity McLaren et al. (1968) found that the effect of salinity on develop-

    ment times of Pseudocalanus from Halifax, Nova Scotia, was slight. Only in one of several experiments was development significantly slower at abnormally high salinities (about 9% slower at 39x0 than at 29-35%,). Survival of embryos, however, may be affected by salinities (see p. 24).

    3. Xeasonal and short-term temperature acclimation Recent work (Hart and McLaren, 1978) shows that embryonic

    duration of Pseudocalanus varies to some extent with the temperature experienced by females. The seasonal differences in development time are given in Table XIX. If one considers the females collected in April to be cold acclimated and those collected in October to be warm accli- mated then one would expect that development in the laboratory at 10C and 6C would be relatively shorter for the April animals than the October ones. This does not occur and Hart and McLaren (1978) con- clude that the seasonal differences in development times can not be attributed to temperature acclimation, but is possibly explained by the larger size of females and their eggs in the colder season (see p. 105).


    Hart and McLaren (1978) also looked a t short-term acclimation by keeping females a t lO"C, 6C and 2C during the period of oogenesis. They found that eggs hatched slightly but significantly later at 10C when females had been kept at 2C or 6C. Thus short-term differences in development appear to be attributable to temperature acclimation unlike the seasonal differences noted on Table XIX.


    (From Hart and McLttren, 1978)

    A ~ ~ T o x . Mean Mean development times Temp. at cephalothorax i n hours (f 95% c.1.)

    collection females (mm) 10C 6C

    Month of collection of females time of length i n

    April October

    2 1.12 82.0 f 2.3 125.0 f 1-7 13 0.86 73.4 f 1.3 117.0 f 1-6

    4. Effects of body and egg size The constant a in Brjlehrtidek's equation is the theoretical develop-

    ment time one degree above a (p. 101). It must be stressed that under no circumstances do we visualize actual development of Pseudocalanus taking place either at a (biological zero) or one degree above u. How- ever, it is of interest that, when b is given the constant value of -2.05, then a is positively correlated with egg diameter amongst geographically different populations of Pseudocalanus (p. 102, Table XVIII). Thus, as suggested by McLaren (1965) and McLaren et al. (1969), by accounting for local differences in temperature through fitted values of a, the fitted values of a reflect the effects of egg size. The effect of size is of course most clearly shown by the embryonic duration of the large form from Ogac Lake (Fig. 22). If Bi5lehr&dek's equation is used with the values for the parameters given in Table XVIII for the large and small forms of Pseudocalanus from Ogac Lake, then it can be shown that the ratio of the embryonic duration of the large to small form is about 1.6:1 ab any temperature between 0 and 10C. This ratio is more similar to that of egg diameters than to that of egg volumes (-3:l). McLaren (1 966) points out that proportionality of development time and egg diameters might be expected if control were through surface : volume restrictions.

    Corkett and McLaren (1969) give a positive correlation between egg diameter and cephalothorax length for the Halifax, N.S., population


    I A * * * I A

    80 I . + I .

    * * 4

    March April

    Odune July * * 7 Aua. 70 * oci.



    - E E 0.13 v

    v m

    4 4 .

    Fro. 23. Relations botween embryonic duration at 10C (A) and egg diameter (R) with size of adult females. (After Hart and McLaren, 1978.)


    and recently Hart and McLaren (1978) have investigated this relationship in detail for samples taken from March to October (Fig. 23). The;y showed that within the local Halifax population embryonic duration at 10C (Fig. 23A) and egg diameter (Fig. 23B) are strongly correlated with cephalothorax length.

    It might be expected that egg size by itself would be responsible for differences in development times through, for example, the surface :vol- ume ratio decreasing with increasing diameter (McLaren, 19GG). Hart and McLaren (1978) present evidence that shows that factors other

    FIG. 24. Hatching of Pseudocalanus. Note the bulging of the inner membrane, followed by the crumpling of the outer membrane, and finally the rupture of the inner mom- brane, which is left protruding from the outer membrane. (From Marshall and Om, 1964.)

    than egg size alone determine development time. They showed (using partial regression analysis) that female size had a significant effect on embryonic duration independent of egg size and that embryonic duration was significantly correlated with size of male parent as well. In addition they found that individual egg size within a clutch had no effect on the development time of that individual egg.

    In the previous section we discussed seasonal and short-term acclimation and we now see how such acclimation may be affected by size. Since size of female P ~ e u ~ ~ ~ u l u ~ ~ ~ ~ changes seasonally near Halifax (Table XIX) and elsewhere (p. l l G ) , seasonal differences in embryonic development rate can be partly attributed to such changes.

  • ' " 1 A D=u(T+ 13.40)-2'05 t "1 Ad.?, u=19350\

    501 \

    * \ m t \ crn.u=12850 \:

    x " r = \ 9190

    ' * \


    I 0 l O O 2 4 6 8 10 12

    c III, u- I1890 \


    Temperature ( "C)

    FIQ. 26. Times between hatching and the beginning of various stages of Paeudocalanw from (A) new Halifax, Nova Scotia (each point an individual, after McLaren, 1974) and from (B) the North Sea (open circles are means, closed circles individuals, after Thompson, 1978). BBlehr6dek'e funQtiOIIf3 aa for embryonic duration (see Fig. 22). exoept for differences in a for each stage.


    In conclusion Hart and McLaren (1978) have shown that short-term temperature acclimation affects embryonic duration in Pseudocalanus slightly, and in the expected compensatory way, but that seasonal differences can be attributed to environmentally and perhaps genetically (p. 124) determined differences in sizes of parents and eggs.

    B. Hatching

    Hatching in Pseudocalanus has been described by Marshall and Orr (1954). The embryo is surrounded by two membranes and during hatching the outer one splits, the inner one bulges out, increasing in volume to about twice that of the embryo, and eventually the nauplius struggles and breaks out through the inner membrane (Fig. 24). The discarded inner membrane may remain attached to the outer (Marshall and Orr, 1954) or the inner membrane may become completely detached from the outer during hatching (Corkett, 1968, who gives a photograph of a newly hatched nauplius, a hatching one, and two embryos).

    C. Development rate of nauplii and copepodids

    The phyaiological and hormone control of development rate (i.e. moulting rate) of some Crustacea is reasonably well understood. However, the subject has barely been explored in Copepoda (Carlisle and Pitman, 1961) and evidently not at all in Pseudocalanus. Of particular interest would be information on physiological or hormonal causes of suspended development during the winter at middle and a t higher latitudes (see p. 157).

    However, for many purposes it is of greater interest to enquire into the two obvious controls of development rates in nature-temperature and food supply-which are the substance of the following sections.

    1. Eflect of temperature Although Pseudocalanus has been reared in a number of laboratories,

    the effect of temperature on times taken to reach various post- embryonic stages of development has been examined only in populations from Nova Scotia (Corkett and McLaren, 1970 ; McLaren, 1974) and the southern North Sea (Thompson, 1976). These researchers used excess amounts of food and argue that the development rates of the copepods were maximal at the various temperatures. Their results are sum- marized in Fig. 25. Corkett and McLaren (1970) supposed that time taken to reach any given stage might be the s-me multiple of embryonic


    duration a t any given temperature. Assuming that B6lehrBdek's function applies with a = 13.4 and b = -2.05 (i.e. the same as for embryonic duration in Fig. 22), this is the same as assuming that the temperature responses of times to develop to older stages can be adequately described by differences in a alone. This can be amplified as follows.

    If for stage I,

    and for stage 11,

    :. A t any temperature T

    D, = a, (T - a)b

    D,, = a,,(T - a)b

    DIP,, = %/a11 if b and cc are common to all stages. Figure 25A strongly supports this view for Pseudocalanus.

    Thompson (1 976) estimated average times (by planimetric integra- tion of numbers versus time) taken to reach various stages from samples taken at regular intervals from large populations. She did not separate males and females in these estimates. In spite of methodological differences, her results (Fig. 25B) are very similar to those for Pseudo- calanus from Nova Scotia. Here, too, the times taken to reach various stages are well described by the equation for embryonic duration (see Fig. 22), with changes only in the proportionality constant, a. However, there is an awkward " step " in the relationship for older stages at about 8C. This suggests that the animals at colder tempera- tures were somehow thwarted from more rapid development. Possibly there was some abnormality of response in the laboratory cultures a t these rather low temperatures for this North Sea population. Additional evidence for this assertion comes from the fact that Thompson (1976) was unable to obtain successful hatching of eggs a t temperatures below 3.7"C, or successful rearing of stages above N V at 3.7"C.

    Table XX gives estimates of the relative amounts of time required to reach successive stages of development, expressed as multiples of the time for embryonic duration; that is, the a of Bglehrhdek's function for each stage, calculated as in Fig. 25, is divided by the a for embryonic duration from Fig. 22. Because of the possibly abnormal retardation of development below 8C among North Sea animals (see above), we have calculated for use in Table XX the a values for successive stages only for data from higher temperatures in Thompson (1976). This gives estimates of a for the older stages that are 3-5-4.8% smaller than those in Pig. 25B.



    (Data from Fig. 25.)

    Beginning of stage Nova Scotia North Seaa

    N I1 N 111 N IV N V N VI C I c I1 c I11 c IV c v c VI

    - 4.29

    5-99 -

    - -


    0.18 0.55 2.01 2.82 3.51 3.91 5-14 6-14 7.12 8.14 9.46

    a Multiples of embryonic duration only for data >S"C (see text).

    The estimates for Pseudocalanus from Nova Scotia and the North Sea, of the relative times taken to reach various stages are very similar (Table XX). Among all nauplii, N I11 (the first feeding stage, see p. 112) has the longest duration (1.5 embryonic durations). All copepodid stages have roughly the same relative durations. It is probably sufficiently accurate for some purposes to assume that each copepodid stage has about the same duration as embryonic duration a t any temperature ; from Table XX the five stages average 0.95 embryonic durations (i.e. (9.03-4+29)/5) in the Nova Scotia animals, and 1-11 (i.e. (9.46-3-91)/5) in those from the North Sea.

    We believe that the estimates in Table XX, or perhaps the approxi- mations noted above, can be used to predict the duration of develop- mental stages of Pseudocalanus in conditions of excess food, provided embryonic durations are known for at least two temperatures (the minimum required to fit BGlehrBdek's function with b assumed to be constant at -2.05). Since embryonic duration, ignoring the large form of PseudocaEanus, differs little among regions (Table XVIII), especially at higher temperatures (Fig. 22), we propose that esti- mates for older stages from different geographical localities should not differ much from those shown in Fig. 25. It is possible to examine this proposition using scattered estimates for other localities. In using published estimates, the possibility has to be considered that food shortages, disease and other such factors can prolong development times beyond those possible a t the given temperatures. Indications of


    such retardation might be the occurrence of a wide range in develop- ment times, or of some " stragglers " that moult long after the others.

    The first recorded laboratory rearings were those off Plymouth by Crawshay (1915) who found that adulthood was reached 35-40 days after hatching at 12.3"C. Although the food supply used by him cannot be assessed, it was probably inadequate for maximal develop- ment.

    Katona and Moodie (1969) succeeded in rearing large numbers of Pseudocalanus over perhaps four generations in large-volume con- tainers a t 15C. They obtained information on developmental durations only from eight smaller vessels of 250 ml volume, in which the progeny of individual females were reared. These gave estimates considerably longer and more spread out than those in Fig. 25B: 16-25 days for the time from hatching to C I and 30-38 days to adulthood. Numbers and sexes are unspecified. Although Katona and Moodie give no information on feeding procedures in the small vessels, they indicate that the rearing medium in the large-volume containers was renewed only every two weeks. Algal food (mostly Platymonas sp. and Isochrysis galbana) was added to these containers to keep cell concentrations at 100000/ml, but altogether the conditions of rearing do not seem to have been as optimal as those used by Corkett and McLaren (1969) and Thompson (1 976).

    Corkett (1970) reported on the successful rearing of three individuals from Halifax, N.S. beyond C I from among those reared to this stage by Corkett and McLaren (1969). Although the fastest individual developed at precisely the rate predicted from Fig. 25A (26 days to adulthood), the other two lagged considerably, so that mean time to maturity was 35 days. The food medium was added to but not changed every few days as by McLaren (1974). We assume that the retarded individuals were not developing at a physiologically maximal rate.

    The large number of experiments conducted on Pseudocalanus off the island of Sylt in the North Sea by Paffenhbfer and Harris (1976) were designed to test the effects of food concentration on growth rates (see p. 130). They used large-volume, rotating containers, and changed food frequently. Within the range of food concentrations used by them, there was little or no evidence of retardation. In eight experiments, the times between hatching and C I were 10.5-12.5 (mean 11.4) days, and between hatching and 50% adult were 24-32 (mean 25.3) days. If we assume that embryonic duration for animals off the island of Sylt is the same as for the North Sea animals studied by Thompson (see Fig. 22), then the times estimated by Paffenhbfer and Harris are precisely as predicted from Table XX : 10-7-11.8 days for hatching to


    C I and 24-8-26.0 days for hatching to adulthood (the range represent- ing both Nova Scotia and North Sea ''multipliers" respectively).

    Sazhina (1968) reared individuals of the Black Sea population of Pseudocalanus to maturity in the laboratory at 8-10C. Details of experimental procedures and numbers of animals involved are not given, and estimates are presented only to the nearest day. However, results conform quite well to those summarized in Fig. 25. Durations for nauplii in days were: N I (l), N I I (2), N I I I (3), N I V (349 , N V (3-4), N VI (2-3) for a total naupliar period of 14-18 days. The lower value is probably a better indication of potential rates. For copepodids, the times were: C I (2), C I1 (2), C I11 (3), C I V (5) and C V (5). Lengthening of duration in later stages (contrary to Table XX) indicates to us that these stages were not developing a t maximal rate. Nevertheless, the lower estimate of the range 3 P 3 9 days given by Sazhina as time from hatching to maturity agrees with mean estimates for other populations (Fig. 25).

    Sazhina (1974) gives duration of the naupliar stages (presumably equivalent to appearance of C I ) for animals from the Black Sea as 14-18 days at 8-10C (a summary from Sazhina, 1968) and 1 6 1 9 days at 11-13C ; the times at the higher temperatures suggest that develop- ment was retarded (see Fig. 25). For " Mediterranean " animals (no locality given, but presumably the Adriatic) she gives 12.3 days at 11-13"C, very close to times in Pig. 25. There are no details on numbers of copepod or conditions of rearing, except that green algae were used in the Black Sea experiments and mixed food in the " Mediterranean '' ones. However, we predict with some confidence that rates apply- ing elsewhere (Fig. 25) will also apply to Black Sea and Adriatic populations.

    Andreeva (1 976a) determined the relationship between temperature and the duration of C I from the Sea of Japan as about 12 days a t 3.5"C and 4 days a t 15C. These times are much longer than predicted on the assumption that stages take about the time required for embryonic duration (about 7 days at 3.5"C and 2.2 days at 15C in the North Sea ; Fig. 22). However the ratio of times a t 3.5"C and 15C is appropriate (3-0 in the Sea of Japan, 3.2 in the North Sea). Andreeva's (1976a) plot of individual durations shows considerable scatter (the range averaging about & 40% of the mean durations between 10" and 15OC). The animals may have been experiencing physiological or feeding problems that retarded their development rates. In an earlier note, Andreeva (1975) gives 2-3 days for embryonic duration, 12-13 days for the naupliar period, and 23-25 days for the copepodid period, but does not state the experimental temperature involved. The first two are reason-


    able for temperatures of ca. 10-12"C (see Fig. 22, 25)) but the last shows clear evidence of retardation (see Table XX).

    2. Effects of food supply We have indicated above that inadequate food may retard develop-

    ment in rearing experiments. Differences in quality of food have evi- dently not been looked into, but therc is much information on effects of amounts of food.

    Thompson (1976) found that nauplii reach N I11 but do not develop further if starved. From her estimates of stage duration at the eleven temperatures shown in Fig. 25B, it can be estimated that the relative times (i.e. as units of embryonic duration) taken to reach N I1 and N I11 were 0.22 and 0.53-almost precisely as for the fed N I1 and N I11 in Table XX. Her estimates of duration of starved N I11 are invalidated by the death of all of them in this stage. We conclude (with Thompson) that food is unnecessary to sustain maximal development rates during the first two nauplius stages and that N I11 may be the first feeding stage.

    Corkett and McLaren (1970) found no retardation in individuals reared a t 1 16C in concentrations of Isochrysis galbana replenished weekly at 1.5 x lo5, 3 x lo5, or 6 x lo5 cells/ml. Mean time from hatching to C I was 10.6 days and range of individual times was 9.6- 12.5 days. However, a t 3 x lo4 cells/ml, the results were complex. In two dishes with three nauplii each, three individuals reached C I in 11.5, 12.6 and 14.5 days. The rest remained in nauplius stages for 25 days, and then were fed abundant food (6 x lo5 cells/ml) and reached C I after about nine days. Nine days is close to the number of days that would be predicted to be taken if these retarded nauplii were stopped a t N I I I (9.6 days between beginning of N I I I and C I at ll*5OC, from Fig. 25B). These results suggest that 3 x lo4 cells/ml of Isochrysis galbana replenished weekly is a critical, threshold level for sustaining development rate. It has been shown (p. 90) that this is also a critical level for maximal production of eggs and will be shown (p. 129) that this is the level at which fat is laid down. This level of I . galbana, a t the time of replenishment, is about 500 pgC/I. calculated from Table VI I and may be effectively about half this level in view of probable filtering inefficiencies of such small cells (see p. 63).

    Paffenhofer and Harris (1976) examined effects of food supply extensively and rigorously. As noted above (p. 110) there was little evidence of developmental retardation at any food concentrations used by them. At (nominal) food concentrations of 5 6 2 0 0 pgC/l., the ranges of times for individual experiments were 10.5-11.5 days to reach C I


    and 24-26 days to reach adulthood. At a nominal food concentration of 25 pgC/l. (actually about 30 pgC/l.) C I was reached on average in 10.5 days. However, at the same nominal food concentration (actually about 21-27 pgC/l.) subsequent development was retarded slightly, and time to 50% adult was 29 days. It appears that this level of food is about a t the threshold for sustained development. Since the experi- ments of Paffenhofer and Harris involved the diatom Tholassiosira rotula in rotating culture vessels, the lower estimate of this critical level compared with the results using the smaller I . galbana (above) is probably more nearly natural.

    Paffenhofer and Harris (1976) work is of great importance in demonstrating that development times are little affected by food concentrations comparable with those occurring in nature. They report that algal concentrations near the island of Sylt ranged from 68-780 pgC/l. (annual mean 192), and refer to comparable values for total particulate C for the northern North Sea. They conclude: ( This suggests that all developmental stages of the neritic P. elongatus are able to adapt t o a range of food concentrations, neither mortality nor generation time being markedly affected by low food concentra- tions . 3. Genetic variation of development rates

    Differences in development rate between populations of Pseudo- calanus may have a genetic component. McLaren (1965) concluded from field samples that the small form from Ogac Lake developed at about 0.42 stages per day compared with 0.28 stages per day for the large form. This ratio of development rates (1.5 : 1) is about the sarne as the ratio of embryonic durations (1.6 :1, p. 103) determined in the laboratory for the large and small populations of Pseudocalanus from Ogac Lake.

    These differences in development rates are clearly genetical. I n eggs a t the 32-cell stage the DNA content was about seven times greater in the large form than found in the small form (McLaren et al., 1966). Woods (1969) speculates that this larger amount of DNA is itself responsible for the slower development rate and that this slower development rate serves to restore a life cycle more suitable for the environments of Ogac Lake (p. 139), and we have in fact referred earlier to the large form of Pseudocalanus as a possible (instant species (p. 10).

    Hart and McLaren (1 978) found that embryonic duration was signi- ficantly related to size of males chosen for extreme sizes from a sample taken near Halifax, Nova Scotia. Since the male could only contribute


    genetically, Hart and McLaren conclude that development rate, like size (see p. 124) was heritable among these animals.

    D. Longevity of adults

    We have already indicated (p. 93) that female Pseudocalanus may potentially produce of the order of ten successive clutches of eggs over a period of time determined by temperature, and that they might live for an equal post-reproductive period. However, in nature it is unlikely that maximal potential longevity is often attained, and post-reproduc- tive life is inconsequential for demography and production since neither growth nor egg production takes place. The brief review here may, however, be of some intrinsic interest.

    The maximum realized length of life in nature is over two years in the high arctic, where adult females may live for some months at least (p. 137). Adult males, as already noted (p. S O ) , are scarce in nature because of their shorter lives. In Crawshay's (1915) pioneer work, one adult female survived for 121 days in the laboratory at 12.3"C.

    The laboratory work of Urry (1965) and Corkett and Urry (1968) on effects of quantity and quality of food on mean survival of adult females has already been discussed (p. 177). However, as their experi- mental animals were captured in nature, the maximum, rather than the mean might be a better reflection of their potential longevity. Accord- ingly, we have estimated from Urry (1964) the age of the longest lived individual in each of 21 experiments at 10 5 1 C in which food was considered to be adequate for sustained existence (i.e. Isochrysis at 30 000 cells/ml or more replenished weekly, and food species that gave comparable survivorship, Table XII). The mean of these 21 estimates is 107 days (range 84-144). Because different numbers of copepods were used to initiate these experiments, confidence intervals cannot properly be estimated. The eight wild-caught females considered by Corkett and McLaren (1969) to have fulfilled their reproductive potential of 8 or more clutches (see p. 93) lived on average 92 days (range 75-103) at 6-7". The seven females reared and mated in the laboratory by Thompson (1976) lived on average 79 days (range 31-140) after mating, which occurred soon after maturity (Table XVI). The most that can be said from these scattered results is that adult female Pseudo- calanus are capable of living for more than 100 days at quite elevated temperatures.

    Males, by contrast, were found by Urry (1964) to live for only 15 days on average, compared with 33 days for females when both were given 30 000 cells/ml Isochry& galbana. Mean survival for starved


    females in several experiments ranged from 17 to 19 days indicating that males evidently gained no sustenance from I . galbana.

    Probably because of small numbers, there was no evident effect of temperature on longevity of the seven females reared by Thompson (Table XVI). However, a trend is evident (Table XXI) for starved adult females as reported by Corkett and Urry (1968). The very short survivals a t 19.5-21C are surely pathological, but those at lower temperatures may reflect normal physiological processes that may also apply to the determination of potential length of life of feeding adult females.

    TABLE XXI. LONGEVITY OF STARVED FEMALE Pseudocalanus IN TEE LABORATORY. (After Corkett and Urry, 1968.)

    Mean longevity (days)

    No. of copepods Temperature C

    91 5-7 71 11 10-17.5 35 13 11-19.5 24 7 19-5-21 4

    Recently, Dagg (1977) compared survival over a short period of ten starved and ten continuously fed (superabundant Gonyaulax tamarensis) female Pseudocalanus and found no difference (six alive after sixteen days). However, these numbers seem rather small on which to base his conclusion that Pseudocalanus can withstand rather low periods of total starvation, suggesting that they are capable of metabolically removing themselves from changes in the food environment.

    E . Body size Pseudocalanus shows a great deal of variation in body size. Cephalo-

    thorax lengths of individual adult females have been recorded as small as 0.67 mm (Carter, 1965) and as large as 1.8-1.9 mm (Lacroix and Pilteau, 1971, their Fig. 4). We believe that explanations for this variability are now largely complete. Therefore we attempt to review only a fraction of the large literature that refers to seasonal and local variations in size of Pseudocalanus with its many speculations. Rather, we will attempt to demonstrate the propositions that size is affected by temperature, but not directly by food supply, and that there is marked genetic variation in size, both within and between populations. The systematic significance of this variability has already been referred to (p. 11).


    1. Effects of temperature on size (a) Inferences f rom nature

    The earlier literature on size variations of Pseudocalanus in nature is admirably reviewed and analysed by Deevey (1960b). She found high negative correlations ( r < -0.6) between length of adult females and temperature in waters with annual temperature ranges of 14C or more. Conversely, correlations with temperature were smaller, but high positive correlations ( r > 0.5) were found with various measures of phytoplankton during the month prior to sampling where waters had an annual temperature range of 13C or less. Where possible, she came to these conclusions using partial correlations.

    Deevey (1960b) concluded that these correlations imply causality : that the relative effects of temperature and food on seasonal variations in length depends on the extent of the annual temperature range and the quantity of phytoplankton present. McLaren (1963) argued that the association between size and food supply was indirect, operating through the effect of food shortage in retarding development (p. 112). I n all localities from which data were available, Deevey (1960b) found that food supply was negatively correlated with temperature-partly a consequence of spring maxima in phytoplankton. This means that size might be most closely correlated with immediate temperatures when they are low since food would allow rapid development then, and this form of dependence cannot be eliminated by partial correlation.

    I n order to stress the sufficiency of temperature as an explanation of seasonal differences in size, we will first discuss some examples from nature in which Deevey (1960b) and others have implicated food as well.

    Loch Striven, Scotland (Marshall, 1949; Marshall et ab., 1934) has a fairly narrow annual temperature range (6O-l3"C, means for water column, see Fig. 29). I n 1933 the major diatom bloom occurred in late March to early April, with smaller bloom in May, July and late summer. Few diatoms were found in winter. Adult female Pseudocalanus showed small size in winter, an abrupt increase to maximal size in April, and then a gradual decrease during summer (see p. 143, Fig. 29). Size and temperature are strongly and negatively correlated between April and autumn, but the persistence of small animals during the cold, diatom-poor winter reduces the correlation with temperature, and introduces the strong partial correlation between size and food during the previous month, as calculated by Deevey (1960b). However, the original papers make it clear that these small overwintering adults had been developing from about mid-July of the previous year, whereas the large adults in April were born beginning in February (see also


    p. 143). McLaren (1963) used such information from Marshall (1949) and Marshall et al. (1934) to plot mean size of adult females on each collection date against estimated mean temperatures during their lifetimes. The results (Fig. 26) indicate that temperature is a sufficient explanation for size variations.

    Similar arguments, taking into account small overwintering copepo- dids and adults from the previous warm autumn, can be used to explain the reduced correlation between size and temperature at time of sampling in other mid-latitude areas with narrow temperature ranges considered by Deevey (1960b); for example, the North Sea (see p. 147), the English Channel (see p. 146) and Norway (see p. 151).

    In high latitudes, the protracted life histories of Pseudocalanus may even lead to spurious positive correlations between size and temperature at time of sampling. Thus Ussing (1938) found in East Greenland that reproduction during the phytoplankton maximum in June gave large young copepodids in July which developed (probably in deeper water) to large, overwintering C V by September (see p. 141). Reproduction in summer, when food is scarcer and temperature slightly higher, gave smaller copepodids that did not moult into CV until the following spring. There was little size variation in the subsequent adults. Clearly temperature at the time of capture would be a poor indicator of size under these conditions, with large C V occurring during the warm summer and smaller ones in the cold spring. But it cannot be concluded, as Ussing (1938) and Deevey (1960b) did, that food is directly respon- sible for the observed size differences.

    Similar interpretations can be applied to size variations described in other northern localities (see also p. 141) by Digby (1954), Fontaine (1 955), Grainger (1 959) and Cairns (1 967). However, in some of these localities there is bimodalism of size that might also reflect genetically different size forms (see p. 123).

    Studies of two landlocked populations in northern Canada are free from effects of larger or smaller individuals being recruited from outside the study areas. Carter (1965) found that size of adult females varied little in Tessiarsuk, Labrador. From depth distributions and tempera- ture profiles it seems that this population was subjected to a narrow range of temperatures during the season. A group of small, rapidly disappearing females a t the beginning of the summer may have largely or completely matured in the warmer waters of the previous autumn (see p. 140). McLaren (1969) described seasonal variations in sizes of all copepodids and adults in the three basins of Ogac Lake, Baffin Island. By detailed analysis of phytoplankton, temperatures and depth distributions of the copepods, he concluded that size variation


    could be attributed to temperature during development. A paradoxical recovery of size of young copepodids during later summer when food was scarce and temperatures rising he suggested might be due to relatively more rapid development of smaller individuals or to their disproportionately high mortality. McLaren's (1969) study stresses the complexity of interpretation that is required to explain size varia- tions in high latitudes, even in a relatively " controlled " situation.

    All in all, size varies rather narrowly within most of these high- latitude areas, and variations between localities with different thermal

    Temperature ("CI

    FIG. 26. Relationships between female size and environmental temperatures in various localities. Points for Canadian arctic are (see text): 1, Tanquary Fiord; 2, Foxe Basin; 3, Ungava Bay; 4, Tessiarsuk; 6, Ogac Lake. (After McLaren, 1966, with additions for the Canadian arctic from Cairns, 1967, and Carter, 1966.)

    regimes can be more revealing (Fig. 26). The points for Foxe Basin (2 in Fig. 26), Ungava Bay (3) and Ogac Lake (5) have been used and explained previously (McLaren, 1965). That for Tessiarsuk (4) is from Carter (1965), and represents the mean size of females on 10 and 20 September (estimated from his Fig. 5), since these developed during summer (his Fig. 4) at depths around and below 10 m (his Fig. 7) where temperatures can be estimated (his Fig. 3). The point (1) for Tanquary Fiord represents mean size in 1963 and 1964 combined from Cairns (1967, his Fig. 5) and assumes that small seasonal temperature variations near the surface are unimportant relative to the almost uniform temperatures of - 1 "C throughout the season between 20 and 100 m (his Fig. 1). Given these approximations and assumptions, Fig.


    26 indicates that there may be uniform temperature response of populations of Pseudocalanus throughout the Canadian north.

    As noted above, Deevey (1960b) concluded that temperature is all-important when its seasonal range is wide. McLaren (1963, 1965) chose to depict her size-temperature relationship for Long Island Sound (Fig. 26). Here the copepod populations might be relatively enclosed . A ten-fold variation in chlorophyll had no statistically significant effect on size, and the water is almost unstratified during the growing season, so that mean temperatures are more reliable.

    Unfortunately, there appears only limited information on seasonal size variations of the otherwise extensively studied populations of Pseudocalanus in the Black Sea. Kovalev (1967) lists mean total (?) lengths for animals from several depths for the months of February (1.17-1.19 mm), August (1.09-1.12 mm) and September (1.08-1.09 mm), which suggest that seasonal size variations in this population may be rather narrow. A later note (Kovalev, 1968) indicates a range of 1-00-1.23 mm in the Black Sea and 0-8P1.04 in the Adriatic.

    The relationships in Fig. 26 together seem to be overwhelming evidence from nature that temperature is the primary environmental determinant of body size of Pseudocalanus. They also reveal clear regional variations in response. McLaren ( 1965) fitted BBlehrAdeks temperature functions to the data (with fewer points for northern Canada) in Fig. 26. This is not necessary to describe the obvious adaptation of each temperature-response curve to the regional thermal r6gime. Adaptation is hardly surprising ; otherwise monstrously large copepods might occur in cold northern waters, and exceedingly small ones in warmer regions. It is also interesting that the same range in mean body size seems to be maintained in all three geographical regions in Fig. 26.

    (b) Evidence from the laboratory Only recently has the effect of temperature on body size been

    confumed in experiments. A hint of the effect is first found in the work of Katona and Moodie (1969), who collected females off Plymouth when the surface temperature was 86OC. These produced laboratory cultures that went through about four generations in the laboratory at 15OC. Means of cephalothorax lengths are given as 1.01 f 0-05 mm in the females from nature and ranged from 0.84 f 0-02 to 0.89 f 0.004 in successive samples from the laboratory stock (the & values are said to be S.D., but are very small and are presumably S.E.). Without data for other temperatures the reduced size of females in the laboratory cannot be assigned with certainty to temperature.


    A series of experiments were carried out with C I11 captured near Halifax, Nova Scotia, and reared to maturity at constant temperatures of about 5, 8 and 12C and varying temperatures of 8-12", with a mean of 10C (Lock and McLaren, 1970). The results showed the expected inverse relationship between female size and temperature, and no significant response of male size. The founding populations of C I I I differed in mean size, so that the effect of temperature is best expressed as percentage increments of size between stage I11 and adult (Table XXII). Although the size difference of the females at the temperature extremes proved to be highly significant, confidence intervals cannot be set for the percentage increments, as the animals were not reared individually.

    McLaren (1974) added to these results by rearing animals to C I11 in the laboratory. Somewhat surprisingly, he found no effect of temperature. Mean cephalothorax lengths (k 95% c.1.) were 0.60 f 0.04 mm at 4.2"C, 0.60 f 0.02 mm at 7-3"C and 0.59 -& 0.02 mm at 11*7"C.


    (After Lock and McLaren, 1970.)

    Mean size C 111 mm

    yo size increment to ad. $2

    5C 8C 10C" 12C

    0.55 0.63

    60 52 45 43 59 51 49 45

    a 12 h at 8" and 12 h at 12" each 24 hour.

    Thompson (1976) carried out extensive experiments to determine the effects of temperature on size. She presents her data as tables with mean lengths, S.D. and numbers, and graphs the means without regressions. We have chosen to present her results by fitting regressions to her means (weighted by n) for each temperature (Fig. 27, insert). This allows us to express the relative effect of temperature as the percent- age decrement in length (mean calculated for all temperatures) for each degree Celsius. This in turn allows comparisons between the effects of temperature on each stage (Fig. 27).

    A striking pattern emerges from Thompson's results. If two groups of copepods were reared a t 10" and 11C respectively, the latter should average about 1% longer at NV. However, if they are reared further to


    C I, they might differ little in length. This suggests that during the interval between NV and C I, temperature may have a positive effect on size. After C 111, the effect is clearly negative again. However, the confidence intervals for C V and adult animals are very wide.

    0.5- 4 6 8 10 12 14


    I I

    I I I

    I I I I I f

    I ( I I

    I 0

    I I I I

    I I

    , I I I I

    I I I I I I I I

    I I I I I I


    1; I I I

    I I I I I I

    N I N I I N I I I N I P N Y N P I CI C I I CIIl C E C Y Ad.

    This is

    Fra. 27. Effect of temperature on body size of North Sea Psewlocalanus reared in the laboratory (data from Thompson, 1976). The unbroken lines are based on linear regressions of lengths on all experimental temperatures. The broken lines are based only on linear regressions of lengths on temperatures above 7.3"C, as shown in the insert for C 111-adult (cephalothorax lengths, sexes combined). Overlap of the 95% c.1. with a length decrement of 0% indicates non-significance of the temperature effect.

    not a consequence of small numbers of older stages ; the same numbers of individuals of each copepodid stage were measured at each tempera- ture. Rather, it is due to the erratic effects of low temperatures on size of these older stages, as clearly shown on the insert of Fig. 27.


    The older stages at the three lowest temperatures in Thompson's experiments also seemed to develop more slowly than expected (Fig. 25B), and we have suggested (p. 108) that temperatures below 8C might have caused abnormalities in the laboratory. Therefore we have fitted regressions to the means for higher temperatures, as indicated on the insert of Fig. 27. The regression coefficients, expressed as percentage length decrements per "C, show a more persistent and significant pattern of increase among older stages when only temperatures above 8" are used.

    Thompson's results, as expressed in Fig. 27, are compatible with those of McLaren (1974) in showing the small effect of temperature on size of C I11 as compared with adults (see above). However, they do not confirm the conclusions by Lock and McLaren (1970) that adult males were little affected by temperature. From tabulated results in Thompson (1976), the percentage decrement in length per "C is calcu- lated as 3.43 & 1.86% for adult females and 2.92 f 1.54% for males (the 95% confidence limits are calculated for regressions on tempera- tures above 8"C, as for Fig. 27). There is some resemblance between the regression for adults from the southern North Sea and that for females from Lock Striven (cf. Fig. 26, Fig. 27 insert).

    2. Effects of food on size We have already suggested (p. 116) that the association between

    body size and food supply in nature is indirect : that food shortages may retard development and therefore diminish the correlation between size and current temperatures, but that body size is not ultimately affected by this shortage. Certainly the association between temperature and size in the field leaves little room for a further effect of food. McLaren (1963) showed from data in Deevey (1960b) that a ten-fold variation in chlorophyll (as an index of food) did not correlate with the deviations from the size-temperature curve for Pseudocalanus in Long Island Sound.

    Food was kept a t very high levels in the experiments of Lock and McLaren (1970), McLaren (1974) and Thompson (1976), ao that any effect of food supply was not evident. We have suggested (p. 110) that animals from Plymouth reared by Katona and Moodie, which were retarded in reaching maturity, may have been short of food. However, their size (female cephalothorax lengths 0.84-0.89 mm) was similar to that predicted for females from the southern North Sea (0.83 mm, from regression for females a t temperature > 8C.)

    The extensive experiments of Paffenhofer and Harris (1976) give excellent evidence on the effects of food on size. They give sizes only


    as ash-free dry weights, which are not directly comparable with the cephalothorax lengths considered above. It is clear that wide variations in food supply have little influence on ash-free dry weight, except for males a t the lowest concentration of food (Table XXIII). The great importance of these results (as for their results on development times described on p. 113) is the demonstration that food has such a small effect on body size at food concentrations a t the lower range of possible food supplies in nature.

    TABLE XXIII. WEIGHTS OF Pseudocalanus ADULTS REARED FROM NORTH SEA POPULATIONS. (After Paffenhofer and Harris, 1976.)

    Nominal food concentration (pg (711)

    25 50 100 200

    No. experiments 1 2 4 1 Mean pg ash-free

    Mean 68 pg ash-free dry wt 16.0 18.3 (14*0-22.5)a 22.1 (19.0-23.7) 17.5

    dry wt 3.1 9.5 (7.0-12.0) 11.3 (8.4-13.9) 13.2

    a Ranges in parentheses.

    3. Genetic variation in body size Differences in the size-temperature relationship between popula-

    tions of Pseudocalanus (e.g. Fig. 26) are more marked than the differences in developmenctemperature relationships (e.g. Fig. 25). The differences in size (p. 9) between the large and small forms of Ogac Lake and Winton Bay are also genetic, and McLaren (1965) suggested that the differences might be due to cell size, rather than cell number. Woods (1969) enlarged on this possibility and argued from the literature that " an increase in the amount of DNA should result in an increase in the cell volume but a decrease in the metabolic and division rates".

    However, Pseudocalanus also shows a great deal of continuous size variation within samples from any given locality (see Figs 29-33). Some of this variation is doubtless due to the occurrence of animals that have been exposed to different temperatures during maturation. Recent evidence (McLaren, 1976b) indicates that size is also markedly heritable. McLaren reared at 10C femaIe offspring of families from 9 males each mated to 2-4 females. This enabled him to estimate by analysis of variance the contributions of males and females to the cephalothorax length of adult female offspring (see Falconer, 1960). McLaren found the heritability (h2) of cephalothorax length of adult


    females at 10C was 0.93 (significantly different from 0,P N O e O l ) , based on male parents. This is extraordinarily high, and indicates that size (which we have already shown to be little influenced by food supply) under uniform conditions a t 10C is almost entirely genetically deter- mined. Most interestingly, the female contribution to size of her off- spring (which is normally greater than that of the male in most such experiments, because of non-genetic maternal effects) was very small and not significantly different from zero. McLaren (1976b) suggests that this result is related to size-assortative mating.

    A further development of our understanding of the continuous variation in size of Pseudocalanus near Halifax, Nova Scotia, comes from the recent demonstration (McLaren, 1976b) that size of females in the smaller range (ca. 0.8-1.05 mm in Fig. 23) is strongly correlated with cellular DNA contents. This suggests that the continuous variation iii body size is a result of continuous variations in cell size, caused by the continuous variation in nucleus size.

    F. Body composition and weights

    The composition of the marine plankton has been extensively studied, sometimes with little obvious application to problems of growth, development and production. Much of the literature on copepods is reviewed by Ikeda (1 974), but there is little information on Pseudo- calanus. Here we will review what is known, and will focus ontjhat which is useful in describing the size and growth of the animals. This approach leads into a consideration of oil storage in the next section.

    1. Wet and dry weights Wet weights are probably unsatisfactory as a measure of size of

    Pseudocalanus. Marshall and Orr (1966) give a range of estimates of from 50% to 80.7% water (mean 72.3%) for 15 lots of C IV, C V, and adult female animals. Nakai (1955) lists a value of 87.7% water for a very large lot of unstaged animals. Ikeda ( 1 970) gives a mean wet weight of 40 pg and a mean dry weight of 12 pg (i.e. 70% water) for one lot of 80 adult females and 8 adult males.

    Harris and Paffenhofer (1 976) used ash-free dry weights as a measure of size in their experiments with Pseudocalanus and state that the average animal was 12.8y0 ash. Ilceda (1970) found that the ash-free weight of the above-mentioned lot of Pseudocalanus was 9.66 pg/animetl (i.e. ash was 20y0 of total dry weight). Nakai (1955) found that ash was only 2.3% of dry weight of his samples, and Laurence (1976) obtained a value (mean S.D.) of 8.50 f. 0.11%.


    2. Calori$c content Martens (1975; see also Kraneis and Martens, 1975) has measured

    calorific content of Pseudocalunus. He expresses his results in a regres- sion on carbon (dry wt in pg) as: cal = 0.023 + 0.0067 x carbon. Assuming that the relationship is actually a proportional one, 1 pg C = 0.011 cal. This agrees well with an estimate of 4.6 cal/mg dry wt (at 50% carbon, giving 1 pg C = 0.009 cal) in Greze (1970) and with a mean (& S.D.) of 5-07 5 0.18 cal/mg dry wt (5-54 & 0.20 cal/mg ash- free dry wt) in Laurence (1976).

    3. Lipid and protein Substantial work has been done on the lipid and protein fractions of

    copepods, but only the work of Nakai (1955) seems to have dealt with Pseudocalanus. For a large number of animals he calculated that fat was 17.3% of dry weight and protein 71.5%.

    This estimate of fat content cannot be taken as average for pur- poses of calculation. The variability of lipid (in the " oil sac ") is implicit in some of the following sections. Nothing seems to be known of the qualitative aspects of lipids in Pseudocalanus although other copepods have been extensively studied.

    The composition of body proteins of Pseudocalunus has evidently not been studied. However, Jeffries and Alzara (1970) have assayed free amino acids in this and other copepods, largely in the context of environmental salinities. They detected all the standard amino acids except cystine and ornithine. Glycine was about one-third and proline about one-fifth of the total, and taurine, alanine and arginine were also well represented. The total free amino acid (about 550 pmoles/g dry weight) was about as expected for marine fornis, but the predominance of the two above-mentioned amino acids gives Pseudocalanus the highest index of " biochemical dominance " and the lowest index of " biochemical diversity " of the six species studied by Jeffries and Alzara. They believe that this is related to its euryhalinity and general adaptability (p. 25) .

    4. Carbon, nitrogen, phosphorus, hydrogen and silicon Some elements have been used as measures of size, biomass and

    " condition " in studies of growth, production and excretion of copepods.

    Carbon was estimated by a wet-ashing method to be 49% by regression on individuals of dry weight between 3 and 30 pg by McLaren (1969). These were formalin-preserved animals and had lost


    much of their lipid. Two lots of unpreserved animals from Ogac Lake (where little lipid is found in the copepods) deviated little from the overall regression. Ikeda (1974) gives estimates of 45-1-46.5% C for four samples of individuals (stages not given) taken in May and June 1971, off Japan and weighing 10.7-16.4 pg in dry weight. Another four samples of C V taken in September 1970, weighed 25.5-27-9 pg/ individual and were 63.3-66-7 % C. Ikedas samples were fresh-frozen and analysed by gas chromatography. The very high C values in the September sample were presumably attributable to high lipid content in large oil sacs. Indeed Ikeda illustrates an individual stage V copepodid from the September sample showing a very large oil sac. Martens (1975) gives a regression of carbon (C) on dry weight (W) as: C = 2.27 + 0-187 x W (expressed in the same weight units). However, such a regression might more properly be fitted through the origin. His mean estimate is 36% carbon, with wide variations.

    To convert Pseudocalanus dry weights to carbon, Paffenhofer and Harris (1976) use conversion factors of 30% for N I-C I, 34% for C I-C 111, and 37% for C 111-adult. However, they later (Harris and Paffenhtifer, 1976) make it clear that these estimates are based on the much larger Calanus helgolandicus from California.

    We suggest that dry weights of Pseudocalanus when they are not very lipid-rich are about 50% carbon. In calculations of growth and production, it may be better to consider the highly mobile lipid carbon separately.

    Ikeda (1974) determined that nitrogen was 11.4-12-4% of dry body weight of Pseudocnlanus in MayJune and only 6.4-7.2% in September. The low C :N ratio in September is presumably due to high fat content (see above). Christiansen (1968) reported higher N contents for NV-VI (dry wt 0.60 pg, 15% N), CI-I11 (2.73 pg, 27% N), C V (9.75 pg, 28% N) and adults (14-42 pg, 20% N). These animals, unlike those analysed by Ikeda, had been feeding in the laboratory. We have shown (p. 45) that feeding animals produce substantially more NH,, and the high N values in Christiansens animals may in part represent gut contents. Martens (1975) gives a regression of nitrogen (N) on dry weight (W) as : N = 0.477 + 0.027 x W (expressed in the same weight units). The average N content was 6.5% of dry weight. Butler et al. (1969) reported that N was 7.8% of dry body weight in mixed small copepods , which were in fact almost all C IV and C V Pseudocalanus. We suggest that a figure of 7% N for average unfed Pseudocalanus might be used.

    Hargrave (1966) lists phosphorus contents for starved animals as 0.58 pg for copepodids and 0.01 for nauplii; this seems high. Butler


    et aZ. (1969) give the only estimate known to us of P as a per cent of body weight of Pseudocalanus (see above qualification) : 0-61 % of dry body weight.

    Hydrogen content wa8 estimated by Ikeda (1974), who found that, as might be expected, it varied with carbon. He found C:H ratios of 6.5-6-9:l in samples from MayJune and 6-6-6.9:l in September, evidently unaffected by amount of fat present.

    Nakai (1955) lists SiO, as constituting 0.04% of dry weight of Pseudocalanus. Although they have been studied in the marine plankton, we can find no information on other elements in Pseudo- calanus.

    5. Weight-length relationships A number of authors have listed weights or other measures of body

    size for various purposes. We believe that cephalothorax length is often the most useful measure of size, not only because it is easier to determine, but because it is not subject to variations due to food contents, oil storage and preservation effects. Given this variability, it may be better for some purposes to calculate weights from a general weight-length regression.

    Krylov (1968) determined the weight-length relationship of a variety of formalin-preserved copepods (unfortunately total length in mm and wet weight in mg). He found that K in the expression, wt = K (length)3 was roughly the same for all copepodid stages of a species. He gives two estimates of this constant for Pseudocalanus : 364 for White Sea animals, and 336 for Black Sea animals.

    Robertson (1968) gives dry weight to length relationship for seven samples of " Para-Pseudocalanus " in which the calculated exponent (2-13) is substantially less than the above. The size range of his samples (means 0.70-0.91 mm) was probably too small for an accurate deter- mination.

    McLaren (1969) showed that the exponent in the weight-length relationship was greater than 3.0 (from his original data, 95% c.1. 3.40-3-88) for a much greater size range of formalin-preserved speci- mens (C 111, C IV, CV, adult 3 and adult $2) from the Canadian arctic :

    dry wt in pg = 11.9 (cephalothorax length in mm).3*64

    The greater-than-cubic exponent is also implicit in observations that large Pseudocalanus are relatively wider (McLaren, 1965).

    We suggest that the above formula is much the most reliable available. It applies to " lean " animals, and may be a good indicator of weight for various metabolic contexts. However, there is no doubt


    that unpreserved animals may be heavier than predicted by this regression. The mean weights of four lots of preserved animals from Plymouth (Conover, 1959) averaged only 7% higher than predicted by the above equation from their lengths. Weights of 13 unpreserved samples from Loch Striven (Marshall and Orr, 1966) average fully 67% larger than predicted. We suggest that the difference is due to fat contents.

    6. Weight of eggs Adults do not grow (although females may increase their store of

    oil ; see next section), but females do produce eggs. Two lots of preserved eggs from southwest Baffin Island gave almost identical dry weights of 0.30 and 0.31 pg per egg (McLaren, 1969). Clutches from this locality averaged about 70 eggs with a total volume of about 0.65 mm3 (Fig. 19B). This allows us to write a general relationship for all localities from Fig. 19B :

    Dry weight of clutch in pg = 6.35 (cephslothorax length in mm).4*1s

    G. Oil storage

    The oil sac in Psezcdocalanus in nature can vary greatly in size from non-existence to a condition where it almost fills the body (see illustra- tion in Ikeda, 1974). Some laboratory studies have been made on possible sources of variation.

    Lock (1968) carried out rearing experiments on C I11 animals captured in nature, in an effort to determine the effects of temperature on size (see p. 120). He also measured the oil sacs in animals maturing in one experiment. He approximated the size of oil sacs by making models of them on a scale of 100 : 1 with modelling clay, and determining volumes by displacement. More oil was stored at low temperatures (Table XXIV), a t which temperatures females, but not males, were also larger in body size (p. 120). Because of great variability among indi- viduals, this effect is only significant (p < 0.05) among males. The size of oil sacs is significantly smaller (p < 0.01 at 5 and 10C) in egg- bearing females, suggesting that other (unfertilized) females had not used their oil store in oogenesis. The size of oil sacs in males and females a t alternating temperatures of 8-12C (mean 10C) was larger than for animals raised at 8" and 12", but because of great variability, the effect fell short of significant. Even so, there is a hint in these results that some sort of energy bonus may accrue from alternating temperatures.



    Mean size of oil sac in p3 >: l o 0 f 95% c.1. (no. measured) Temperature

    Females Females with eggs

    Males "C without eggs

    5 7 .3 & 1.69 (18) 9.2 f 3.08 (7) 4.6 f 3.90 (8) 8 4.3 f 1.75 (10) - 1-7 f 1-06 (16)

    1 On 4.8 1.42 (25) 11.6 f 2.41 (7) 3.6 f 2.59 (13) 12 1.6 & 0.91 (16) - 2.0 f 1.33 (12)

    a 8" for 12 h, 1 2 O for 12 h each 24 hour during rearing.

    Corkett and McLaren (1969) found that oil sacs of adult females in the laboratory were more-or-less constant in size a t given food levels during the period of egg production. Generally the oil sacs became smaller and sometimes even disappeared altogether before death. Experiments with a small number of females suggested that oil sacs did not increase much in size when food concentrations (Isochrgsis galbana replenished weekly) were increased beyond 1 x lo5 cells/mI, but that they were very small or absent at food concentrations of 3 x lo4 cells/ml or less. As we have shown elsewhere, at these low food concentrations eggs are not produced at the maximal rate (p. go), and development rates may be retarded (p. 112).

    Paffenh6fer and Harris (1976) noted well-developed oil sacs in all copepodids and adult stages at food concentrations of 50, 100 and 200 pgC/l., and by inference not in those reared at 25 pgC/l. At 25 pgC/l. time to adulthood was slightly longer (p. 113) and adult males weighed less (p. 123), perhaps due to reduced oil content.

    Observations of occurrence and sizes of oil sacs in Pseudocalanus in nature may thus be of great importance, for we believe that the presence of an oil sac in copepodids (except when they are overwintering and perhaps " resting '' in some sense) indicates that development is proceeding a t a temperature-determined rate. This has to be verified.

    Similarly, we believe that oil sacs in adult females may mean that they are producing eggs at maximal, temperature-dependent rates (cf. p. 98).

    H. Growth rates

    Growth rates are implicit in the previously described observations on development rate, body size, and length-weight relationships. For example, for animals from Halifax the length of C I11 animals and

    A.Y.B.-16 7


    the length increment to adult females has been given on p. 120 and in Table XXII. We assume that each copepodid stage takes the same amount of time as does embryonic development a t each given tempera- ture (p. 109, Fig. 22). From these times and the estimated weights (equation, p. 127) of the C I11 and adult animals, the instantaneous coefficient of increase (k) of dry weight on a daily basis (t is time in days between stages) can be calculated from the weight of the earlier stage (W,) and weight of the later stage (W,) from : W, = Woekt. Then, 100(ek-1) gives growth rates as percentages. of body weight per day which is convenient for comparison with the practice (which we have followed) of giving rations, respiration losses, etc., in this form. For Pseudocalanus C I I I to adult female from Halifax, these are then approximately 7, 10, 12, 14, 15 and 17% of body weight per day at 0", 3", 6", So, 10" and 12.5". The same procedure can be used for Pseudocalanus (sexes combined) from the southern North Sea, using data from Thompson (1976). The regressions for length (L) on tempera- ture (T) between 8 and 14C are from Fig. 27 (insert): L = 0.427- 0-00264(T-11-74) for C I ; L = 0-577-0*00336(T-ll.74) for C 111; L = 0.900-0-3452 (T-11-74) for adults. Using the same procedure as for the Halifax animals, growth rates for C I to C I11 are estimated at 16, 19, 25 and 32% ,at So, lo", 12.5" and 15OC respectively. For the period between C I11 and adulthood (both sexes combined), the esti- mates are 16, 18, 18 and 17% respectively at the same temperatures.

    It can be seen that growth rates increase with temperature among older copepodids in the Halifax population, but not in the North Sea animals. This is because the negative effect of temperature on size is especially marked in the North Sea animals. Clearly, different popula- tions will exhibit quite different responses of growth rate to temperature, depending largely on the size-temperature relationship.

    Paffenhafer and Harris (1 976) estimated instantaneous growth rates a t 12.5OC directly as increase in ash-free dry weights of copepods. They indicate that little fat is included in these estimates. We have already discussed their observations that food had no effect on develop- ment rate, except at the lowest concentrations used by them (p. 113), and that low food levels had little effect on weight of adult females, but more on adult males (p. 123). Table XXV summarizes their findings on effects of food on growth rates, converted from instantaneous rates to percentages of body weight per day. The manner in which they evaluated naupliar weights is not evident, as young nauplii may not feed (p. 112) and may lose weight during early stages. The low growth rates between C I and adult a t a food level of 25 pgC/l. are probably related to the smaller size of adult males and slightly retarded develop-


    ment rates a t this level (Paffenhofer and Harris, 1976). The high values for C I-C I11 and low values for C III-adult at food levels around 50 pgC/l. are interpreted by Harris and Paffenhsfer (1 976) to mean that older copepodids are less able to secure rations a t this low food level. However, it is possible (since the rates for C I-C I11 are unusually high) that experimental error is involved. At any rate, the extreme rates at 50 pgC/l. tend to cancel out, giving overall rates of 18-23% growth of body weight per day between C I and adult.

    There is thus excellent agreement between growth rates at 12.5" given by Paffenhofer and Harris (1976) and those estimated above from the work of Thompson (1976) for animals from a nearby part of the North Sea. We therefore feel that laboratory or field estimates of the relationship between size and temperature in any given locality are all that is required (given the relative invariance geographically of develop- ment rate in relation to temperature) to calculate potential growth rates in nature when the food supply is adequate.

    I. Rate of prodwetion of egg matter

    Adult males may not feed (p. 114), but adult females certainly do. Yet they cannot grow in the usual sense after the final moult to adult- hood. Paffenhofer and Harris (1976) and Harris and Paffenhofer (1976) make a curious attempt to calculate growth rates of adults from " 50% adult to full adult ". This may compound the effects of larger adults maturing later, oogenesis and possibly fat deposition, and the very small estimates of growth rate do not appear to be very useful. The most significant use of food by females is surely in egg production.

    It is possible to determine the potential rate of production of egg matter in the same terms that we have used for growth of body dry weight. As an example, we use Thompson's'(1976) data, from which cephalothorax length (L) of an adult female (note that the regression in our Fig. 27 is for adults of both sexes) is given as a function of tempera- ture (T), when greater than S"C, by:

    L = 0.939 - 0.0322 (T - 11.57).

    Dry weight of adult females is calculated from the expression on page 127 and weight of their clutches from formula on page 92. Time between clutches is assumed (see p. 128) to be 1-25 multiplied by the duration of clutches (Fig. 22). This allows us to express amount of egg matter produced per day as a percentage of female weight, which is determined by the given temperature. These values are lo%, 12%, 14% and 16% per day at 8, 10, 12.5 and 15C respectively. These estimates for the


    southern North Sea are thus not far short of those for growth rate of older stages given in the previous section. Since eggs may be more calorific than most body tissues, egg production might be nearly equivalent to growth of younger stages.

    J. The balance equation and growth efliciencies There have been a number of attempts with zooplanktonic species

    to determine growth rates and the various efficiencies involved by estimating values of the components in the balance equation of growth (review in Conover, in press). The general equation can be written :

    G = I - E - U - R

    where G is growth rate, I ingestion rate, E egestion rate (faecal produc- tion), U excretion rate and R respiration, all in the same units.

    Gross and net growth efficiencies are respectively the proportions of I and of I - E that appear as G, all in the same units for a particular time period. These efficiencies are sometimes calculated by use of information on chemical composition, respiration, excretion and population data. The only such calculations known to us for Pseudo- calanus are in Christiansen (1968). He used nitrogen contents and excretion rates to estimate a gross growth efficiency of 74y0 and a net growth efficiency of 12.3% for the interval N V to adult for animals in Bras dOr Lake, Nova Scotia. The values are at best approximate, since some components were calculated by difference from outmoded observations.

    We have described assimilation efficiencies (I -E),/I, averaging about 65% in Pseudocalanus (p. 76). Respiration losses (R) have been estimated to amount to about 10% of body weight per day (p. 43). As Conover (in press) points out, we seem to know least about the signifi- cance of excretion (U) in terms of the balance equation of growth. Dissolved organic N and P might be represented by an equivalent loss in body weight, but even NH, excretion involves some loss that is not expressed in respiration. It has been suggested that about 5% of body N (p. 49) and about 10% of body P (p. 51) might be required each day by Pseudocalanus for maintenance. Perhaps 213 of the P might represent organic loss (p. 49) and a small amount of N (not measured in Pseudocalanus) likewise. A figure of 10% of body weight for U is probably generous.

    The work of Paffenhofer and Harris (1976) showed that older stages of Psewdocalanw may grow (Table XXV) at about 10% to 17%



    (After Paffenhofer and Harris, 1976.)

    Growth as yo body wt/day No. of Food cone.=

    experiments (pgC/Z.) Hatching to C I to end End C II I to C I c I I I adult

    1 25 20 12 11 2 50 15 30-46 4-7 4 100 16-17 22-37 17-21 1 200 20 19 17

    Nominal levels; actual levels deviated somewhat.

    of body weight per day at ingestion rates (Fig. l2F) of 60-140% per day. Entering these values as G and I along with the above estimates for E, R and U, we can see that the balance equation may in fact be balanced only at the lower ingestion rate of 60% of body weight per day.

    Harris and Paffenhofer (1 976) have fortunately estimated gross growth efficiencies directly from measurements of ash-free dry weights of accumulated rations and of growth in the same units during various intervals between hatching and adulthood (Table XXVI).

    Paffenhofer and Harris (1976) concluded that daily ingestion rates continued to increase at food levels above those at which growth rates did not increase further. This should lead to reduced growth efficiencies (probably due to reduced assimilation efficiency) at higher food levels. Although Harris and Paffenhofer (1976) found that the regressions of growth efficiencies for various developmental stages on food concentra- tions were all negative, none was significantly different from zero a t the 5% level. However, since the estimates of daily ration were based on large numbers of measurements, the reduced efficiencies implied in the work of Paffenhofer and Harris (1976) might on analysis prove sig- nificant. In other words, we suggest that the lack of significance between growth efficiencies and rations in Harris and Paffenhofer (1976) results from unnecessary grouping into reduced sample sizes.

    At any rate, the results in Table XXVI may be taken to imply gross growth efficiencies of the order of 25% at food levels that are comparable to those occurring routinely in coastal waters. In order to grow at rates of 10-20% per day, or produce egg matter at about the same rates, a copepod must thus consume at least 4 0 4 0 % of its weight per day. Most laboratory studies of feeding rate have not revealed such high values for daily rations (p. 72).


    TABLE XXVI. GROSS GROWTH EFFICIENCIES OF Pseudocalanus. (After Harris and Paffenhofer, 1976.)

    Nominal food level Number Mean growth eficiencies

    WCP. of Thalassiosira experiments N I-C I C I-C 111 C 111-Adult


    25 1 24.7 39.7 21.5 50 2 25.8 24-7 27.1

    100 5 24.4 24.8 20.1 200 2 25.6 25.8 14.5

    K. Retrospects and prospects

    It is we think possible that more is known about the growth and development of Pseudocalanus than of any other copepod. There have been a number of themes in the work that we have reviewed that are only now coming into a coherent focus.

    First of all, the work on Pseudocalanus stresses the great importance of temperature in the control of growth and development of planktonic animals. In the zooplankton literature in general, there has often been more stress on food and feeding and a tendency to carry out elaborate experiments a t single temperatures, instead of attempting to determine the temperature functions of growth processes.

    Secondly, as already noted (p. 133), we believe that most estimates of feeding rates in the laboratory are too low to support observed growth rates, such as those found by PaffenhOfex and Harris (1976). We will later argue (p. 155) that Pseudocalanus can develop and grow a t tempera- ture-dependent rates in nature, indicating that no shortage of food occurs during large portions of the year.

    Thirdly, we have shown that approaches to questions of growth and development through the " balance equation ", admittedly somewhat desultory in the case of Pseudocalanus, are outclassed by the direct approaches of Paffenhofer and Harris (1976). Respiration, excretion, assimilation and grazing are all of interest in their own right, but are unlikely to give a very accurate appraisal of the growth status of the animal in nature.

    Finally, we suggest that the conclusion that Psezcdocalanus fre- quently grows at maximal, physiological rates in nature may be true of other important copepods as well. We believe that use of temperature functions of size and development rate and perhaps simple transforma-


    tions between species based on size (Corkett and McLaren, 1970), or perhaps DNA content (McLaren et al., 1966), will lead to powerful, predictive techniques for the future.


    A. General features, terminology and approaches We have learned enough about the biology of Pseudocalanus from

    laboratory studies to know that even the most obscure or complicated life cycles must have some general features. It will help to review these before considering examples from nature.

    The nauplius emerges after an embryonic duration that is con- trolled by temperature (p. 101). The individual may develop after a temperature-dependent time up to N I11 without food (p. 112), but any further development cannot occur without food. Above a certain threshold level of food supply, development will proceed at a tempera- ture-dependent rate. If food is sustained, each copepodid stage may take roughly the same amount of time that is required for embryonic duration at the given temperature (p. 109). Mating must occur shortly after the females moult into adulthood (p. 83) and her first eggs may appear after moulting on average about the time taken for embryonic duration (p. 92).

    The female carries sacs or masses of eggs that constitute a clutch of eggs. If food is sustained, females may in theory produce up to ten or so clutches (p. 93), but this number is probably seldom achieved even in continuously breeding populations, because of natural mortality. A new clutch can appear after the previous one hatches, and after a further lapse of on average about 25% of the time taken for embryonic duration a t the given temperature (p. 93).

    Each clutch gives rise to a brood of young and all the broods produced by a female belong to the same generation (sometimes wrongly called a brood in the plankton literature). Although the time between hatching and appearance of first eggs has been called generation time in the literature on zooplankton, including Pseudocalanm (e.g. Paffenhsfer and Harris, 1976), this is incorrect. The true length of a generation is technically difficult to calculate, and we will find no use for it in this account. Nevertheless, the appearance of successive generations can often be recognized, as we shall see.

    We distinguish the productive season as that time of the year when growth, development and reproduction are sustained. Pseudocalanus suspends development during winter at high latitudes and may dis-


    appear, at least from inshore waters, during summer in the southern parts of its range. We shall present evidence that animals may store much oil and " voluntarily" suspend development in summer or autumn. We refer to these animals as being in " resting stages " although we do not imply that they give up all activities. Because of such periods of rest, the productive season tends to start with a popula- tion of animals that are largely at the same stage of development, generally late copepodids or adults, so that the initial and even sub- sequent generations can be more-or-less synchronous.

    We shall show that at high latitudes where development is slow this synchrony of life cycles allows us to identify, not only generations, but also more-or-less synchronous broods within these generations. Such a nearly simultaneous spawning gives a cohort (a generation or even a single brood) of animals that can be identified in sequential samples. Although attempts have been made in the literature on Pseudocalanus to infer life cycles from counts of various stages in temperate waters, this is much more difficult. Females may spawn a series of broods that nre unlikely to be synchronous, so that it is not possible to follow a single cohort of offspring through successive developmental stages. However, we can take advantage of two facts : (1) even when younger stages develop rapidly and are ephemeral, adult femsles are long-lived (p. 114) ; and (2) the size of adult females is strongly affected by seasonal differences in temperature (p. 11 6). Thus where generations are more-or- less synchronous and successive, there should be periods when female size is stable, followed by periods of rapid change in size, followed by periods of renewed stability at a new size. We shall see that this is precisely what is observed when samples are taken with sufficient frequency.

    Most attempts to describe life cycles have been based on samples taken in the open sea, where exchange of water and populations with different histories makes interpretation more difficult. Only Fish (1936), working in the Gulf of Maine, has attempted to follow life cycles while tracing presumed movements of populations in a, region. Studies in semi-enclosed bodies of water (Marshall, 1949 ; Carter, 1965 ; McLaren, 1969) have produced the most detailed and accurate information, giving us insights into life cycles elsewhere.

    B. Representative life cycles

    1. Tanquary Fiord, Ellesmere Island The most extreme environment in which Pseudocalanw has been

    studied in detail is Tanquary Fiord, at 81'N in the high Canadian arctic.


    Here Cairns (1967) took a series of samples with fine-meshed nets in 1964 and estimated the relative abundance of stages (Fig. 28A).

    At the beginning of the season, in late May, at least some adult females had already reproduced, but the young were stalled in NIII (which can be reached without food). After the first week of June, wasting of the snow-cover over 2-5 m of ice allowed light to penetrate the water, and development of these nauplii commenced.

    I U . , ... . . .

    E G G S - = I - I I ~ I I I


    NO /m2

    10 20 I

    0- , 20,000 May June July Aug. Sept.

    FIG. 28. Life cyclos of Pscudocnlanws in three localities in northern Canada as shown in the development of stages in samples from successive dates. Cohorts are traced as G,B,, where n is the generation number and m is the number of a brood within this generation. (A, after Cairns, 1967; B, after McLaren, 1969; C, after Carter, 1965.)

    At the same time, a group centered on C I11 began to develop. Later in the season, a second mode of nauplii appeared, but did not gain much development before the end of the seaaon. We suggest that these two modes of nauplii represent respectively two groups of more-or-less synchronous clutches produced by the female population, which was clearly dying out by the end of the season. We have accordingly labelled these cohorts as G,B, and G,B, (as first and second broods of generation 2).

    We agree entirely with Cairns (1967) that the frequency distribution of stages can only be interpreted as reflecting a two-year cycle in this


    population of Pseudocalunus. The oldest animals (Go) represent a generation that was born two summers previously. The mode of cope- podids advancing from C I11 to C V during the summer (GI) represents a generation that was born in the previous summer. The older mode of the current generation (G,B,) advanced to C I I by the end of the summer. Each of these generations need only advance one more stage to achieve the level of development found at the beginning of the 1964 season. The younger animals (G,B,) presumably would die out. Although only coarser-net ( # 6) samples were available to Cairns from 1963, the patterns among copepodids were similar to those of 1964: adults and a mode a t stage I11 were present a t the beginning of the season, and modes at C V and C I1 a t the end.

    Cairns also noted that a few small individuals disappeared from C IV and C V largely before mid-June and appeared as small adults (mean ca. 1 mm) among the large ones (mean ca. 1.2 mm) thereafter. He suggests two possible explanations. The small animals may repre- sent a basically annual form, perhaps genetically distinct (see p. 113). Or, they may represent the persistence of a limited number of individuals from the second seasonal brood of two years previously (i.e. a putative GOB,). Surface waters warmed from about -1C on 12 May to +l"C on 25 August 1964. Although this does not seem to be a large difference, the size-temperature response in these cold waters is very steep (Fig.' 26), and could readily explain the difference in sizes.

    2. Ogac Lake, BaBn Island

    The most detailed study of Pseudocalanus in a high-latitude setting was made by McLaren (1969), who was able to follow life cycles of isolated populations in three basins of Ogac Lake, a landlocked fiord on Baffin Island a t 63"N. The cycle in the innermost basin in 1957 is summarized in Fig. 28B. The overwintering Go matured rapidly in mid-June, large numbers of eggs (G,B,) appeared on 18 June, and it can be inferred that G,B, largely died out in summer, and that GIBl formed the basis of the overwintering generation. McLaren (1969) concluded from size-frequency distributions that almost all adult females in early August were Go, and that they were largely replaced by G,Bl in mid-August, so nauplii in late August were members of a new generation, as indicated in Fig. 28B. Perhaps some of G,Bl participated in the overwintering group.

    Life cycles in the middle and outer basins of Ogac Lake in 1957 were also basically annual (McLaren, 1969). Because it is more productive than the inner basin, G,B, in the middle basin largely matured by


    late August, and GIB, reached older copepodid stages. The outer basin is more productive than the middle or inner basins, but colder, so that development of three broods was sustained, although slow, during summer. I n late August, a tidal incursion greatly reduced the population, and in mid-September the potentially overwintering older copepodids were derived from G,B, in the outer basin. The pattern in the middle basin in 1962 was similar to that of 1957, except that a third brood, G,B, was sustained and reached late naupliar stages by mid-August .

    McLaren (1969) showed that the frequencies of individuals in designated broods were about as expected if each of the females in the same samples had produced a clutch of a size determined by their mean body size (see p. 96). That is, each brood did indeed represent a more-or-less synchronous production of full-sized clutches by the entire adult female population. The time between broods was about as expected from the prevailing temperatures in the lake (see p. 97). The observations thus indicate that reproductive rate was maximal during the short period in early summer when food was above some threshold, but was negligible thereafter. Evidence from an experiment with fertilized polyethylene columns suspended in the middle basin in 1962 showed that production of G, was dependent on the size and abundance of females of Go, not on the amount of food that was present during the productive season (McLaren, 1969). In the fertilized columns, GIBl and G,B, completely matured and GIB, reached late copepodid stages by early August, when a massive G,Bl appeared before termination of the experiment.

    The appearance of second summer generations in all basins of Ogac Lake, and especially in the fertilized column, indicates that the basically annual life cycle in these Pseudocalanus from high latitude need not be intrinsically controlled. That is, there is not some obligatory resting or overwintering stage a t the end of summer. In the warm waters of Ogac Lake, the tendency for unseasonable and wasteful maturation and reproduction at the end of summer may be more pronounced than it is in colder waters of the seas outside. Woods (1969) suggested that the large forms in Ogac Lake and in the similar Winton Bay represent evolutionary attempts to restore normal arctic size and slower develop- ment rates in these unusually warm waters. In support of this, she showed that two broods of the previous summer were represented in the overwintered generation of the large form in Ogac Lake in 1962, and that G,B, of the large form only reached young copepodid stages by early August, whereas (see above) G,B, of the small form had matured by this time. This means that the earliest broods of the large


    form (and therefore those produced before overwintered females have suffered further mortality) are the most successful ones.

    3. Tessiarsuk, Labrador Carter (1965) studied the life cycle of Pseudocalanus in Tessiarsuk,

    a landlocked fiord at 56'30" in northern Labrador. Here, as in Ogac Lake, there were advantages of sampling an isolated marine population. At the beginning of the 1961 sampling season in the outer basin of the lake, the first brood of young had already developed to a mode at C I (Fig. 28C). Adult females (Go) during early summer were distinctly bimodal in size (means of about 0.75 and 0.95 mm in Carter's Fig. 5). The smaller females had presumably matured in the warmer waters late in the previous summer, whereas the larger ones had overwintered as copepodids and matured in the colder waters of spring and early summer. The disappearance of the small females after the beginning of August presumably signals the replacement of Go by newly matured individuals of G,B,, but not before Go had produced a second burst of clutches, G,B,. The young in September are clearly a new generation,

    Samples taken by Carter (1965) in the following spring, on 10 April 1962, showed much reduced populations, with modes at C I11 and N 111. This suggests that most of G,B, had died out, and that the founding generation in 1962 originated largely in G,B, o i the previous summer, as in Ogac Lake. The presence of only a single size group of large (m. 0.95 mm) mature females on 19 May also indicates that all of them had matured from copepodids in the cool waters of spring. Carter suggested that copepodids in the lake in spring 1962 were probably remnants of G,B,, which would imply a basically semiannual cycle. Our analysis implies that G,B,, already " stalled " as nauplii in early September, died out during winter.

    The life cycle in the somewhat isolated inner basin of Tessiarsuk was very similar to that depicted above, except that GIBz was slightly more difficult to discern in midsummer, possibly due to sampling errors in this larger, deeper basin. The frequency distributions of stages at the end of the 1961 season and a t the beginning of 1962 were almost identical to those found in the outer basin.

    The life cycle in Anaktalik Bay, outside Tessiarsuk, did not show the same clarity as those in the lake. Both early and late naupliar maxima appeared, but whether these represented successive broods or generations cannot be discerned. A marked scarcity of older copepodids and adults, except at the beginning of 1962, suggested to Carter that most adults may have matured and spawned outside Anaktalik Bay.



    4. Other arctic local~ties No other populations from arctic waters have been studied in the

    detailed way of those from Tanquary Fiord, Ogac Lake and Tessiarsuk. However, the few other studies in general conform to one another.

    Grainger (1965) indicates that breeding and development of Pseudo- calanzts in the Arctic Ocean were unknown, and we know of no sub- sequent studies.

    Ussing (1938) and Jespersen (1939) found that the overwintering stock in fiords of East Greenland matured and began to breed in April and May, with egg-bearing females present until August. Most of G, reached C IV in late summer and overwintered in this stage. A few matured to produce nauplii of G,, probably unsuccessful, in autumn.

    Digby (1954) found that the cycle in Scoresby Sound, East Green- land, was basically annual small late copepodids giving rise to small adult females in spring, and younger copepodids developing in the cold waters to larger adults in early summer. Some of these large adults live through another winter, thus having an essentially 14-year cycle. A few individuals spawned early in the year may have matured between September and November and have been responsible for nauplii at that time, this G, being probably unsuccessful.

    Grainger (1959), working in a comparably high-arctic locality in Foxe Basin, northern Canada, found that adult males were abundant only in March through May, and adult females (and their nauplii) were common from April to September. The predominant overwintering stages were C IV and C V. Although Grainger concludes that the cycle was basically annual, he suggests that part of the population may have taken 14 or 2 years to mature. His argument is based in part on the occurrence of a size-bimodalism in C V females, but not clearly in any other stage. The larger size mode occurred between late September and early February, and disappeared at the time of appearance of substantial numbers of adults in the samples. Grainger (1959) interprets size differences (probably not correctly) in terms of food supplies, but we can only suppose that the large C V females represent a stock that had developed in colder water, perhaps elsewhere.

    Fontaine (1955) studied Pseudocalanus life cycles in the subarctic (sensu Dunbar, 1947) waters of Ungava Bay, northern Quebec. She concluded that the cycle was basically annual, but that a small portion reached maturity and spawned during late summer.

    5. Loch Striven, Scotland The magnificent survey by Marshall (1949) is by far the most

    thorough and revealing study of Pseudocalanus life cycles from tem-


    perate latitudes. It is based on weekly vertical hauls from 40 fathoms with a fine-meshed (200 mesh/inch) net. Here, the most useful means of delimiting generations is by size changes in successive samples of



    I. 2

    1 .a



    -I L I


    I 1 1 I I I I I I Jan. March May July Sept.

    F I ~ . 29. Relative abundance of C IV and egg-bearing adult female Pseudocalanus, and length-frequency distributions of adult females in samples from Loch Striven, Scotland, with temperature data. Frequency scales of histograms varied and some samples left out for clarity. (Data from Marshall, 1949, and Marshall et al., 1934.)

    Generations designated as G,.

    adult females. By reanalysing her data and expressing them in different ways, we have come to conclusions that extend or are a t slight variance with her own. Figure 29 summarizes much of what we have to say.

    As Marshall herself concludes, it seems clear that the adults (Go) at


    the beginning of January trace their origin from warmer waters in the previous autumn. Some 50% of the overwintered animals at this time were in C V, and the slight size increase of adult females in subsequent weeks is a consequence of maturation of these small C V animals at the cooler temperature obtaining in late winter. By 20 February the proportion of egg-bearing females showed a sharp increase, and this proportion was generally maintained until early August. We can define the productive season in terms of sustained high egg production as late February to early August.

    The appearance of the new G, spawned and developed in cold waters is dramatic, and shows little overlap with the females of the overwintered generation. Subsequent generations of adult females were spawned in increasingly warmer waters, and this is expressed in diminished size through the season. If successive generations retain any of the synchrony evident in the appearance of G,, this should be expressed as a series of persistent size modes, representing the females of the current generation. Between these periods of persistent size, there should be periods of rapid change of size, as females of the new genera- tion replace those of the previous one. This is precisely what is observed in Marshalls (1949, her Table X) data. Provided a suitable spacing of samples is chosen (there is not room for all her samples in our Fig. 29), the succession of generations appears very convincing. In each case, we have included the first and last samples in which a particular domi- nant size mode is expressed. We infer that during the productive season in Loch Striven, there were six successive generations (Gl-G,) of Pseudocalanw.

    Although useful in suggesting maximum reproductive rates in nature (p. 98), the information on proportion of egg-bearing females (Fig. 29, top) offers little insight into the possible succession of genera- tions. There is perhaps a hint of reproductive decline among old females of Go in mid-March and G, in late April. However, the pro- portion of C IV in the samples supports our conclusion that six genera- tions of adults were produced. Marshall (1949, her Fig. l) shows abundance of each stage as a percentage of the total numbers of animals. However, this method of expression is influenced by the highly variable mortality of younger stages and the persistence of adult females, which do not pass through in a wave of abundance. We have thought it better to express abundance of C IV as a percentage of total copepodids (Fig. 29, top). If the population were at equilibrium and if no mortality occurred during copepodid stages, then CIV on average should constitute 20% of all copepodid stages. Clearly neither of these situations applies and C IV is generally scarcer at the beginning


    of the season. However, as the season progresses, and particularly after G,, there is clearly an accumulation of C IV, and we agree entirely with Marshall that these animals have suspended development to form an overwintering stock (Go) ; at the same time some animals clearly continue to undergo normal development. These animals are evident as a series of peaks, through the season, of C IV. Only in the case of G, is there any ambiguity in these peaks, and all of them fall, as expec- ted, shortly before or around the time of appearance of the new size modes of females.



    @en. Mean no. temp C Dates

    Times between generations Cephalothorax length

    (mm) (days)

    Observed Predicted 0 bserwed Predicted

    G, < 20 Feb-4 April 6-5 G2 4 April-15 May 8.5 G, 15May-12 June 12 G, 12 June-3 July 12.5 G, 3 July-24 July 14 G, 2 4 J d y - 1 4 A ~ g 15.5

    > 42 48 1-14 1.12 42 38 1.04 1-03 28 28 0.99 0.89 21 27 0.94 0.88 21 24 0.83 0.81 21 22 0.78 0-75

    We now proceed to indicate that the successive generations of animals in Loch Striven were developing at a rate that was temperature- dependent. The first appearances of successive generations are shown in Fig. 29, as are temperatures during the developmental periods of each generation. We assume that successive generations spend their lives nearer the surface than the bottom. This is true of earlier genera- tions and at least of young stages in later generations (Marshall, 1949, her Fig. 15). The times between appearances of generations from the data in Fig. 29 are influenced first by the basically weekly sampling schedule carried out by Marshall during much of the season. Second, the f i s t appearance of a generation of adult females represents the

    vanguard , not the bulk of such females. In calculating predicted times between generations (Table XXVII), we have used the mean estimate for the period from hatching to adulthood from Thompsons (1976) experimental work for the southern North Sea. As can be seen (Fig. 25B) vanguard females in the laboratory may mature sub-

    < <


    stantially earlier than average ones, so we ignore the short additional time required for embryonic duration. We have used the regression of size of adult females as a function of temperature from Thompson (1976), ignoring the evidently abnormal size response below 8", and extrapolating for lower and higher temperatures (p. 122).

    The concordance of observed and predicted generation lengths and sizes is remarkably good (Table XXVII). We take this analysis as a strong indication that part of the population of Pseudocalanus in Loch Striven was undergoing growth and development a t a maximal, food- satiated rate between late February and late July. The prolonged absence of females of G, into September and the drop in reproductive rates after early August suggest that growth and development were thwarted by food shortages late in the season (although Marshall, 1949, registered abundant diatoms and flagellates then). The new mode of females on 2 October would be " G, " but presumably at least some joined the overwintering stock for the subsequent year, so we designate them as Go.

    One fascinating aspect of the situation in Loch Striven as revealed by Marshall is the co-occurrence of part of the population that develops a t maximal rates, and part that enters some sort of resting phase. We shall later suggest that this is commonplace among temperate popula- tions of Pseudocalanus.

    6. Plymouth, England Digby (1950) analysed vertical hauls with fine meshed nets from a

    station five miles off Plymouth, England, in water about 50 m deep (Fig. 30). At the beginning of the season adults of Go were small. Digby interprets the mode of larger adults appearing in late February as harbingers of the new generation, but the fact that they are not as large as subsequent females indicates that they matured from small overwintered copepodids (cf. Loch Striven, above) , and we designate them as part of Go. Large adults of GI were taken on 3 April and 28 April. The appearance of G, on 14 May, 41 days after 3 April, seems a little behind schedule (expected ca. 36 days a t ca. 9"C, see Fig. 25B), but large numbers of nauplii on 8 May (adults not measured then) indicate that G, appeared a few days prior to 14 May. The distinct drop in size on 2 June appears to represent G3, on schedule (expected ca. 32 days a t 1Crll"C). Digby considered that the small peak of nauplii in late June represented the beginning of G,, but we would interpret them as nauplii of G,, whose adults may be evident then and more clearly in early July, Digby acknowledged that " abundance of later stages and percentages present a rather confused picture " and


    that " the generations become more merged ", but he concludes from abundance peaks that three generations were spawned between late June and early October. Abundance peaks (particularly those in which many stages seem to peak simultaneously) are unreliable and size of adult females reveals little, presumably because of relatively small temperature change during August to October (Fig. 30, bottom) and because of advective influences in this open-channel sampling site. Naupliar numbers had dropped to low levels in September, and C I V

    FIG. 30. Size-frequency distributions of adult female Pseudocalanw and interpretation as generations (G,,), in samples from off Plymouth, England, with temperature data. (After Digby, 1950.)

    and C V began to outnumber C 1-111 in late September, comprising fully 85% of copepodids on 9 October and 91% on 23 October. Digby interprets this preponderance of late copepodids as a peak in a develop- mental sequence of the last generation of the season, and some may have matured, judging from the small drop in size of females in late October. However, since Pseudocalanus almost disappeared thereafter, we suggest that these late copepodids represent an accumulation of overwintering stages, perhaps better represented in deeper waters farther offshore.

    In conclusion, we suggest that the productive season at Plymouth


    extended from late February until a t least the end of October, with overwintering stages accumulating during this month. Up to early July the succession of generations was about as predicted from prevail- ing temperatures. If we assume that subsequent generations were not thwarted by food shortage, and able to develop at a temperature- dependent rate, at a mean temperature between early July and late October of about 16"C, a further five generations could have been spawned, for a total of nine generations during the productive season.

    7. Northumberland coast, England Evans (1977) made a thorough study of life cycles and production

    of copepods at a station five miles off the Northumberland coast. He concludes that size of Pseudocalanus is strongly affected by temperature, but argues that statistically significant differences between size distributions are the sine qua non for separating generations. He delimited the following sequence of generations between February 1971 and July 1972 :

    . . JFM)(AM)(J)(JAS)(O)(NDJFM)(A)(M)(JJ . . . In each case, the brackets delimit samples of females for the given months whose mean sizes differed (P < 0.05) from those immediately preceding and following.

    The appearance in 1971 and 1972 of a supposed new generation in April coincides with the timing in Loch Striven (Fig. 29) and off Plymouth (Fig. 30). Examination of Evans' data (his Fig. 10) indicates that the population sampled in April 1971 was indeed G , (along with May sample, largest mean length of season with small 96% c.1.). However, the sample of April 1972 probably included overlapping generations of Go and G, as females were intermediate in mean size between those of March and May, and had the highest 95% c.1. of any sample during the two years (cf. similar situations in Fig. 32, below). The completeness and accuracy of subsequent statistical delimitations of generations is questionable for four reasons. (1) samples were monthly, which may have allowed some generations to be unsampled (cf. G, in Fig. 29): (2) normal variate statistics may be inappropriate for distinguishing some generations with non-normal size-frequency distributions : (3) advective influences off the Northumberland coast (as off Plymouth) could confuse the pattern. This would appear to be the only possible explanation for a sharp and significant drop in size in October 1971 at a time of falling temperature (Evans, 1977 his Fig. 3, 10): (4) as Evans himself notes, extra generations may have occurred

  • I

    'I I

    ZJ 3


    at times when sea temperatures were relatively stable. For example, mean temperatures for 1971 were 11.4, 12.3 and 12.4" respectively in July, August and September (Evans, 1977, his Fig. 3).

    Evans uses a temperature function (from Corkett, 1970) for age of maturity that leads to an overestimate of the time required (see p. 110). He concludes, using the temperature function, that seven generations, rather than the five distinguished by him, could occur at a temperature- dependent rate during the year. We estimate that a mean temperature of around 10C (from his Fig. 3) could have allowed about seven generations (from Fig. 25B) to develop during the period between early April a


    9. Coast of Norway From variations in size and composition of samples of Pseudocalanus

    from Msre (62'52") on the coast of Norway, near Bergen, Ruud (1929) concluded that there were three main '' spawnings " (abundance of eggs and nauplii), one in March, a second in May, and a third near the end of July. In the absence of size-frequency distributions of females, detailed assessment is not possible. In Oslo Fjord (Wiborg, 1940), Pseudocalanus is said to spawn all the year round. Breeding was most intense in February to May, June to July, and August to September, but it is not possible to infer any sequence of generations from the available data. Overwintering in C IV and C V was common only in the innermost parts of the fiord. In NordBsvatn, a semi-landlocked fiord near Bergen, a succession of spring-summer generations probably occurred (Wiborg, 1944), but this cannot be inferred in the absence of size-frequency distributions of females. Older copepodids over- wintered in deeper water.

    Wiborg (1954) studied life cycles of Pseudocalanus in greater detail from samples taken in 1949-1950 from three localities off the Norwegian coast, giving information on size-frequency distributions of adult females. Here, as in the North Sea area, interpretation is complicated by the passage of water through the sampling areas. He estimated that water might be transported from the southernmost sampling site (Sognesjeen, 61'04") to the next one up the coast (Ona, at 62"54'N), in about a month. However, populations in the vicinity of Eggum, at 68'08'N off the Lofoten Islands, are presumably quite isolated from the southern ones.

    In all three localities, the f i s t main spawning period tabulated by Wiborg occurred between late February and the beginning of April. He concluded that there were three subsequent main spawning periods in each locality in both years, a t various times in MayJune, July- September, and September-November.

    Wiborg interprets size variations of adult females (his Fig. 66, and Table 51) partly in terms of population origins, but size variations certainly follow the pattern shown by populations farther south. At the more southerly Norwegian stations, distinctly larger individuals of GI appeared on 28 March 1950 a t Sognesjsen, 28 March 1949 and 17 April 1950 a t Ona, and on 23 April 1949 and 28 April 1950 at Eggum. There is a suggestion in these and subsequent samples that generations in the more northerly Eggum were some weeks behind the other two localities, but samples were too infrequent for detailed analysis, and the transport of animals may give a misleading picture.


    We illustrate the sequence of samples a t Eggum because of its interest as a northerly locality with a long productive season (Fig. 32). Samples during 1949 were taken from 190-200 m up to 50 m (except on 5 January when the whole water column from 195 m was sampled). Thus we have chosen to use estimates of mean temperatures for depths 50-200 m (from isopleths, Wiborg, 1954, his Fig. 7) as a measure of the temperatures experienced by the developing animals (Fig. 32, bottom). Although Go, G, and G, seem quite distinct and in keeping with the pattern in, for example, Loch Striven (Pig. 29) , the lapse of time between the appearance of G, and G, seems too short (from some time between 8 and 23 April to 21 May, or perhaps 40 days at most) for a, generation

    FIO. 32. Size-frequency distributions of adult female Pseudoculunus and interpretations (After Wiborg, as generations (G,) in samples from Eggum, northern Norway.


    to develop a t a mean temperature of ca. 6"C, which should take more than 50 days (see Fig. 25). Possibly this is a consequence of transport northward of populations that were slightly more advanced farther south. Although G, seems clear in late June, size did not diminish further in August. This could be interpreted to mean that no generation was produced in the interval but it can be noted that temperature changed very little during this period, rising a bit more steeply in autumn when size showed a further decrease. Certainly the sustained presence of nauplii in all three localities, with a distinct increase in autumn, suggests that populations could have been developing at maximal rates during this period. At a mean temperature of about 7"C, two generations of adults could have been produced between late July and late September, for a total of four or five for the season.


    Wiborg (1954) distinguished between P. elongatus, which name he believed applied to the common coastal form. having 3-5 annual spawnings (more according to us), and P. minutus (syn. P. gracilie, see p. 7) which he believed applied to the offshore, northern form of the Norwegian Sea (see below). He found some of the latter in his samples, distinguished by their shape and larger size, and states that it seems likely that P. minutus in Norwegian coast waters has only one spawning a year, in March-April.

    Recently Davis (1 976) has examined the overwintering strategies of Pseudocalanus and other copepods in some Norwegian fiords and sounds in the Troms0 area. He confirmed that between early November and late February C IV and C V were abundant, with a scattering of C 111, but that only a few adult females and no adult males were to be found.

    10. Norwegian Sea The study by Ostvedt (1955) in the Norwegian Sea a t 66N and

    02E depicts a life cycle of Pseudocalanus in sharp contrast to those of neritic waters farther south or west. Here there is a single annual spawning (egg-bearing females late April to late June), and a pro- nounced seasonal migration from and to the depths (see p. 162). Almost the entire population is below 1 000 m as C V between July and April. These become mature and females are fertilized and rise to the surface layers, where the new generation is spawned. These descend as C V to repeat the annual cycle.

    Soviet workers (Pavshtiks and Timokhina, 1972) have studied seasonal differences in the timing of the season of production in the Norwegian Sea, being essentially earlier south and west and late north and east. They illustrate (their Pig. 3) seasonal peaks of numerical abundance of Pseudocalanus in June in Atlantic waters, early July in mixed waters, and in late July in the East-Icelandic Current. However, no information is given on the timing of its major spawnings.

    11. Baie-des-Chaleurs, Gulf of St. Lawrence Lacroix and Filteau (1971) did not use fine enough nets to capture

    younger stages, and probably began sampling too late in the season (May-June) to detect overwintering generations. However, their size- frequency distributions of their small form changed during the season in a way that could reflect turnover of several generations. Early in the season, a group of large females (cephalothorax means 14-1-5 mm) was present, but these largely or entirely disappeared as the season progressed. On the other hand, large C V (means 1.2-


    1.3 mm) occurred throughout the summer in deeper, colder water. Lacroix and Filteau interpret these as a population of another " form ", major (see p. 8), possibly having an annual cycle. Parallels with Wiborg's (1954) distinction between life cycles of presumed P. elongatus and P. minutus (see p. 152) may be noted.

    12. Gulf of Maine and Bay of Pundy Fish (1936) made extensive studies of abundance of all stages of

    Pseudocalanus (grouped as ova, early and late nauplii, early and late copepodids, and adults) in the waters of the Gulf of Maine and Bay of Fundy. To some degree the account is confused by the use of small numbers of samples over wide areas to depict " stocks ". However, some such scheme is necessary in view of the open circulation of waters in the Gulf of Maine. Fish concluded that the succession of generations was clearest in the stock that spawned first (i.e., Go) in the western coastal region of the Gulf in March-April. He found advanced nauplii in late April and adults (GI) in late May. Tempera- tures at this time in this area were probably of the order of 34C just below the surface (Bigelow, 1927), so that a month for this period of development is as expected (see Fig. 25A). A maximum of late nauplii (of G,) in the latter part of June, ova and young nauplii (G3) on July 30, and late nauplii (G3) on August 15, are all attributed to this western Gulf stock in various parts of the region. Eggs at the entrance of the Bay of Fundy in September 15-16 were attributed to G,.

    Although neither the details of the life cycle nor the mean tempera- tures during development can be very accurately determined, it seems likely that more generations could have occurred between late May and mid-September than the two supposed by Fish.

    13. Delaware Bay Studies on the American east coast south of Cape Cod by Fish

    (1925), and by Deevey (1952, 1956), are inadequate for details of life histories of Pseudocalanus. However, they do amply confirm the fact that Pseudocalanus is essentially a, winter-spring form in this southern extremity of its range. It is also of some interest to note from Deevey (1952) that adult males occurred in samples throughout the season (January-August) in Block Island Sound. Also, neither there nor in Long Island Sound (Deevey, 1956) was there any evidence for a pre- ponderance of a " resting '' stage in summer.

    Deevey ( 1960a) depicts size-frequency distributions of females during 1931, 1932 and 1933 from samples taken off the mouth of Delaware Bay. Sampling was most frequent during the first part of


    1931 (Fig. 33). Deevey suggested that there were winter, spring and early summer ,generations in these waters, but we infer that there were more. We assume that the large individuals on 10 February were later recruits to GI developed in colder waters. The appearance of three generations in 121 days between 22 January and 25 May is reasonable for a mean temperature of about 6C (ca. 45 days per generation, from Fig. 25). The shortening of the period between generations up to G , is also reasonable, but it is affected in part by the low frequency of

    FIa. 33. Size-frequency distributions of adult female Pseudocalanus and interpretations as generations (G,) in samples from outside Delaware Bay, eastern U.S.A. (After Deevey, 1960a.)

    sampling. In the period between 25 May and 23 July, three genera- tions could have developed a t the high temperatures (i.e. up to G,). However, the resemblance in size between females from 22 July and those on 10 December, when Pseudoculanw reappeared in samples after a summer and autumn of absence, suggests that animals in July had already suspended development for the summer season, to reappear as Go of the subsequent season. We suggest that an origin of these Go animals in G6 (as in Fig. 33) is more probable than an origin in G,. In 1933, animals in November were much larger than those of July, indicating to Deevey that an earlier autumn generation had been produced in that year.

    14. Black and Adriatic Seas Extensive studies of Pseudocalanus in the Black Sea have been

    made by Soviet and Roumanian investigators, but there appear to be


    no data on size-frequency distributions of females, from which genera- tions might be inferred. Porumb (1971, 1972) tabulates much informa- tion on the relative and absolute abundance of all stages of Pseudocalanzcs, including eggs. Although it is present in all seasons, reproduction is more intense in winter and spring, when its biomass is 5-6 times as great as in summer or autumn. Reduced abundance during the season of high reproduction is attributed to predation. Altogether, it is not possible to use Porumb's numerical data to follow generations.

    Sazhina (1971) has assumed that development rate during the period from October to March in the Black Sea is not food limited. Based on her laboratory estimates (Sazhina, 1968) of age of maturity at 34-39 days at 8-lO"C, she suggests that five generations are produced in a 180-day period (October through March).

    Although measurements on Pseudocalanus from the Adriatic are available in some works (e.g. Friichtl, 1920) these are inadequate for use in delineating life-cycles. Recent work (e.g. Hure and Scotto di Carlo, 1969) confirms that Pseudocalanus is a winter-spring form. VuEetid (1957) found egg-bearing females in the landlocked Malo Jezero from January to July. 15. Sea of Japan

    Andreeva (1975, 1976b) suggests in preliminary reports that Pseudo- calanus in the northern Sea of Japan shows year-round reproductive activity, with one generation in spring, two in summer, and one in autumn. Reproductive peaks about 50 days apart in summer are said to match experimental generation lengths (egg to egg) of about 45 days, but as we suggest elsewhere (p. lll), her experiments probably over- estimated the copepodid period substantially.

    C. Retrospects and prospects

    Although populations of Pseudocalanus in the far north are clearly short of food for much of the year, the evidence indicates to us that those of temperate waters during the productive season are not food limited, but develop, grow and reproduce at temperature-dependent rates. This conclusion matches the laboratory observations by Paffenhofer and Harris (1976), who found maximal development and growth rates a t food levels that are generally present in nature (see p. 113). In Table XXVIII, we summarize theoretically possible numbers of generations of adult females that might be successively detectable in the plankton during productive seasons of various lengths at various seasonal temperature means. These are given to the nearest number of generations, calculated from the times to reach maturity



    Length of productive season (months) Seasonal mean temperature ("C)

    4 5 6 7 8 ~ ~-

    6 3 3 3 4 5 8 3 3 4 5 6

    10 4 5 6 6 8 12 5 6 7 8 9

    (mean of the two localities in Fig. 25). Presumably very long productive seasons do not occur in the far north or at the southern extremities of the range, so that Pseudocalanus might be expected to have about 3-7 generations per year (plus an overwintering or oversummering genera- tion) wherever it occurs in temperate waters.

    As yet few attempts have been made to go beyond descriptive accounts of life histories of Pseudocalanus (or other marine copepods) in order to deal with population dynamics. McLaren (1969; see also p. 96) showed that abundance of younger stages in Ogac Lake, Baffin Island, was related to abundance and body sizes of adults when food was sufficiently abundant. A paper by Lishev and Freimane (1970) seems to contain the beginnings of an analytical and predictive exten- sion of such relationships, but their collecting techniques are not given clearly and their analysis is marred by questionable reasoning in places. They begin with the unlikely suggestion that Pseudocalanus is basically monocyclic (i.e. one generation per year) in Baltic waters. They then regress the abundance of young stages during various months in the period from 1959 to 1965 on the abundance of younger, (or parental) stages during earlier months. First, they show that the abundance of nauplii in May of various years was positively related to the mean abundance of adult females and males in February and May ; this seems reasonable, although the proper relationship would presumably be proportionality of nauplii with adult females. Next, they show that the abundance of C I V in August samples is positively related to the abundance of C I, C I1 and C I11 combined in May. They assume that the C IV in August actually derive from the earlier young stages. This leads them to propose that the negative deviation of the observed regression line from the line of identity is a measure of intervening mortality. It is highly probable that generations occurred between May and August, but the observed correlation of abundances between seasons is none the less interesting. A strong correlation between abundance of adults


    in October and copepodids in August is less interesting than are similar correlations between abundances of various stages in February and abundances of younger stages in the previous October (presumably no new generations had occurred during this winter period). Lishev and Freimane (1970) also attempt to show effects of temperature on development rates using the relative abundances of younger stages as functions of temperature, but their arguments are certainly erroneous where not incomprehensible. However, in spite of some difficulties with their work, it is of clear importance in showing the strong auto- correlations that may occur within and even between generations of Pseudocalanus. As they recognize, this may have great predictive value, and we urge that their approaches be tried by others.

    Some interesting problems about life cycles of Pseudocalanus remain to be explored. We do not altogether agree with Heinrich (1962) in classifying Pseudocalanus as a copepod that will breed all year round, depending only on a sustained crop of phytoplankton. The work of Marshall (1 949) and others seems to suggest that Pseudocalanus may voluntarily suspend development before the end of the productive season. We speculate that Pseudocalanus may have a life- history strategy that involves a choice between entering a resting stage as the usual end of the productive season approaches and going on to mature and reproduce. Perhaps those individuals that have accumu- lated enough stored oil are somehow triggered into ceasing further development (at C IV-V in Loch Striven). Those that, for any reason, have been unable to store enough oil at a critical stage may go on to produce another generation of individuals, some of which may be successful in preparing for overwintering.

    It may be noted that this speculation implies that the best-fed individuals are in terms of organic matter the least productive during the latter part of the season. This may seem contrary to intuition in terms of production ecology, but is perfectly in keeping with the evolutionary viewpoint that organisms are not interested in maxi- mizing production, but in perpetuating their own kind.

    Another problem that needs to be explored is the possibility that different forms (species) of Pseudocalanus have intrinsically different life cycles as suggested by Wiborg (1954) and Lacroix and Filteau (1971). Another explanation is that large, oil-rich individuals in deeper water during summer in temperate waters may have simply developed to an overwintering stage in cooler, deeper waters. Certainly, animals of high latitudes, although basically annual or biennial, do not always seem to be able to prevent themselves from untimely maturation and reproduction in abnormally warm waters, such as


    Ogac Lake, and autumn maturation occurs among some individuals even in the colder arctic and subarctic waters of Greenland a,nd Ungava Bay. This suggests to us that these northern animals, given enough food, could have several successful generations in a year, without necessarily suspending development.

    We suggest that further studies of " landlocked " populations in various parts of the world would be revealing, as would experiments on the character of overwintering stages.


    Elsewhere we have discussed vertical distribution of Pseudocalanus in the sea during the daytime (p. 120). In this section we are concerned with the dynamic aspect of vertical migration. Die1 vertical migrations have attracted most interest, but Psezdocalanus shows longer term migrations as well and we designate these as seasonal and ontogenetic migrations. Ontogenetic migrations are defined below, but it is important to note here that we limit our definition of seasonal migration to migration to the depths that clearly involves some sort of resting or overwintering phase in the population (p. 157).

    A. Ontogenetic migrations

    By ontogenetic migration, we mean the change in position of individuals in the water column (as observed by night or day) as they develop. Of course, individuals cannot be followed through extended time, and we must infer such movements from the distributions of stages a t any given time or over a period of time.

    The tendency for younger stages of Pseudocalanus to occur nearer the surface has been noted a t least as early as Kraefft (1910), and by numerous authors since (e.g. Ackefors, 1969a, b ; Marshall, 1949; Wiborg, 1940, 1954). Exceptions have occasionally been noted (e.g. Minoda, 1971). There are few details in most of these studies, but observations from two stratified, landlocked arms of the sea in northern Canada (Carter, 1965; McLaren, 1969) and from the Black Sea (Afrikova, 1975) are quite revealing.

    Carter (1965) illustrates vertical distributions of all stages in the inhabitable upper 30 m (oxygen depleted in deeper water) of Tessiarsuk, in northern Labrador, on 2 July, 2 August and 26 August 1961. On each occasion there were proportionately more egg-bearing individuals among deeper females and earlier nauplii were found slightly deeper on average than were later ones. A pattern of upward swimming after


    hatching is implied. Older stages were found generally with maxima in progressively deeper water, sometimes several successive stages showing the same patterns of distribution. A marked bimodalism in depth distribution of some stages is of interest. On 9 July there were peaks of all stages at or just below the sharp thermocline and halocline at 4-6 m, and deeper maxima of C 1-111 and adult females between 10 and 15 m. There were similar dual maxima on 3 August in C 111-IV, CVd, and adult females. There is a suggestion on 9 July of descent among older nauplii, which would have been members of second brood (G,B,, see Fig. ZSC). Perhaps the deeper individuals among C 1-111 in early July and C 111-V represent later-spawned individuals, some from

    Temperature ("C) Sample depths

    06 7 8 9 10




    FIG. 34. Vertical distributiom of P.sedocalanua in the middle basin of Ogac Lake, Baff i Island, around mid-day on 21 August, 1967. (After McLaren, 1969.)

    the second brood of the season, while those staying near the surface were earlier in origin. The bimodal depth distributions among adult females may also reflect a dual origin, for during early summer two size modes representing autumn and spring maturation (see p. 140) were present.

    Carter (1965) also depicts detailed depth distributions in Anaktilik Bay, outside Tessiarsuk. In the bay, where there was little stratification, older stages were found deeper, as expected, but there were no sharp depth-maxima.

    A series of samples from Ogac Lake, a landlocked fiord on Baffin Island, were particularly revealing (Fig. 34). The pattern can be interpreted as ascent to the surface by young nauplii, followed by descent beginning a t C 111. Here again (as in Tessiarsuk, above) it is possible that the two groups in C I11 represent two different origins, in





    -A,--- -!..

    ! \ -! 1


    .,, -\


    -* --

    .,Chlor. \.

    - ,-7 -

    .. , # * -.-.

    I I I I I I I I I I

    suggests that the ontogenetically descending animals were seeking colder waters and were loathe to penetrate the temperature peak at 15 m.

    The pattern of depth distribution in Ogac Lake in mid-August 1962 was entirely different (Fig. 35). The peak of abundance of all


    stages near the surface was related to a persistent peak of phyto- plankton abundance just below the halocline (the chlorophyll peak was reduced by mid-August, as seen on Fig. 35; see McLaren, 1969). The deeper maxima of Pseudocalanus were also found at higher food levels.

    Females in the deepest samples in 1962 showed a bimodal size distribution, the smaller ones probably representing animals that had recently descended from the concentration in warmer, near-surface waters (McLaren, 1969). This suggests that descent can be a sudden " decision " at any stage.

    Afrikova (1 975) depicts percentage distributions of all stages (eggs, NI-V grouped, N V I and each copepodid stage separately, adult females and adult males) in seven strata down to 200 m in three regions (northwestern, central, eastern) of the Black Sea in February, April, August and November. It is difficult to generalize from this massive survey without data on time of day, hydrographical and phyto- plankton conditions, but a few observations on possible ontogenetic movements can be made. A t times the peaks of depth distributions of all stages coincided, so that any movements must have taken place within the 25 or 50 m strata. At other times, adult females, ova, and sometimes NI-V showed primary or secondary peaks in deep water that were not exhibited by N VI so that an upward migration of young stages is implied. Copepodid stages generally occupied mid-depths, with adults often showing clear primary or secondary peaks in deeper water in most regions and most seasons. This suggests that adults may migrate deeper (we will show this below, p. 166, to be true of adult diel migrants in the Black Sea). An exception was in April in the northwestern part of the sea, when females were most abundant near the surface, whereas younger stages were deeper.

    We offer the following tentative conclusions about the nature of ontogenetic vertical migrations by Pseudocalanus. (1) Younger stages are generally found nearer the surface. (2) Animals at the same stage, but of different developmental histories, may show different depth preferences. (3) The avoidance of warm, near-surface tempera- tures by, in particular, older stages may be involved in their descent.

    B . Seasonal migrations Many authors have noted the tendency of copepod populations to

    be found in deeper water as the productive season (as defined in p. 135) progresses. Althoughall stages may be involved, often the descend- ing population may have developed to one or a small number of stages. Among those in more recent studies who mention the phenome-

    A.X.B.--15 8


    non in different populations of Pseudocalanus, VuEetM (1961), Carter (1965), Ackefors (1969b) and Porumb (1971) have suggested that gradual seasonal descent is related to withdrawal from warming of the surface waters. However, others have described a migration t o the depths that clearly involved some sort of resting, overwintering phase in the population, and it is this phenomenon that we wish to designate as seasonal migration.

    Marshall (1949) found that all stages in Loch Striven, Scotland, were mostly above 10 m from late January until late June. Most were below 10 m during July, but nauplii, and C I and C I1 were still above 10 m in August. Although she invoked warming of the surface waters (see Fig. 29) and possible water movements to explain parts of this pattern, Marshall clearly ascribes the descent of the major part of the population after the end of June to the preponderance of the over- wintering stage C IV (later becoming C V).

    Ussing (1938) and Digby (1954) describe a similar seasonal sinking of stages between C I1 and adult in the fiords of East Greenland. They overwinter and gradually develop at depths below 50 m. In the shallower Foxe Basin, in arctic Canada, there was no evidence for such a partial disappearance of the stock in winter (Grainger, 1959).

    Kovalev (1967) indicates that copepodids and females are absent from suface water of the Black Sea in summer, but that there are peaks at 75-100 m in both summer and winter. The more extensive work of Afrikova (1975) shows a strong secondary peak of abundance in deep water of all copepodid stages in the central part of the Black Sea in August 1951. No such peak is evident in samples from November 1954, so that the August distribution might be taken as an example of seasonal descent. However, in February 1956, in the northwestern part of the sea, all copepodid stages were most abundant in the deepest layers, with secondary peaks in shallower waters, ao that the pattern of descent is not clear. We cannot determine if there is a seasonal resting stage in these Black Sea animals.

    A profound seasonal migration in the Norwegian Sea has been described by Bstvedt (1955) and confirmed by Hansen (1960). The overwintering animals below 600 m (mostly 1 000-2 000 m) consisted almost all of C V. A small number of C IV stayed above 600 m. When the ascent began in March, a large portion of the mature animals had already matured below 600 m, and few adult males reached the surface layers. By June, C V began to predominate, and by July most of these had moved into deep water.

    Although only a few studies have demonstrated it, we believe that the seasonal descent of " resting " overwintering stages may be the rule


    among Pseudocalanus populations in temperate waters. McLareii (1963) argued in support of conteiitions by some authors that this behaviour allows animals to conserve their energy stores in the cool depths. McLaren (1974) stressed the fecundity advantage froin large size in colder waters (p. 116) when life cycles are seasonally interrupted. In the Norwegian Sea, the animals migrate beyond 600 m, where there is a sharp temperature change, to depths that are 6-8OC cooler than the surface a t any season (0stvedt, 1955). In inshore waters, the surface may become colder than the deeper waters by the time animals return to the surface to commence breeding (Marshall, 1949). We shall demonstrate in the next section (p. 171) that these resting stages may forego diel vertical migration into warmer waters in summer.

    C. Die1 migrations

    Before proceeding further we must clearly distinguish between the operation of and the significance of vertical migration. Hardy (1956) writing about the phenomena of vertical migration reported, It would be nice and tidy if one could just pin down the operating factor to some such relatively simple thing as the movement up and down of a particular light-intensity-although it would in no way tell us what was the actual reason, in terms of advantage to th,e animal, for such a reaction being evolved (our emphasis).

    In this review, in addition to purelydescribing vertical migration, we will largely concentrate on aspects that relate to the significance of rather than the operation of , since relatively little study has been made on the physiological control of vertical migration by Pseudo- calanus.

    1. Observations Although there are numerous published observations on vertical

    distributions of Pseudocalanus, few show differences between night and day. Here we will stress studies that are based on close spacing in depth and time, give insights into behaviour of different stages, or offer additional data on the physical, chemical and biological circum- stances found in the water column at the times of sampling. In addition to describing diel migration, we will bring the readers attention to conditions in the water column (temperature, food, predators) and to differences among seasons and among stages, all of which have some bearing on the possible adaptive significance of migration described later.

    Evidently the first sketchy observations on vertical migration of




    * + + -

    1 1 1 1

    + t I L m & + -+I 150 1 1 I



    Time of doy

    FIG. 36. Vertical distributions of Pseudocalanwr in the Black Sea at various times, during a 24 hour period in March 1973. (Data for C I, C 11, and adult 3 from Zagorodnyaya, 1974, and for C I11 adult 9, including unbroken and broken arrow8 for presumed strong and weak migrants, after Zagorodnyaya, 1975.)

    Pseudocalanus were made by Savage (1926), Bigelow (1926) only implying that it probably occurred in this copepod. Savage found greatest abundance near the bottom by day and fairly even distribution in the water column at night, but supplied few details.

    Migration in the Black Sea was described by Nikitine (1929) and ;t number of authors subsequently. Porumb (1971) studied migrations


    into the top 5 or 10 m, and found that animals did not enter these waters when temperatures rose above 23C. The most thorough study of vertical migration of Pseudocalanus in the Black Sea (Zagorodnyaya, 1974, 1975) also gives the most striking examples of the phenomenon of which we are aware (Fig. 36). Samples are taken on unspecified dates in March 1973, about 40 miles off the coast near Sevastopol. Unfortunately, Zagorodnyaya gives no details on methods of capture, population sizes or physical-chemical conditions in the water column. Although she states that temperature of all strata a t the time was about 8" (which temperature she uses later in assuming a speed of passage of food through the guts of the copepods), there may have been some thermal stratification at this time (see Petipa et al., 1963). No data are given on vertical distributions of copepods in another series from January 1973, although migration was said by Zagorodnyaya to be weak.

    Clearly, vertical migration was marked in older stages a t least, although doubtfully in adult males (Fig. 36) whose scarcity may have produced sampling problems (see unlikely distribution a t 1900 h). Zagorodnyaya (1975) concluded tentatively from inspection of the distributions that there were two classes of migrants : strong and weak. For example, the almost complete compression of adult females from the upper layers at 0300 into the layer at 50-75 m at 0700, indicates that these upper-layer animals moved faster and farther than those that moved, at most, from 50-75 m to 75-100 m. We include her arrows, tentatively interpreting the movements of these supposed weak and strong migrants (Fig. 36). By using this grouping into strong and weak migrants, in ways which she does not make altogether clear, Zagoro- dnyaya (1975) estimated the residence times of individuals in different depth layers. Using observations of the gut contents of copepods in each layer and experiments on passage of food through the guts (see p. 71), she was able to estimate daily rations for weak migrants, strong migrants, and for possible non-migrants. Accepting the existence of these classes of migrants in March, she showed that strong migrants in stages C I11 to adult female consumed more than weak migrants which in turn consumed more than supposed non-migrants. She also analysed gut contents of animals in January and concluded that the differences between weak migrants and strong migrants during that month were very slight, evidently because migration was only of small amplitude.

    Zagorodnyaya (1 974) showed from observations on fullness of guts (see discussion, p. 74) that almost all food was secured at night. The actual rations she calculated (maximum about 12% of weh &/day by strongly migrant C V) would not be enough to satisfy the daily needs of


    growing copepods (see p. 133). However, the relative differences in daily ration among classes of migrants are of great interest, since they imply that strong migrants either needed more food or could obtain more food, both of which may have energetic implications.

    Zagorodnyaya and Svetlichnyi (1 976) demonstrated diel changes in specific gravity of individual Pseudocalanus associated with these diel rhythms of feeding and migration : adult females, but not non-feeding adult males, showed a lower specific gravity at night when their guts were mostly full.

    Afrikova ( 1976) analysed vertical distributions of Pseudocalanzcs from samples taken at P 5 h intervals over three 24 hour periods in June 1959 from the west-central Black Sea. The net samples were from 0-10 m, 10-25 m, 25-50 m, 50-75 m and 75-100 m, presumably (not stated) by stratified oblique or vertical hauIs. Her Fig. 2 (date?) illustrates a marked thermocline from ca. 8C to ca. 16C between 25 m and 10 m with near isothermy below and above these depths. There was a more gradual halocline from ca. 21%, to ca. 18%, between 75 m and 50 m. Afrikova, in ways not made fully explicit, calculated mean depths of occurrence for each stage at each time during the three 24 hour series. These mean depths (her Table 1) do not match the peak depths for grouped stages on her Figs 1 and 2 (which show continuous curves of biomass against depth rather than histograms of numbers in each sampled layer). We have difficulties in interpreting some of her results, and we feel that the amplitudes and rates of migration for each stage as tabulated by her must be strongly depend- ent on the discrete sampling intervals used for depths and time. However, the general pattern of peaks in her Figs 1 and 2 seems to be fairly consistent within stages between sampling dates.

    Because Afrikova (1976, her Fig. 1) grouped eggs (which cannot possibly migrate unless attached to females) with N 1-111, we cannot interpret movements of these youngest nauplii. Older ones (N IV-VI) are shown as having moved up by day in one sampling series, but generally as peaking in the 25-50 m layer at all times of the day and night during the other two series. Peaks of both C 1-111 and C IV-V are shown as generally between the 10-25 m and 25-50 m layers (i.e. evidently at around 25 m, just below the thermocline). The older animals (C IV-V) were much more concentrated in the upper part of the 10-25 m layer (i.e. in the warmest water available) by night. Adults (sexes combined, but presumably largely females) were much deeper by day, with peaks shown at the boundary of the 50-75 m and 75-100 m layers. At night, peaks were generally between the 25-50 m and 50-75 m layers (one peak shown between the 10-25 m and 25-50 m


    layers). Adults thus showed the greatest amplitude of migration, but this did not evidently carry them substantially into the thermocline ; this contrasts with the above-described pattern for older copepodids. Afrikova does indicate (without giving data) that adult males in one 24 hour series rose in evening (2000--2100 h) to 0-10 m.

    From dissection of guts, Afrikova (1976) concluded that most feeding by copepodids and adult females took place in the 10-25 m or 25-50 m layers, but that some food was secured in deeper waters also. She states that migration by Pseudocnlanus in general was less abrupt nnd the diel feeding rhythm less marked than for Calanus kelgolandicus in the same waters. She also concluded that temperatures and salinities had little influence on the amplitude of migration. However, as we have indicated in the previous paragraph, the response to temperature does appear to vary with stage : young individuals being generally resident at all times at cool mid-depths; older copepodids moving from mid- depths into warm, near-surface waters at night ; and adults living deep by day, migrating farthest up to mid-depths, but not generally accom- panying the older copepodids into the thermocline.

    In the Adriatic region, VuEetii: (1961) found that animals in Vcliko Jezero (a coastal saltwater lake) occurred near the surface in Janiiary and deep in summer. However, her limited samples revealed no evidence of diel vertical migration during either season.

    Bogorov (1 946) found that Pseudocalanus remained constantly in shallow waters in the Barents Sea during summer, but found a weak movement toward the surface in localities in the White Sea farther south. Bogorov interpreted these patterns in terms of the 24 hour daylight obtaining during summer a t the higher latitude. However, we note that surface waters a t these high latitudes would be warmer farther south, especially by Iate summer. McLaren (1969) took daytime and night-time samples from another arctic location, Ogac Lake on Baffin Island (Fig. 35). Here, in spite of complete darkness at night on 14-15 August 1962, and in a highly stratified water column, there was very little, if any, vertical movement of any stage. Slight apparent differences in the distributions (Fig. 35) can be attributed to sampling errors and the differences in depths sampled by night and day. What is of interest is the strong concentration, night and day, at depths where chlorophyll concentrations were highest (the near-surface peak in chlorophyll had been more pronounced in previous weeks ; McLaren, 1969). Development rate at this time of year in 1962 (McLaren, 1969, his Fig. 2; see also Fig. 28B in this work) was very slow, and possibly the animals were obliged to feed throughout the 24 hours. There was strong migration of immature Sugittu elegam (making up the mobile


    part of the predator carbon biomass in Fig. 35). It is of interest that the deeper peaks of predator concentration and the night-time peak of migrant predator concentration coincided with copepod concentrations.

    Some studies in the eastern North Atlantic and adjacent waters have supplied little information on diel vertical migration relating to physical- chemical conditions (e.g. Savage, 1931 ; Malikowski and Ciszewski, 1962). Hansen (1951) found that adult female Pseudocalanus did not migrate through marked temperature-salinity gradients at 9-1 3 m in waters near Oslo in late June 1947. Adult males were less migratory, and we infer that younger stages (said by Hansen to occur a t 0-50 m) were above or were able to migrate through the gradient, but details are not given.

    The most detailed study in European waters has been made by Lee and Williamson (1975) who observed vertical distributions and movements of Pseudocalanus (adults and copepodids combined) in the Irish Sea. Although they depict vertical distributions of tempera- ture salinity, 0,, SiO,, NO,, NO, and PO,, we doubt that most of these have any influence on vertical movements of copepods (contrary to their suggestions ; see also our comments in p. 22), and we show only temperature in Fig. 37. On every date, there appears to have been some vertical migration. However, there was no single pattern with respect to timing of the light cycle. The upward movement well before sunset on 4 May 1969 was particularly striking, as was the lag after sunrise on 4 July 1970, and the presence near the surface a t all times on 21-22 October 1970. These observations are contrary to the usual notion that migrants avoid the surface during daylight hours. Migration appears to have been least coherent on 21-22 October 1970, when the waters were the least stratified thermally of the five dates. In general, the distributions give the impression that only parts of the populations moved towards the surface, and on 11-12 August 1970, it appears possible that another part might actually have moved down. Wide spacing of the horizontal plankton hauls, the rather strong currents in the Irish Sea, and the grouping of all older stages in the counts by Lee and Williamson, probably preclude closer analysis of the data in Fig. 37.

    In the Pacific and adjacent waters, Japanese and Soviet workers have investigated diel migrations of Pseudocalanus, but only some studies refer to conditions in the water column. Minoda and Osawa ( 1967) found Pseudocalanus and other copepods concentrated near the bottom of the thermocline, which coincided with a daytime sonic scattering layer in the Okhotsk Sea in early August. Their widely spaced hauls, above, within, and below the scattering layer, gave no


    evidence of diel migration of Pseudocalanus. The most extensive studies are in Minoda (1 97 l), who found relatively uniform distributions in the upper 50-200 m during May, June and July in the seas east of Kamchatka. We interpret his Figs 13 and 14 as showing increase at the surface by night at two stations, a decrease at two stations, and no change at three stations. Thermal stratification was generally weak in the upper 50 m.

    - 0- 20.21-22 oct.

    4 0 r -

    1200 1600 2000 2400 0400 0800 13 15 Time TempPC)

    FIG. 37. Vertical distributions of Pseudocalanw (copepodids and adults combined) during various 24 hour periods (SS is sunset and SR sunrise) in the Irish Sea in 1969 and 1970. (After Lee and Williamson, 1975.)

    The most complete set of observations of diel vertical migrations of Pseudocalrinus anywhere have been made by Lock (1968) in the relatively enclosed Bedford Basin, near Halifax, Nova Scotia. He paid particular attention to precise depth controls, using horizontal hauls with quantitative Clarke-Bumpus plankton samplers. The rather coarse-mesh net (variously clogged) led to variable results for the youngest copepodid stages, and we review here only the depth dis- tributions of stages C 111-V and adults (Fig. 38). Lock separated the sexes of C IV-V, and although we group them in Fig. 38 we at times

  • f a p"


    60 , ." I

    I . I

    60 t 103 ~ I

    60 f ' i i

    60t% I I SS I ISR 1 : ~ ~ 3 ~ l p l 12 16 20 00 04 08 1200

    0 8 20 60 1.0 1.1 0.4 0.8

    40 60

    c r-

    Temp.('C) 103cells/l 9 L(mm) Var.L(mm) TempPC) lo3 cells/l ? L ( m m ) Vor.L(rnm) Temp.(OCI IO*cells/l ?L(mrnl Vor.L(mml :Q. 38. Vertical distributions of Pseudoealanus in Bedford Basin near Halifax, Nova Scotia, during three 24 hour periods on three occasions, 1967.

    Note that no samples were taken from below 42 m in the first series. Cell counts are net-phytoplankters ; 9 L is mean length of cephalothorm and Var. L is the variance of cephalothorax length of adult females at the two given times of day during each sampling aeries; SS is sunsot and SR is sunrise. (After Look. 1968.)


    discuss sexual differences below. Phytoplankton cell counts do not include very small forms or flagellates, which may predominate in Bedford Basin (Poulet, 1974).

    In early May, C 111-V appeared to be concentrated just below the thermocline at mid-day. Migration to the surface was strong in C I11 and C IV, which were found near the surface well before sunset (see similar situation early in the season in Fig. 37). Among the C IV at the surface in late afternoon 80% were males, although overall in the water column 52% were males. Female C IV thus appeared to spend more time in the cooler depths. Stage CV only occurred near the surface in the midnight sample, and sexes behaved similarly. The evidence for migration of adults (both sexes) is weak but there does appear to have been some increase in shallow waters at night. Animals rising above 10 m would have experienced somewhat warmer waters, but the counts of phytoplankton cells suggest that little variation in food occurred in the upper 35 m or so.

    In mid-July, the pattern was rather different (Fig. 38). Migration in C I11 appeared weak, with perhaps only a small part of the popula- tion involved, in the middle of the night. The non-migration in C IV is very striking. This stage (see scale differences in Fig. 38) greatly dominated the population a t the time, and was found concentrated in deep water throughout the 24 hours, with only a small hint of increase at the 6 m level around midnight. Clearly these are " resting ", potentially overwintering animals, similar to those that have been documented in Loch Striven, Scotland (see p. 144). The change in behaviour in C Vis equally striking. Although part of the population may have stayed in deep water, there was a clear movement to shallow water commencing before sunset, and a movement away from the shallows commencing before sunrise.

    We suggest that, although some CV may also have been resting, some were active migrating members of a developing generation, like their counterparts in Loch Striven. Both sexes of C V were involved in the peaks nearer the surface at night, but only males exhibited this peak in the early morning, thus staying longer in the warm water. Adult females also clearly moved upward to the surface at night, perhaps not quite as far or for quite as long as did C V. Adult males showed little if any migration. It can be seen from the lower panels of Fig. 38 that migrants in July generally did not enter the very warm surface waters. Those a t 6 m (early night peak of C V) were a t about 12"C, where phytoplankton was also evidently very concentrated. Those at 12 m (peak of femaIes shortly after sunset) were at about 7OC at a concentra- tion of cells about two-thirds the maximum value at 6 m.


    In mid-December the evidence for migration among young stages was equivocal. It appears possible that the bulk of the population stayed deep during the 24 hours, and that another part stayed in shallower waters, some approaching the surface near sunset. The situation among adults is intriguing. There was a clear concentration, especially of adult females, at the surface for a short period after sunset. The water column was almost isothermal and phytoplankton evidently scarce a t the time.

    Lock (1968) also graphed means and variances of sizes of adult females for times of day between which depth distributions changed most rapidly (lower panels of Fig. 38). Although he does not supply significance tests for most of the differences between depths and times, he does state that at least 100 females were measured from each time- depth sample. The interested reader may be able to estimate the approximate significance of the differences between means by seeing where they differ by more than d(var . length)/2/100. By these crude methods deeper animals can be shown to have been generaIly signifi- cantly larger on average than those from shallower depths. In a few instances, significant differences occurred between mean sizes at the same depth at different times of day. Also, P tests (ratios of variances) imply that animals were more variable at certain times of day a t the same depths. We do not describe such differences in detail or attempt to explain them here, but simply offer them as indications that animals of different sizes within the same stage may have different migratory habits.

    2. Control by light Although other factors may influence the depths occupied by

    Pseudocalanus (e.g. pressure, see Digby, 1967), the " operating factor " of diel migration has generally been considered to be related to diel light cycles. Little detailed work has been done on the relationship between diel migrations and diel light levels in Pseudocalanus, but some observations have been made, particularly in relation to solar eclipses, and these we outline below.

    Two studies have been made involving the response of Pseudocalanus to solar eclipses. Skud (1968) sampled quantitatively 0, 10 and 20 m at, before, during and after a total eclipse in late afternoon (totality 1745 h) of 20 July 1963, on the coast of Maine. Temperature was about 11.3" at 0 m and 9.3"C at 20 m. Pseudocalanus was one of two species of copepods out of seven believed by Skud to exhibit some response to the diminished light. His graph indicates that Pseudocalanus did not occur in surface samples, so his evidence for upward movement


    must be based on changes in the middle depth, at 10 m. On July 20 only a few per cent of the population were at 10 m before the eclipse, compared with some 30% during and after totality. However, his graph also shows that on the previous day (when animals in general occurred higher in the water column, possibly because it was less bright), 40% of the population was a t 10 m before, 70% during, and 55% after the time of totality on the following day. Such variations seem to us to make interpretation difficult.

    Sherman and Honey (1970) made a study of the vertical distribu- tions of Pseudocalanus a t 0, 10 and 30 m in relation to the near-total eclipse a t Boothbay Harbour, Maine, on 7 March 1970. The water column a t the time was almost isothermal a t 1-6-2-0"C. On the day before the eclipse, adults of both sexes were generally concentrated near the bottom, rising to the surface in late afternoon, and evidently leaving it after sunset, reminiscent of the situation in December in Fig. 38. An odd concentration at 10 m occurred in late morning of both days, but the upward movement at totality of both sexes, especi- ally males, seemed quite clear.

    It is not surprising that Pseudocalanus should respond to decreased light but observations in the previous section suggest that the response is greatly modified by seasons and circumstances. The rise to the surface well in advance of sunset early in the season in the Irish Sea (Fig. 37) and Bedford Basin (Fig. 38) is especially intriguing, as is the complete lack of response of some stages at some times in some conditions of the water column. In the literature in general a common response to light is said to involve upward movement with change of light at both dusk and dawn, with randomization and net downward movement during darkness. There is no evidence of this dusk and dawn rise in the observations on Pseudocalanus in the Irish Sea (Fig. 37) and Bedford Basin (Fig. 38); there was rather at times an asymmetry in the nocturnal response, with more animals near the surface at dusk than at dawn.

    3. The adaptive value of die1 vertical migration Many explanations have been posed for the significance of the

    pervasive phenomenon of vertical migration of zooplankton. Whatever the explanation, it is axiomatic that migrant behaviour must generally confer some selective advantage to individuals. In asking why animals migrate, it is assumed that there must be some '' cost " involved as well. Evidently Afrikova (in a 1972 symposium proceedings quoted by Klyashtorin and Yarzhombek, 1973, but unavailable to us) has esti- mated from loss of stored oil that the energy consumed by a migrant Pseudocalanus would add little to its " routine " metabolism. This is in


    accord with other recent work on energetic costs of vertically migrating Pseudocalanus (Svetlichnyi, et al. 1977) based on calculations of work required to overcome hydrographic resistance and gravity.

    As is so often true of animals, there is probably more than one explanation for a complex behaviour. Furthermore, explanations involving selective advantage in evolutionary time may be difficult or impossible to test. The best we can do is to see if one or another explanation appears to conform better with observations made at some times in some places.

    We propose here to examine three hypotheses as possible explana- tions of die1 vertical migration by Pseudocalanus. The first of these, the predation hypothesis, has not been developed in the literature as a specific explanation for vertical migration of Pseudocalanus. However, it is so widely accepted and seems so plausible that we feel it should be included with reference to observations on Pseudocalanus. The second, energy-bonus hypothesis was developed as part of an essentially demographic hypothesis with specific reference to Pseudocalanus by McLaren (1963). Later, McLaren (1974) found the energy-bonus to be unnecessary in the development of the demographic hypothesis. However, the energy-bonus part of the original (McLaren, 1963) hypothesis stands on its own, and we feel justified in including it with reference to observations on Pseudocalanus. The third, demographic hypothesis, was clearly developed with Pseudocalanus as a model (McLaren, 1974). In examining these three hypotheses we will again bring the readers attention to conditions in the water column (tem- perature, food, predators) that are of consequence in these hypotheses.

    (a) The predation hypothesis McLaren (1963, 1974) agreed that, of a number of long-standing

    explanations for vertical migration, avoidance of visual predators during the day was most plausible and perhaps the chief reason for migration at night, rather than by day, even if migration had some other primary advantage.

    Of course, the observations on Pseudocalanus show that in general it does leave the surface by day, which could indeed help in avoiding visual predators. However, this does not always seem to be a sufficient explanation of its migratory behaviour. For example, why do young stages (which are possibly most vulnerable to predation) tend to remain near the surface (e.g. Fig. 34) and be less migratory (Fig. 36)? Why are adult males, admittedly short-lived even without possible predation, generally so much less migratory (Fig. 36 ; 16-17 July in Fig. 38)? Why do animals approach the surface at times long before sunset (May,


    Figs 37 and 38), or stay there after sunrise (3-4 July, Fig. 37), or spend the entire daylight period in well lit surface waters (p. 167 ; October, Fig. 37), if such behaviour would expose them to visual predators?

    In Ogac Lake non-migrant Pseudocalanus may contend with their chief predator Sagitta elegans (presumably a non-visual predator), migrating toward the surface a t night (Fig. 35). Pearre (1973) also showed that migrating S. elegans in Bedford Basin fed on Pseudocalanus most heavily at night. A case might be made in these situations for the evolution of descent by Pseudocalanus at night to avoid predation.

    All the above observations seem to pose problems for the predation hypothesis of vertical migration. Nevertheless, the advantages of avoiding visual predators seem so plausible, that we believe that predation must play some role in the diel migration of Pseudocalanus, but that it is at times over-ridden by other factors.

    (b) The energy-bonus hypothesis McLaren (1963) offered an original analysis of the way in which

    vertical migration in thermally stratified waters might be advantageous to the individual migrant because of enhanced fecundity (by which he meant clutch size in the case Pseudocalanus). He began his arguments with the widely held notions that animals in deeper, cooler water could conserve energy and that this energy gain could be advantageous for a number of reasons. This had been offered as an explanation especially for the seasonal retreat from warm surface waters by overwintering stages (see p. 162). McLaren (1963) assumed that Pseudocalanus could secure all the food it required by night nearer the surface waters, where food would usually be more abundant and more rapidly ingested at the generally higher temperatures. This food would then be metabolized with less respiratory loss in deeper, cooler waters, thus conferring an energy bonus that would be partly lost by staying in the warm surface waters.

    We have seen that Pseudocalanus may be satiated by food levels that are well within the range found in nature (p. 68), and that it may show marked diel rhythms in feeding (p. 72). We have also shown that, in populations where migration surely occurs, animals are capable of developing at maximal, temperature dependent rates (p. 144). Altogether, the evidence we have reviewed confirms the premise that Pseudocalanus can at times secure an adequate daily ration for maximal growth rates by feeding during only part of the 24 h period.

    Even if energetic costs of migration are small (p. 173), the energy- bonus hypothesis predicts that migration would not be advantageous in an isothermal water column. McLaren (1963) reviewed a wide


    literature on different species suggesting that migration was generally weaker in unstratified waters. Certainly some migration occurs in Pseudocalanus in unstratified waters. However, our review suggests that migration was weakest in two seasonal series (Figs 37, 38) in autumn and winter when waters are isothermal. Observations in December in Bedford Basin (Fig. 38) seem to suggest that adults in particular sampled the surface water at dusk and, finding them unsuitable (no warmer?), returned to deeper water. We have also recounted other evidence that vertical distribution and migration of Pseudocalanus is in general strongly affected by temperature.

    McLaren (1963) suggested that the energy bonus of migrants might appear in accumulated oil for overwintering in copepods. The work of Lock (1968) indicated, if not conclusively, that animals reared in alternating warm temperatures by day and cold temperatures by night laid down more oil (p. 128). However, animals observed in a similar experiment seemed to have food in their guts at all times during the 24 h period suggesting to Lock and McLaren (1970) that a diel feeding rhythm might not have been involved.

    As McLaren (1963) pointed out, the complete cessation of migration by resting animals in the overwintering stock (see C IV on July 16-17, Fig. 38) might be viewed as an extension of the energetic gains of diel migration : these animals by ceasing migration altogether conserve energy at much lower temperatures.

    Altogether, there appears to be some support in observations of Pseudocalanus that part-time residence in deeper, cooler water may be metabolically advantageous for diel migrants when food is sufficiently concentrated.

    (c) The demographic hypothesis From the review of the effects of temperature on development

    rates and sizes of zooplankters, including Pseudocalanus, McLaren (1963) proposed that residence of developing females by day in deeper, cooler waters would increase adult size, and therefore fecundity, over non-migrant individuals in warmer surface waters.

    There was little difficulty in demonstrating an advantage for animals where life cycles were set by seasonality. For example, female Pseudocabnus in the surface waters of the Norwegian Sea would become larger and ultimately have large clutches if they migrated daily to cooler waters, before descending as C IV-C V to overwinter in the cold depths (see p. 152). Since they would not mature untilthe following spring, the slight retardation of development caused by diel migration to cooler waters during summer would be inconsequential.


    However, the situation is different for populations that develop continuously. McLaren (1963) showed that increased clutch size in these continuously developing individuals would not compensate for the retarded maturity at low temperatures. In these, the potential rate of increase (i.e. assuming no mortality) of Pseudocalanus was positively related to temperature. Therefore, he devised a model using von Bertalanffy 's well known growth equation to suggest a mechanism whereby increased " anabolism '' in warmer water and reduced " catabolism " in colder waters (i.e. the energy bonus of the previous hypothesis), could enhance the body size and therefore clutch size of females beyond that expected at the mean temperatures during development. In this way, McLaren deduced that there would be an important demographic advantage to migrants in potential rate of increase.

    Lock and McLaren (1970), in a laboratory test of part of McLaren's (1963) ideas (see p. 120), showed that no suchenhancement of female size occurred when animals were raised from C I11 to adulthood in an alter- nating temperature cycle, For this reason, among others, McLaren (1 974) revised the demographic hypothesis as it applied to Pseudocalanus in particular. First of all, he noted that his earlier arguments were based on false premises : the selective advantage (and evolutionary fixation) of a trait depends, not on the potential rate of increase (i.e. no mortality) of its bearers, but on the realized rates of increase in the face of natural mortality. His subsequent model of the demographic advantages of die1 vertical migration (McLaren, 1974) does away with the necessity for incorporating theoretical metabolic effects. The essence of his model can be described, with references to data and observations in this review, as follows.

    1. Young animals gain little size advantage from living in cool waters (p. 120, Fig. 27), so that development (McLaren assumed up to C I11 for calculations) in warm surface waters would have little effect on ultimate body size but would accelerate maturity.

    2. Older stages gain a size advantage at low temperatures (Table XXII, Fig. 27) which can be translated into increased clutch size (Fig. 19A), potentially sustained for ten successive clutches (p. 93). He therefore assumed that migration occurred between the beginning of C I11 and adulthood, to give this advantage in clutch size.

    3. He then assumed that there were two classes, migrant and non- migrant, of animals between C I11 and adulthood.

    4. He assumed that both non-migrants living near the warmer surface or migrants spending part of the time in deeper, cooler water were food-satiated and developed at maximal, temperature-dependent


    rates (as in Fig. 25), and that adult females produced eggs at maximal, temperature-dependent rates (as in Fig. 21).

    5. He assumed that the non-migrant populations living constantly near the surface were kept in equilibrium, with no increase or decrease of numbers of any stage over one or more generations.

    6 . Under these assumptions, when the same constant mortality rates were applied to all stages, both migrant and non-migrant classes, the hypothetical migrant class decreased relative to the numerically constant non-migrant one. That is, the increased clutch size of migrants failed to compensate for the added mortality resulting from delayed maturity.

    7. With the further assumption that the mortality rate in early life (hatching to beginning of C 111) was greater than that during later life (C I11 to adults and their carried eggs), he was able to show that the hypothetical migrant population could increase relative to the non- migrant one. That is, when mortality rates were relatively small among older animals, the advantage gained through increased clutch size by migrating for part of the day into colder waters was greater than the disadvantage from mortality prior to the delayed maturity.

    The advantage for the migrant over the non-migrant was greater, for a given temperature decrement experienced by the migrants, when surface waters were cooler; e.g. the advantage for a 5C decrement would be greater if the difference was between 5 and 10C than between 10 and 15C.

    McLaren (1974) finally indicated that details and some of the assumptions of his model could be relaxed, and concluded that whatever other values it has, vertical migration in thermally stratified waters may offer important demographic advantages to migrants whose fecundity is increased by development in low temperatures. We can examine this conclusion against observations of Pseudocalanus. Clearly it must be understood as applying only to females.

    The fact that young stages of Pseudocalanus in general are less migratory or nonmigratory and often live near the warm surface may indicate that rapid development is advantageous to these more vulner- able stages. The fact that migration may begin noticeably around C I1 or C I11 (e.g. Fig. 36) is suggestive, since this is when temperature begins to affect size (p. 120, Fig. 27). The fact that adult females (which can gain no further increase in clutch size) may, at times, give up migrations when copepodids continue (e.g., May in Fig. 38) or fail t o enter warmer waters at night when older copepodids do so (e.g., p. 167), suggests that at these times a demographic advantage obtains even when an energy bonus (of. previous hypothesis ; possibly useful to full grown migrating females) is not available or useful. Observations


    that migration may be most coherent and vigoroas early in the season (May in Figs 37, 38) may be related to the greater demographic advantages deduced by McLaren (1974) to occur when surface waters are relatively cool. Finally, the observations from Bedford Basin that female copepodids may spend more time in cooler depths than do males (p. 171) suggests that females may be seeking a further advantage (i.e. ultimate clutch size) that males cannot use.

    D. Retrospects and prospects Although one of us (McLaren, 1963, 1974) has promoted particular

    explanations for the adaptive value of vertical migration by Pseudo- calanus, our survey of the literature persuades us that no single explanation is likely to apply exclusively. Nevertheless, we stress the profound effect that temperature has on development and growth of Pseudocalanus and also the clear responses of the copepods to seasonal and vertical differences in temperature. We conclude that temperature must play an important role in the consequences of vertical migration, whatever its primary value to the animal.

    Unfortunately, the observational evidence on vertical migration of Pseudocalanus, and indeed of most zooplankters that have been studied, is deficient. Collections have been made over 24 h periods from populations that were clearly changing with the flow of water masses. Horizontal samples, even when quite closely spaced, may have missed concentrations a t some depths and times. Important variables (some- times temperature, sometimes feeding status, etc.) have been ignored in most studies. Stages and sexes have been grouped for analysis or illustration.

    We suggest that a carefully planned seasonal study of vertical distributions of Pseudocalanus would be amply rewarding. This should preferably be done in a stable, landlocked setting at temperate latitudes, using techniques to sample the entire water column in narrow strata (e.g. a pump or comparably continuous collector). At least temperature, food supply and predators should be monitored. A very thorough accounting of all stages should be made-all stages and sexes measured, fat contents and gut contents noted, etc. In short, we need the sort of laborious classical work that seldom attracts the current generation of marine biologists.

    XIII. PRODUCTION A. General methods

    By production of Pseudocalanus we mean the total amount of organic matter converted by a population from its food organisms and


    made available for other organisms as food. This is expressed per unit of time under a surface area or in a volume of water. Production occurs, however, whether other organisms use it or not ; a population of Pseudocalanus might, for example, die of salinity shock and decay chemically, yet still have produced organic matter. Thus the concept of production, as currently understood, differs from " yield ", such as might be obtained by man from a fish population. Production by immature stages of Pseudocalanus is obviously a result of growth of somatic tissues. Since adults do not grow in body size (although females may increase their store of oil), all their production must be gonadal. This may be unimportant in males, but clearly production of eggs by females must be included with somatic production by younger stages for a complete estimate of production by Pseudocalanus.

    Methods for estimating production of copepods are becoming fairly well established. Those that have been applied to Pseudocalanus are of three basic sorts, which are described at length, for example, in Winberg (1971).

    1. If life cycles are more or less synchronous (as with annual cycles at high latitudes) it is possible to follow a cohort (a brood or a genera- tion of Pseudocalanus, see p. 135) as its individuals grow in body size and diminish in numbers. The average numbers of individuals present during a time interval (the shorter the better) is multiplied by the average weight of organic matter by which each individual increases during the interval to give the production of somatic matter during the interval. To this must be added the weight of eggs produced during the interval by the non-growing adults. Sometimes " elimination ') (i.e. yield to predators or death and decay) is estimated from the numbers of individuals lost from the population during the time interval and the mean weight of each such individuals. Over the entire life of a cohort, somatic production should be the same as total elimination (except for small errors of integration). However, over a shorter portion of the cohort's life, elimination does not equal production. Furthermore, since increases in mean body size of a cohort can be estimated from sequential samples even when estimates of population decreases are inaccurate, it is generally better to estimate somatic production by multiplying mean number times the increase in weight during an interval. In general, this " cohort method ') of estimating somatic production is widely accepted, but rarely applicable. Sometimes, as we shall see, it has been applied very crudely to Pseudocalanw, with nevertheless useful results.

    2. If life cycles of Pseudocalanus are overlapping and recruitment of young is continuous, so that it is not possible to distinguish cohorts of


    individuals and follow their growth during the season, then the cohort method cannot be used to estimate somatic production. Instead we must use some indirect measure of the rate of growth of each develop- mental stage in the population, together with rate of egg production, applied with faith or evidence to the natural situation. For Pseudo- calanus, growth rates used in production estimates have been based on durations of stages in conditions of excess food in the laboratory. We have seen how durations of stages in these conditions together with weight increments between stages can be used to estimate growth rates as percentages of body weights per time unit (p. 131). Such percentages can be used as production/biomass coefficients (or P/B ratios) which, when multiplied by the biomass (i.e. sum of body weights) of a particular nauplius or copepodid stage, give somatic production per time unit. Rate of egg production can also be expressed as a percentage of weight of a female per time unit (p. 131), thus giving an estimate of the P/B ratio for the biomass of females in nature.

    Soviet and eastern European investigators, using various groupings of stages and approximations of body sizes and temperature effects (as described in Winberg, 1971), have been particularly vigorous in estimat- ing production of Pseudocalanus and other copepods from P/B ratios based on laboratory estimates of growth rates and egg production. Unfortunately, their detailed assumptions and methods are rarely explicitly stated in their published papers.

    Some authors have attempted to estimate production of Pseudo- calanus using durations of stages or even whole generations to calculate turnover times I . Although in principle this approach can give the same results as achieved by estimating growth rates and P/B ratios, i t can lead to conceptual problems, as discussed in Winberg (1971).

    3. Production by Pseudocalanus has been estimated by a number of methods, including the so-called physiological method (Winberg, 1971), that involve use in one guise or another of the balance equation of growth (see p. 132). In essence, the rates of ingestion, assimilation, respiration and sometimes excretion are estimated experimentally (or often from general metabolic equations) to give estimates of production of organic matter by individuals (whether this appears as growth or eggs) by difference. These estimates can be used directly in P/B ratios. As we have stressed earlier (p. 133), any use of the balance equation is tenuous at best. However, to the extent that the components of the balance equation can be estimated from experiments on populations in the field, assumptions that laboratory growth rates apply in nature might be avoided.

    In the following section we will describe all the attempts known to us


    to estimate the production of Pseudocalunus in nature. We shall pay particular attention to the methods that have been used, with reference to the general approaches that we have described above and to the observations on growth of Pseudocalanus that we have reviewed else- where.

    B. Production estimates 1. Oguc Lake, Bafin Island

    The only attempts to estimate production rates of Pseudoculunw using the cohort method appear to be those of McLaren (1969). He used estimates of dry weights and carbon contents as described in page 125. In Ogac Lake, as we have already seen (p. 138, Fig. 28B), the individual cohorts (broods in this case) could be traced with great assurance, showing decrease in abundance and increase in weights of individuals through the season. Weights of clutches that gave rise to each brood could also be estimated (p. 128). Although cohorts could almost always be readily separated, there were a few small problems in interpretation. For example, occasional greater mortality of older individuals within a brood gave negative production estimates that were taken as zero, not negative. Although there may be small errors in McLarens estimates of production, the cohort method involves no ussumptions about rates of growth, so that his overall estimates are probably quite accurate.

    Overall production in carbon (including 10-20 mg/m2 during the winter period, that could not be estimated exactly) was about 400, 500 and 350 mg C/m2 in the outer, middle and inner basins of Ogac Lake in 1957. In 1962, about 430 mg/m2 was produced in the middle basin, between 8 June and 27 August. In an experiment in 1962 with a fertilized polyethylene column in the middle basin, production was about 710 mgC/m2, or about 1.7 times as high as in the lake. (McLaren, 1969, p. 1509, gives this as 1.9 in error.) Production in 1957 had virtually ceased by September, and the production by overwintered copepodids at the beginning of the seasons only contributed an esti- mated 1-13% of production in the 1957 and 1962 seasons. Eggs were a large factor (see p. 96), supplying between 26 and 45% of overall production in the various basins and during the two years. Clearly any estimates that ignore such production of eggs by adult females will be in error. The growth of the various summer cohorts made up the remain- ing production. Because animals became bigger as the season pro- gressed, production was generally sustained through the summer, even though growth was slow and populations greatly reduced by mortality.


    2. BlackSea Soviet investigators have estimated production rates of a number of

    Black Sea copepods from body weights and durations of stages estab- lished in laboratory studies. Greze et al. (1968) have carried out such calculation for Pseudocalanus in the waters off Sevastopol during at least some of the four seasons for each year from 1960 to 1966. The biomasses of Pseudocalanus tabulated by them varied up to %fold seasonally within years and up to 7-fold between years within the same season. However, their tabulated P/B ratios varied much less: the largest is given as 0.203 for autumn 1960, and the smallest as 0.104 for winter 1965 (from their Table 3, wrongly labelled as " biomasses '' in the English edition). The exact methods of calculation used for these estimates are not described. However, reference is made to standard tables of wet weight of each developmental stage and to the work of Sazhina (1968) which, as we have noted (p. lll), gives acceptable estimates of development times for nauplii and copepodids at 8-10C. We are not told how egg production might have been incorporated, although estimates of the size and frequency of clutches are also given by Sazhina (1968). The daily P/B ratio were probably calculated as a daily percentage of growth of mean body weights of individuals grouped as nauplii and copepodids in the manner outlined in Winberg (1971). The ratios are said to have been corrected for seasonal differences in temperature, possibly with '' Krogh's normal curve ", commonly used in Soviet work (see Winberg, 1971).

    The overall mean estimates of daily P/B for each season in Black Sea Pseudocalanus differ little from one another : 0.143 for January to March at 7~8C; 0.173 for 1 April to 20 June a t 12.3"C; 0.159 for 20 June to 1 October at 21.4"C (temperature probably too high for deep living Pseudocalanus at this season-see p. 166) ; 0.174 or October to December at 14.1"C. (Greze, 1973, gives seasonal estimates based on the same data that differ slightly for reasons that we cannot determine.) These P/B ratios in turn differ little from the estimates of growth rate in dry weight per day calculated for older Black Sea animals (see p. 130) of l6-18% per day at temperatures of 8 to 15C. Thus, we believe that the daily P/B ratios in Greze et al. (1968) are in keeping with what we have learned about Pseudocalanus in our review.

    Conover (1974), assuming carbon to be 5% of wet weight:and a 40 m water-column, rendered the estimates of Greze et al. (1968) for Pseudo- calanus as 2.57 mg C/m2/day, or 939 mg C/m2/yr. An estimate for the " neritic zone " of the Black Sea off Sevastopol of 0.32 mg dry wt/mS/ day is given by Greze (1970). Assuming this to be 50% carbon and in


    40 m water column gives rates about twice as high as those estimated by Conover (1974). Conovers estimate is in turn twice that for Ogac Lake (above). However, Pseudocalanus is one of only two common copepods in Ogac Lake, whereas several other species in the Black Sea contribute to an overall annual production of copepods in the upper waters (using Conovers conversions for Greze et al., 1968) of some 3,360 mgC/m2/yr, some 4-5 times that of Ogac Lake (about 750 mgC/m2/yr, from McLaren, 1969).

    Porumb (1972) has estimated production of Pseudocalanus in the upper 50 m of the coastal waters (out to 50 nautical miles offshore) off Romania. Again, she does not detail methods, but refers to those used by Greze et al. (1968) and the references therein. She tabulates mean standing crops, P/B coefficients, the production by months, seasons and the year for the period July 1970 to June 1971. From her annual P/B coefficients it can be inferred that the daily P/B ratio was about 0.089 (32.796/365), rather lower than those estimated by Greze et al. (1968). Assuming with Conover (1974) that carbon is 5% of wet weight, and that Porumbs estimates of production apply to the upper 50 m, a value of production of 313 mgC/m2/yr can be calculated for Pseudocalanus. This is rather lower than that given above by Greze et al. (1968) for the waters off Sevastopol.

    Because of the reasonably close resemblance of the P/B ratios used in these Black Sea studies to growth rates of Pseudocalanus that we have calculated for other localities (see above), the production estimates may be reasonable. However, i t must be stressed that they are only acceptable if the Black Sea populations are at times developing at temperature-dependent rates, with no food shortages or resting phases. This may be plausible for the Black Sea region, but we have seen no published evidence to support the assumptions. In fact, in the work of Sazhina (1971) we are informed that the period of (abundant?) occurrence of Black Sea Pseudocu lun~ is 180 days from October to March.

    3. Sea of Japan Shushkina et al. (1974) have estimated production of Pseudocalanwr

    C 111-IV from an experiment with radiocarbon tagging of food algae in a mixed population of herbivorous and carnivorous zooplankton in large, unconcentrated samples from the northwestern Sea of Japan. From an elaborate model of the food web or this group of zooplanktonic species and the distributions of radioactivity among them following the experiment they deduce (by computer solution) a daily P/B ratio of 0.18 1 for C 111-IV Pseudocalanus.


    It is not possible to discover all details of their methods and calcu- lations, but this result compares quite well with estimates based on the assumption that copepods grow at maximal, temperature-dependent rates (see Black Sea and other estimates). This comparison is not made by Shushkina et al. (1974). Rather, they compare their results with those from the " physiological method " as outlined in Winberg (1971), assuming growth efficiencies of 0-4 and 0.3, and deriving estimates of daily P/B ratios of 0.23 and 0.36 respectively. As pointed out earlier, this method is unlikely to be very accurate.

    Andreeva (1 97Gb) has evidently estimated production of Pseudo- calanus in the northern Sea of Japan using durations of stages in the laboratory (but see p. 111) and body weights. In her preliminary account, she merely notes that P/B coefficients are similar to those for the Black Sea.

    4. North Xea There are two recent, independent estimates of production for

    Pseudocalanus from the North Sea. Although both are based on the assumption that there is more-or-less continuous development of generations in the areas studied, the approaches and assumptions used are quite different.

    Evans (1977) has used a statistical means of separating successive generations of adult female Pseudocalanus in samples from Northumber- land coastal waters. We have already indicated (p. 147) that this approach may not have distinguished generations during summer when temperatures were high and changing slowly. However, Evans uses this method to indicate the turnover times of adult females during the period between spring 1971 and spring 1972. In order to estimate production, Evans used weights of copepodids and adults as calculated with Robertson's (1968) weight-length equation. Although this equation is inaccurate outside rather narrow length limits (p. 127)) errors from this source are probably not too serious. Weights of nauplii were estimated by assuming that the same growth increments apply to them as to copepodids, with due consideration of shape differences between nauplii and copepodids. Two estimates of production are made by Evans. The fist simply sums the weights of adult females (means of samples) considered to represent each generation. The weights for each generation are then summed for the entire sampling period. As Evans points out, this estimate of production will be lower than overall pro- duction. The second method assumes that the populations are elimina- ted entirely between each designated generation and a '' more probable production figure is obtained by summing the standing stock of


    juveniles as well as adults . Although Evans notes that the possibility of extra generations (the adult females not statistically separated) means that his production estimates would be low, his second method will certainly give underestimates for other reasons as well. Essentially it is an approximate turnover time method, in which biomass is divided by the time (generation time) in which it is replaced. It will give a somewhat low approximation of the production to date of a particular generation from time of its origin (with a very low biomass taken by Evans as zero), to the time of sampling (when all biomass is counted as production). Also, it fails to account for production subse- quent to sampling and prior to the replacement of the generation. It also does not include egg production.

    Estimates by Evans using his second method indicate that Pseudo- calanus had the highest production of five copepod species off the Northumberland coast, about 47.9 mg dry wt/m3/yr out of 143-4 mg for the five species combined. Production of Pseudocalanus in the 50 m water column sampled by Evans was thus about 1 197 mg C/m2/yr (assuming carbon is 50% of dry wt, see p. 126). This (together with an estimate for all five copepods of 3 585 mg C/m2/yr) is similar to estimates or the Black Sea, but is probably substantially too low if the number of sources of error are taken into account.

    Recently Thompson (1976) has estimated the abundance of various stages of Pseudocalanus during a series of sampling periods between 12 December 1967 and 3 June 1968 over a wide area of the southern North Sea. She makes use of her extensive laboratory data (see p. 108, Fig. 25B) to convert numbers in each stage to production of num.bers using the relationship :

    No./m2 of stage during sampling period ____ = No. produced/m2/day.

    stage duration in days

    This, then, is a refined turnover time method in which each stage was treated separately. Her estimates of stage dura,tions as functions of temperature are based on regressions that give slightly different results from those in Fig. 25B.

    To convert production of numbers to production of biomass, Thompson used lengths at experimental temperatures and a formula linking wet body weight of copepodids and adults of copepods to total body length from Kamshilov (1951). In this way, she estimated that an average of some 280 >< 108 mg wet weightlday of copepodid and adult Pseudocalanus were produced over the study area in the southern North Sea during the winter-spring sampling period. From her estimate of the area sampled (30640 km2) this is about 1 mg wet wt/m2/day.


    Since only about 5% of this would be carbon (see p. 183), the implied production rates seem much lower than those for other localities.

    Although Thompson's actual measurements do not include egg production and probably contain small weight errors, they represent an admirable attempt to combine production estimates based on laboratory growth data with a sampling programme on a sufficiently large scale to be meaningful for a region.

    5 . Baltic Sea Production of Pseudocalanus in the Gdansk Deep area of the Baltic

    was briefly reported in a symposium abstract by Ciszewski and Witek (1975). By methods that are not detailed, they estimate that annual production of Pseudocabnus amounted to 137 g wet wt/m2/yr, about 5% of which would be carbon (see p. 183).

    This estimate is higher than any we have from other regions. The V/B ratio reported by them is 10-3, which seems similar to those from elsewhere, if 0.103 on a daily basis is meant.

    6. Norwegian Sea Pavshtiks and Timokhina (1972) summarizing earlier work by

    Timokhina, attempt to estimate the production of Pseudocalanus and other major zooplankton species for the entire area of the Norwegian Sea. To do so, they depended on samples taken from the upper 500 m from two east-west and one north-south section during 1959-63 and 1968-69. They use the method of Boysen-Jensen (as described in modern terms in Winberg, 1971), which is essentially a simplified version of the cohort method for populations with an annual life cycle. The population loss during a year is estimated from samples a t the beginning and end of the annual cycle, and this is multiplied by the mean biomass per individual between the beginning and end of the cycle. To this is added the biomass not yet dead at the end of the cycle. Pavshtiks and Timokhina, however, gave no details on the ways in which they evaluated numbers or weights.

    Estimates for the Norwegian Sea as a whole, are given in a table as millions of tons. For Pseudocalanus, these estimates (wet wt?) ranged as low as 1.57 x lo6 tons in 1961 and as high as 5.28 x 106 tons in 1962. Pavshtiks and Timokhina point out that the method of evaluation gives minimal estimates, and also that the catching efficiency of their plankton nets was unknown. Nevertheless, we consider the attempt to be of interest in demonstrating that approximations can be made even from rather unpromising material.


    7. White Sea Fedorov et al. (1975) have estimated production of phytophagous

    copepods, including Pseudocalanus, in the White Sea from a 24 h experiment on 26-27 June 1970, and a 3-day experiment on 18-21 August 1971. During these time periods they made frequent measure- ments of biomass of phytoplankton and zooplankton species in the 75 m water column and made less frequent estimates of phytoplankton production rates. They followed the approaches of McAllister (1969) to calculate consumption of phytoplankton by zooplankton, using observed phytoplankton production and changes in biomasses of phyto- plankton. The rest of their analysis is based on the " balance equation " approach, with coefficients of assimilation and respiration assumed from the literature, evidently with no account of the (low?) prevailing temperatures. They conclude that production by phytophagous zooplankton (of which Pseudocalanus was 26% of the biomass) was 26 mg C/m2/day. The mean P/B ratio was about 0-17 ; the concordance of their ratio with estimates for Pseudocalanus from the Black Sea is of doubtful significance in view of the fact that some of the assumed rates used by Federov et al. are based on Black Sea studies.

    C. Retrospects and prospects

    Although the estimates of production rate in Ogac Lake by McLaren (1969) are probably the least disputable that we have reviewed, the environment of Ogac Lake is very special and the opportunity for using the cohort method is not available for most of the geographical range of Pseudocalanus. We believe that we have summarized enough information in this review so that production of Pseudocalanus in many localities (some with published data available for analysis) could be estimated with little or no further information, provided that development rate in the population over the period of interest is not limited by food. We have argued in several places in our review that this assumption is probably valid for a substantial part of the year in many temperate localities, and have demonstrated its validity for Loch Striven, Scotland (p. 145) and less completely for a number of other localities (see Section XI). However, the investigator wishing to validate the assumption for any given locality has been given a number of techniques (egg frequency counts, p. 98; oil sac sizes, p. 129; and especially intensive sampling and analyses of female sizes and perhaps relative number of specific copepodids, p. 143) that might be used. If it can be assumed or demonstrated that food is not limiting, then the


    following methods (including some approximations and short-cuts ) can be used to estimate the parameters of production. (1) We have shown (p. 11 1) that development rates of the various stages as functions of temperature differ little over various parts of the world, so that Fig. 25A or B might do as approximations. (2) We have shown that volume of a clutch of eggs is about the same function of female length in different regions, so that the potential rate of production of egg matter as a per cent of female body weight is a similar function of temperature everywhere (p. 131). (3) A general weight-length relation- ship for Pseudocalanus copepodids and adults (p. 127) allows weight estimates t o be made from length, if not made directly. (4) Unfortu- nately there are no direct estimates available of weights of nauplii. Evans (1977) estimated that growth factors (length multiples between moults) of 1.17-1.28 (mean 1.22, implying a weight increase of about 1-8 times) apply for Pseudocalanus. Since nauplii contribute very little to overall production, McLarens (1969) assumption that they double weight between moults, might do. From weights and stage durations, growth rates of stages can readily be calculated, and applied as P/B ratios to counts or biomasses of animals in samples.

    It should also be possible to construct purely theoretical models of Pseudocalanus production for various regions, since size-temperature relationships can be added to the above information. Although these are local in application (see, e.g. Fig. 26) they should be readily estab- lished from a small number of points from experimental or field data.

    From estimates of growth rates that we have given for various stages and temperatures, approximations might be made for P/B ratios applying to entire samples. For example, we suggested (p. 130) that older copepodids from the North Sea might grow a t about 17% of body wt/day irrespective of temperature. Younger copepodids and nauplii might be more affected by temperature, but generally contribute little to biomass in nature, so that an overall rate of 20% might do at North Sea temperatures. Production by adult females can be reckoned in terms of egg matter, and is more temperature dependent. Overall, a P/B ratio of 0.20 might suffice for the North Sea for some purposes.

    None of the attempts to estimate production of Pseudocalanus that we have reviewed take into account all the kinds of information alluded to above. However, there remains a more serious problem for the future of such studies. Only Evans (1977) has attempted (with shortcomings that we have noted) to discriminate generations in the field objectively. Some of the other estimates depend on the assumption that food is in excess, and temperature in control. However, we have also described the way in which overwintering, resting stages begin to accumulate


    in the population in some regions while other members of the population continue to produce a t maximal rates (p. 144). In our opinion, the most important work remaining to be done on the production biology of Pseudocalanus (and perhaps other copepods as well) is in the establish- ment of the growth status of individual stages in samples from nature. Does stored fat in young stages and in adults denote full production potential? Does fat above certain levels in C IV denote resting ? Are there other morphological criteria of growth status?

    Of course, determining production of Pseudocalanus should not be viewed as an end in itself. We know very little about the impact this production has in nature, and what we do know is the subject of Section XV.


    A. Dinoflagellates

    1. Blastodinium hyalinum Chatton, 191 1

    (a) Taxonomy Apstein (1911) described and recorded this genus as Parasit 1

    in a number of copepods including Pseudocalanus. Chatton (191 1) made observations on Apsteins work and writes Dans le MBmoire que jachhve, en ce moment, sur les Phidiniens parasites, je lui ai rhservh le nom de B. hyalinum, n. sp.. Chatton (1911) does not give a descrip- tion of this parasite in that paper although he does say it is closely related to B. contortum Chatton. I n his large monograph Chatton (1920) refers to this parasite as B. contortum hyalinum which differs from B. contortum in lacking torsion and pigmentation ; when removed from the host gut and left in Bea water this variety dies earlier than B. contortum since it is less resistant.

    Sewell (1951) from extensive study concluded that Chatton (1920) confused more than one species under the name B. contortum hyalinum. Sewell refers to the parasite discussed here as B. hyalinum Chatton, and confines this species to the form found in the North Sea, which was described but not named by Apstein (1911) and to the forms Chatton (1920) recorded from the Mediterranean. We adopt here the view of Sewell and refer to this parasite as B. hyalinum Chatton. In addition Sewell (1951) examined a number of specimens of Pseudocalanus collected from the North Sea and confirmed that B. hyalinum infected Pseudocalanw .


    (b) Life history The parasite lies within the alimentary canal of Pseudocalanus and

    initially consists of a single cell, the trophocyte or trophozoite (Fig. 39A). Transverse or oblique division gives two daughter cells, the anterior (i.e. nearly always at the anterior end of the host) becoming

    Parasite / Gut A

    Secondary trophozoite First layer of

    sporocytes I / 0

    Tertiary Secondary layer trophozoite of sporocytes F m t loyer o f

    C I I sporocytes I

    Fro. 39. The dinoflagellate parasit,e Blastodinium hyalinum. A, parasite in the gut of a calanoid copepod. B, monoblastic stage from Pseudoculun~. C, diploblastic stage. D, polyblastic stage. (A after Chatton. 1920; B-D after Sewell, 1961.)


    a secondary trophocyte and the posterior a gonocyte. The gonocyte forms a large number of sporocytes by repeated division (Fig. 39B).

    The monoblastic stage in the life cycle occurs when the secondary trophocyte is surrounded by one layer of sporocytes on all sides, apart from a distinct gap which may be present and is called by Chatton (1920) the hilum (Fig. 39D). The secondary trophocyte divides into an anterior tertiary trophocyte and a posterior gonocyte, which in turn undergoes repeated divisions to give a second layer of sporocytes lying within the first layer ; this is the diploblastic stage (Fig. 39C). The poly- blastic stage is formed when the trophocyte continues to divide, ultimately into a number of layers of sporocytes (Fig. 39D).

    In the genus Blastodinium the trophocyte may not divide into a trophocyte and a gonocyte, but into two trophocytes (i.e. by schizo- gony), and each of these trophocytes may subsequently undergo division into more trophocytes and gonocytes (Sewell, 1951). The end result is a single primary layer of sporocytes enclosing two separate layers of secondary sporocytes, each enclosing a trophocyte. Usually the release of sporocytes from the host sets the two daughter tropho- cytes free within the alimentary canal to develop into separate para- sites. Schizogony enables more than one parasite to infect a host and hence gives rise to a larger number of sporocytes than would have been possible without schizogony. Chatton (1920) and Sewell (1951) agree that two or more individual parasites in a host have likely arisen by schizogony. Sewell does not state expIicitly that schizogony occurs in B. hyalinum inside Pseudocalanus but does give a table (his p. 329) in which size measurements of parasites are given for four cases of double infections and one triple infection of B. hyalinurn from the North Sea, from which it may be inferred that B. hyalinum can undergo schizogony in Pseudocalanus.

    The rupture of the cuticle surrounding the parasite sets the sporo- cytes free into the alimentary canal of the host. The sporocytes are small immobile cells with two nuclei (Fig. 40A). Sometime after expul- sion from the anus and after an unknown number of divisions they form dinospores (Fig. 40B), with 2-4 flagella attached in the region of the equatorial groove. Under unfavourable conditions the dinospores are able to encyst and host infection presumably takes place by ingestion of the dinospores or cysts (Fig. 40C) with the hosts food.

    (c) Eflect of infection on the host Chatton (1920) found that in host individuals parasitized with

    Blastodinium the gonad was immature and the genital ducts un- developed. He also noted that he had never seen a parasitized male.


    Cattley (1948) examined a number of Pseudocalanus from the North Sea, parasitized with 3. hyalinum, and found very distinct changes in the fifth pair of legs. He concluded that in the male the parasite is able to arrest the development of the male characters of the copepodid (externally, the fifth pair of legs), while in the final moult it causes the copepodid to undergo sex reversal and appear externally as a mature but sterile female ; he found spermatophores on three such individuals.

    Transverse groove

    / Transverse flogello Longitutlinal groove

    FIQ. 40. The sporocytes (A), dinospore (B), and (C), a cyst of Blastodinium hyaliizurn, a parasite of Pseudocalanus. (After Chatton, 1920.)

    Cattley believed that the parasite had no effect on the morphology of female hosts and that the C V moulted into a fully formed but sterile individual.

    Sewell (1951) examined a large number of individuals from several host species (not Pseudocalanus) infected with 3lastodinium and found both sexes infected with the parasite. In none of the infected males (usually C V, rarely adults) could Sewell detect any change of structure from the normal. In females, a late infection evidently only partly reduces the development of the ovary and oviduct whereas an early infection has more profound effects. The first two segments of the

    A.M.B.-15 6


    urosome may not fuse to form the genital segment, as occurs in a normal female (p. 34), but remain, separate as five segments, resembling the male condition. Even with fusion, the genital operculum may not develop, and there may develop a fifth pair of legs similar to that found in the male C V. Sewell (1951), therefore, was of the opinion that intersex individuals in copepods are modified females and not male individuals that have undergone partial or complete sex reversal as proposed by Cattley (1948) for Pseudocalanus. Sewell (1951) makes the further observation that those individuals in which a modified fifth pair of legs is present and which in all other characters appear to be females, but in which no parasite has been found, result from an early infection from which the individual has later recovered.

    (d) Occurrence Blastodinium hyalinum is widespread (see ranges in above account)

    in the most wide ranging study (with Continuous Plankton Recorder). Vane (1952) states that it occurred in 3.8-60% of individual Pseudo- calanus (mainly C V and adult females) in samples from the North Sea in 1948-49. It was most common in July-August, especially in the central part of the North Sea, minimal in December-March.

    2. Dissodinium pseudocalani Drebes, 1969 (a) Taxonomy

    Dissodinium pseudocalani is a parasitic dinoflagellate found by Drebes (1969). The reproduction of this species resembles that of D. lunula and so the parasite was provisionally put in this genus. D. pseudocalani has thus far only been observed as an ectoparasite on the eggs of Pseudocalanus.

    Drebes (1972) subsequently indicated that his Dissodinium pseudo- calani Drebes, 1969, is a synonym of Sporodinium pseudocalani Gbnnert, 1936 (see p. 196), and suggested that fwrther nomenclature changes will be made after he has concluded his revision of a few dinoflagellate genera. We accept the possibility that the two species discussed above are synonyms but we prefer here to give an account of the two forms separately, particularly since Sournia, et al. (1975) com- ment that the two parasitic species seem distinct.

    (b) f i f e history

    and an ectoparasitic phase on Pseudocalanus eggs. The life cycle includes a free drifting phase unattached to any host

    Mature primary cysts (Fig. 41A) usually drift unattached to the


    host. They are spherical or oval, between 150-250 pm, and contain green or orange protoplasm, which is the same colour as the hosts eggs. The protoplasm invaginates in one region (Fig. 41B) and the nucleus divides mitotically to form nuclei on the periphery of the

    FIG. 41. Diagrammatic representation of the life cycle of Diasodinium pseudocalani, a parasite of Pseudocalanus. A, primary cyst in plankton. B, multinucleate proto- plasm, invaginating. C, division into 16 cells. D, development into 16 secondary cysts. E, secondary cysts forming dinospores. F, liberated motile dinospores. G, infeotion of host egg. H, growth of mature trophont. I, the trophont still attached to egg membrane of host. (After Drebes, 1969.)


    protoplasm, which then divides to form, generally, 16 segments (Fig. 41C), but sometimes 8 or 32.

    Secondary cysts (Fig. 41D) are formed by the rounding off of the 16 segments formed in the primary cyst; these become oval and about 76 x 47 pm.


    Sporulation occurs when the secondary cysts divide to form 16 or 32 flagellated dinospores (Fig. 41E), which are colourless swarmers of the Gyrodinium type (Fig. 41F).

    Host infection occurs when a dinospore attaches itself to the surface of a host egg (Fig. 41G) and sucks out the contents. The trophont develops as an ectoparasite on the egg, then generally separates and continues its development in a primary cyst in the plankton (Fig, 41H, I). Later developmental stages were occasionally seen with the parasite still attached to the host egg membrane (Fig. 411).

    (c) Occurrence The parasite appears in the North Sea off Heligoland in the German

    Bight from late April until early June and is fairly common in the second half of May. The reason for this marked seasonality is not known.

    3. Sporodinium pseudocalani Gbnnert, 1936 This parasite was found as a free cyst in the plankton off Heligoland

    in April 1934. At this time Pseudocalanw was the most numerous zooplanktonic species and one parasitic cyst was found in a clutch of eggs of Pseudocalanus. Gbnnert (1936) was unable to elucidate the complete life cycle, but described the formation of sporoblasts (= primary cysts) which develop into sporocysts ( = secondary cysts) containing dinoflagellate-type nuclei. As Drebes (1972) observed, Gbnnert (1936) confused the membrane of the primary cyst with the egg wall of the host and therefore concluded that the dinoflagellate was endoparasitic, although he did not rule out completely the possibility of ectoparasi tism .

    This species is probably synonymous with Dissodinium pseudocalani Drebes, 1969, the life history of which has been described in detail above.

    4. Ellobiopsis chattoni Caullery, 1910 Ellobiopsis chattoni is an external parasite of pelagic copepods

    first described by Caullery (1 9 lo), who provisionally considered it to be a peridinian dinoflagellate, although no developmental stages or dino- spores were observed. Apstein (1911, " Parasit 19 ") recorded an exter- nal parasite of Pseudocalanus which was identified by Jepps (1937a) as Ellobiopsis. Specimens of Pseudocalanus with Ellobiopsis have been recorded subsequently from the Gulf of St. Lawrence (Pinhey, 1927), Loch Striven (Marshall, 1949), the southern Norwegian Sea (Hansen, 1960) and off Ireland (Fives, 1969). Wing (1975) found a low level of


    infection of Pseudocalanw by Ellobiopsis chattoni in southeastern Alaska. Throughout the year only 1-6 Paeudomlanus were found to be infected each month from many thousands of potential hosts that were examined. Wing found no distinct seasonal trend of infection.

    The systematic position of this parasite has been disputed. Jepps (1937b) considered that the available evidence suggested a fungus relationship, but a t present the whole group is considered as belonging to the dinoflagellates by Loeblich (1976), and this is the view adopted here.

    An account of Ellobiopsis chattoni on Calanus finmarchicus is given by Jepps (1937b). It is assumed that spores formed by sporulation are responsible for infection of new hosts, although this process has not been observed.

    B. Qregarines Apstein (1 91 1, " Parasit 3 ") recorded gregarines in Pseudocalanus,

    and Jepps (1937b) observed them in the gut of Calanw. These parasites have not been studied in detail in copepod hosts, but the young parasite (sporozoite) becomes typically intracellular as it grows. It then leaves the host cell and the mature trophozoites adhere externally to the digestive lining. The trophozoites fuse in pairs (syzygy, observed in Calanus by Jepps, 1937b) and ultimately produce young sporozoites.

    C. Trematodes Giesbrecht (1882) reported that Pseudocalanus was the most

    frequent host of a trematode, probably Hemiurw, that was also found free-living in Kiel Harbour. Entry into the host (later copepodids and adults) was between two thoracic segments or between cephalothorax and urosome, using the tapered posterior end for penetration. Other references to trematodes (probably H . appendiczclatus according to Thompson, 1976) in Pseudocalanzcs are Canu (1892), Apstein (1911), Wright (1907) and Marshall et al. (1934). Trematodes (or cestodes) were considered by Fives (1969) to be responsible for the red colouration often found in Pseudocalanus. Thompson (1976) concludes that these parasites do not have any detrimental effect on the copepod, merely acting as an intermediate host, the final hosts being fishes that feed on copepods.

    D. Nematodes Apstein (1 91 1, " Parasit 17 ") observed nematodes in Pseudocalanw,

    and Marshall and Orr (1955) reported them in Calanw as Contracaecum


    sp. The eggs of Contracaecum from the faeces of definitive hosts (birds or sea mammals) develop into larvae that may be eaten by copepods and subsequently by second intermediate hosts (Huizinga, 1966).

    The genus Thynnascaris parasitizes fish as adults and its larvae occur in fish and invertebrates. Popova and Valter (1965) and Valter (1968) have completed experimental studies on the intermediate hosts of Contracaecum aduncum (= Thynnascaris aduncum according to Norris and Overstreet, 1976) ; eight copepod species were subjected to experi- mental infection with larvae and Pseudocalanus was the second most infected copepod species (26% became infected). The larvae remained in the body cavity of the copepod where they increased in size (Popova and Valter, 1965).

    E. Crustaceans

    All epicaridean isopods parasitize crustaceans and feed on blood. They undergo a marked metamorphosis in their life cycle (see Kaestner,

    PIa. 42. Two mioronisoium larvae of an epicaridean isopod parasite, on Pseudocdanue. (From Sam, 1899.)

    1970). The young leave the mother as pelagic epicaridean larvae and survive for a period on stored yolk before attacking a pelagic copepod or other host and transforming into a parasitic microniscium. After several moults on the host, its appendages become reduced and it becomes a free-swimming cryptoniscium stage, which then seeks out a final crustacean host. Sars (1899) gives an account of two microniscia on a female Pseudocalanus a t two different stages of development (Pig. 42), and Marshall (1949) found a microniscium on a female Pseudo- CaZanus, but nothing is known about final hosts of these parasites.


    I!. Retrospects and prospects

    Our knowledge of the parasites of Pseudocalanus (as for marine parasites in general) is fragmentary, and advances will probably have to depend on the efforts of specialists working on the parasitic groups, rather than on the incidental findings of copepodologists. Although some of the parasites are fatal or sexually sterilizing to their hosts, their impact on Pseudocalanus populations is thought to be small (e.g. by Vane, 1952, and Wing, 1975). However, those parasites that use the abundant Pseudocalanus as intermediate hosts could have substantial impacts on less common final hosts.


    We have indicated near the beginning of our review (p. 17) that Pseudocalanus is one of the most widespread and abundant metazoans in the world. Given this status, it is certain to be of substantial import- ance in the lives of other organisms. Here we review briefly the role of Pseudocalanus as a consumer, as a source of nutrients and as food for others (especially larval fishes), and discuss the first hesitant attempts to include Pseudocalams in descriptive and predictive models of marine food webs.

    A. Effect on phytoplankton

    1. Peeding on phytoplankton The feeding of herbivorous copepods clearly removes phytoplankton

    from the water column, but evidently the impact of Pseudocalanus on its food species has not been fully assessed. Zagorodnyaya (1977) esti- mates the fraction of edible biomass of phytoplankton in the Black Sea removed by Pseudocalanus during two times of year. To do so she calculated daily rations of copepodids and adults, using the balance equation approach (see p. 132). She concludes that these animals removed about 18% of the standing crop daily (compared with 11 yo by Calanzis hegolandicus) in inshore waters in spring, and 8% (compared with 40% by C. helgolandicus) in offshore waters in winter. As these conclusions are local in implication, we feel that the following general account is useful.

    A population of Pseudocalanus growing or producing eggs a t about 15-20% of its biomass per day (pp. 130,131) might need a minimum of about four times this amount of food (p. 133), which it might obtain from food concentrations as low as 25 pgC/I. (p. 130). If we can imagine


    that such an unconcentrated phytoplankton biomass could, if ungrazed, double its quantity each day, then a population of 3 or 4 adult female Pseudocalanus per litre, each weighing about 10 pgC, could keep the plant population in check.

    However, we have shown that copepodids can consume up to 140% of their weight per day at phytoplankton concentrations of 200 pg C/1. (p. 67). Since growth rates do not increase with ration above at most 50 pgC/l. (p. 130, despite equivocal analyses from growth efficien- cies, p. 133), this seems to us to indicate that " superfluous feeding " by Pseudocalanus could occur at phytoplankton levels substantially below the 390 pgC/l. suggested by Beklemishev (1962) for copepods. Possibly, however, die1 feeding cycles (p. 72) and vertical migration (p. 165) reduce this " wastage " in nature.

    The faecal pellets produced by Pseudocalanus (whether with superfluous food or not) may carry material below the photic zone. The pellets produced by Pseudocalanus are of the order of 106 to 3 x 106 pm3 (from Corkett, 1966 ; Martens, 1972), and these might sink at up to 100 m/day (Fig. 1 in Smayda, 1969).

    2. flupply of nutrients Although Pseudocalanus removes organic matter from the water

    column, it also resupplies nutrients to the phytoplankton. We have concluded that rates of excretion of nutrients by Pseudocalanus are strongly dependent on food concentrations (p. 51).

    Evidently the only estimates of the possible contributions of excretion by Pseudocalanus to phytoplankton requirements come from two studies in Bras d'Or Lake, a landlocked arm of the Atlantic in Nova Scotia. Here Christiansen (1968), using rates of NH3 excretion described elsewhere (p. 44), estimated from population densities that Pseudocalanus supplied about two-thirds of the N excreted by the copepod community, but that this was only about 4.8 mg N/m2/day, which was about 4% of the daily phytoplankton requirements of about 118 mg N/m2/day.

    In the same environment, Hargrave and Geen (1968) calculated that the phytoplankton needed about 7.5 mg P/m2/day. From esti- mates of population densities and excretion rates of P (see p. 49), they suggested that about 15 mg P/m2/day could be supplied by copepods, sometimes predominantly Pseudocalanus. Although they note possible sources of error, they conclude that regeneration of P (unlike that of N, see above) by copepods like Pseudocalanus is important.


    B . Predators I . Fishes

    There are many records of the occurrence of Pseudocalanus in the diets of fishes, and we cannot refer to them all. Rather, we attempt to outline the possible importance of Pseudocalanus to numerically and commercially important fish species. Where possible we refer to recent, more general studies of diets in which Pseudocalanus figures. We also attempt to give geographical balance in our survey.

    Although Pseudocalanw occurs in diets of some postlarval fishes, it is much more important as a food for larval fishes. Most marine fishes have very high fecundities that are balanced by high mortalities. Most of this mortality occurs during the larval stage, as was first stressed by Hjort (1914). May (1974) restates I Hjorts critical period concept as a concept that maintains that the strength of a year-class is determined by the availability of planktonic food shortly after the larval yolk has been exhausted . May concludes that field and labora- tory evidence, although often circumstantial, indicate that starvation is indeed an important cause of larval mortality when yolk has been exhausted, as Hjort hypothesized.

    In order to signify the relative commercial importance of each species of fish considered here, we quote the most recent available fishery statistics (P.A.O., 1974) on the nominal catch for 1973.

    (a) Salmon Salmon as diadromous fishes breed in fresh water and their young

    may migrate to the sea at various stages of development. Among them, the pink (= humpback) salmon (Oncorhynchus gorbuscha) goes to sea as plankton-feeding fry. It produced a catch in the northeast Pacific of 34 x lo3 metric tons in 1973. Young pink salmon (36-104 mm) off southern Hokkaido have been shown to contain Pseudocalanus in their stomachs (Okada and Taniguchi, 1971). Parsons and LeBrasseur (1970) showed in the laboratory that young pink salmon 90 mm long fed best off Calanus plumchrw and less well off the smaller Pseudocalanus. In the Strait of Georgia, however, it appeared that pink salmon less than 30 mm long fed best on smaller copepoda, such as Pseudocalanus (LeBrasseur et at., 1969).

    The chum (= keta or dog) salmon (0. keta) is an important food fish in Japan and North America, with a catch of 126 x lo3 metric tons in 1973. Okada and Taniguchi (1971) found Pseudocalanus in the guts of juveniles, and LeBrasseur et al. (969) showed that such small copepods are an important food source.


    (b) Herring The Atlantic herring (Clupea harengus) yields one of the world's

    great fisheries, with a total catch in the Atlantic of some 1 956 x lo3 metric tons in 1973. Hardy's (1924) classical study in the North Sea showed that Pseudocalanus was numerically 86% of the food of herring between 12 and 42 mm.

    The importance for herring of food availability after the yolk sac has been absorbed has been investigated by Blaxter (1 963). He related the dimensions of food organisms to the maximum gape of the jaws, which is just sufficient to take an adult Pseudocalanus " end on "when larvae reach 12 mm. He found that Pseudocalanus were not generally taken until the larvae reached 12 mm, and that Calanzls was not taken until the larvae were 30 mm long. He concluded, however, that Calanus were rarely taken by postlarval fish, and then only when the copepods are in younger stages, but that Pseudocalanus is of major importance.

    Legare and Maclellan (1960) have carried out the most extensive study of herring feeding in relation to zooplankton in the western North Atlantic. They found that Pseudocalanus was the second most abundant copepod in the region of the mouth of the Bay of Fundy. It was third in incidence in stomachs from within Passamoquoddy Bay and, along with Calanus, even more common in stomachs from outside the bay, especially in fish longer than 200 mm.

    The Pacific herring (Clupea harengus pallmi) produced a catch of some 539 x lo3 metric tons in the North Pacific in 1973. Lowe (1936) investigated food in various sized herring from off southern British Columbia. For fish 9-12 mm long, the most important food items were small eggs and nauplii. Pseudocalanus was present in guts of all larvae longer than 13 mm.

    (c) Atlantic mackerel . The mackerel (Scomber scombrus) produced some 1 017 x lo3 metric

    tons in the Atlantic and 11 x lo3 metric tons in the Mediterranean and Black Seas in 1973.

    Bullen (1908) found that PseudocaZanus was common in stomachs of postlarval mackerel in the English Channel, especially in the month of May. Among " fishermen's signs " was one stating that mackerel are abundant in " yellow water )), which seldom appears before the last week in April. Bullen showed that phytoplankton was almost absent from " yellow water ", but that copepods were abundant, especially Calanus and Pseudocalanzls.


    (d) European pilchard The pilchard or sardine (Sardina pilchardus) makes up several

    important fisheries. I n 1973, Portugal took 101 x 103 out of a total of 177 x 103 metric tons from the northeastern North Atlantic, probably largely outside the range of Pseudocalanus. There is also an important fishery in the Mediterranean, of some 144 x lo3 metric tons in 1973.

    Although Lebour (1920) recorded Pseudocalanus among the food items of larval (9-25 mm) pilchard off Plymouth, the fish largely occurs south of the range of Pseudocalanus, except in the Black Sea, where the copepod may be an important food item (I. I. Porumb, 1969).

    (e) Sprat The sprat (Sprattus sprattus) is an important fishery for the U.S.S.R.

    and Denmark, which together landed over half of the 507 x lo3 metric tons taken in the northeastern North Atlantic in 1973. There is also a small fishery (9 x lo3 metric tons) in the Mediterranean and Black Seas.

    Nguyen et al. (1972) found that Pseudocalanus was important seasonally in samples of sprat from the Bornholm Deep in the Baltic, making up about 43% of food items in April and 59% in May. Miller (1969) found that Pseudocalanus also dominated the diet of fish taken in April and May off the Estonian coast, and that most feeding took place a t night.

    In the Black Sea, Porumb (1971) found that a reduction of Pseudo- calanus populations in April could be traced to its fate as a principal food of sprat, which is a migrant to Romanian coasts at this time of year.

    (f) Atlantic cod The cod (Gadus morhua = G . callarim) yields the greatest catch

    among demersal fishes whose larvae feed on zooplankton. It is import- ant both in the northeastern North AtIantic, where some 1 727 x lo3 metric tons were taken in 1973, and in the northwestern part, where some 808 x lo3 metric tons were caught.

    Wiborg (1948) investigated the food of larval cod in coastal waters of northern Norway during spring and summer of a number of years between 1930 and 1947. The larvae ranged from 3.1 to 13.0 mm long. When Pseudocalanm was abundant in the plankton in May 1933, copepodids occurred in larvae 4-7-6-5 mm long. Nauplii were found in small larvae, many with a yolk sac, in 1939. Pseudocalanus was not found in larvae taken in 1930 and 1947, evidently because the copepod


    was scarce at the times of sampling. As expected, copepods are not important in the diet of postlarval, " 0-group " cod, which feed almost exclusively on euphausiids, although Pseudocalanus was recorded in some stomachs (Wiborg, 1949).

    Marak (1960) investigated feeding by larval cod in the Gulf of Maine and over Georges Bank. He found " Pseudocalanus-type " (i.e. including Paracalanus) remains in six larvae 9-16 mm long.

    (g) Polar cod The small polar cod (Boreogadus saida) forms a significant fishery in

    the northeastern region of the North Atlantic, some 82 x lo3 metric tons having been taken in 1973. Diet of its larvae has been investigated by Ponomarenko (1967), who found that copepods were important to larvae between 4.6 and 39 mm long, and that Pseudocalanus occurred in 57% of specimens in the size range 19.1-28.7 mm.

    Pseudocalanus nauplii have been used as food for polar cod larvae reared in the laboratory (Aronovich et al., 1975).

    (h) Haddock The haddock (Melanogrammus aeglefinus) offers a huge catch of some

    593 x 103 metric tons in the northeastern North Atlantic, compared with only 26 x 103 metric tons in the northwestern part.

    Marak (1960) found among larvae between 4 and 46 mm long, " Pseudocdanus-type '' copepods (see under cod, above) mainly in larvae between 13 and 23 mm long.

    Ogilvie (1938) found Pseudocalanus commonly in larvae 3-5-31 mm long from Scottish waters. She considered the largest individuals to be postlarval. Pseudocalanus eggs and younger stages were found in smaller larvae, and adult females were common in those more than 12 mm long.

    (i) Whiting The whiting (Merlangius merlangus) formed an important fishery

    of about 207 x lo3 metric tons in the northeastern North Atlantic and a smaller one of about 1 x lo3 metric tons in the Mediterranean and Black Seas during 1973.

    Lebour (1920) found that Pseudocalanus was a favoured food item of larval whiting up to about 9 mm long during spring and summer off Plymouth. Although the larvae take other copepods, Lebour con- cluded that they select Pseudocalanus in preference to other like-sized forms, such as Temora.


    (j ) European plaice The plaice (Pleuronectes platessa) yielded 164 x lo3 metric tons

    in the northeastern North Atlantic in 1973. Scott (1922) examined over 600 larvae 13-87 mm long from off the

    coasts of Wales and the Isle of Man, and found that 22% of them contained Pseudocalanus.

    (k) European hake Of the several commercial species of hake, the European hake

    (Merluccius merluccius) gave an important catch in the northeastern North Atlantic of some 110 x lo3 metric tons in 1973.

    Lebour (1920) found a Pseudocalunus in a single larval hake (5-5 mm long) in a sample of 12, but felt able to conclude that " it seems likely that young Hake, like the Gadus species, begins by taking Pseudo- calanus, Calanus afterwards being frequently taken ".

    (1) Sandeels Sandeels (sandlances or sand launces) of several species (Ammodgtes

    spp.) are important fisheries, especially for Denmark, which landed 283 x lo3 of the 307 x 10% metric tons taken in 1973 in the northeastern North Atlantic.

    Sandeels occur in large shoals in shallow waters and are caught by fine-mesh trawls, so that in this sense they can be classed as demersal fishes. They are important as food for other larger demersal fishes.

    Lebour (1919b) found Pseudoculunus in the guts of fish 19-21 mm long in a sample of 109 A . tobianus ranging from 3 to 21 mm long. She also found (Lebour, 1918, 1920) Pseudocalanus frequently in the guts of Hyperoplus lanceolatus ( = A . lanceolatus) 1 P 2 5 mm in length.

    The Pacific sandlance (A. personatus) forms an important fishery for Japan, which took 194 x 103 metric tons from the northwestern North Pacific in 1973. LeBrasseur et al. (1969) examined gut contents of larvae (< 30 mm) and young (> 30 mm) of this fish from the Strait of Georgia, British Columbia. At the time of sampling, Pseudocalanus and two larger Calanus spp. were available as food. Fish of the size range 20-40 mm had 48% of their stomachs filled with zooplankton in the 0.5-1.0 mm size range, whereas large (> 40 mm) fish had 85% of their stomachs filled with zooplankton in the 1-1-1.5 mm range. Species of zooplankton were not identified, but it can be inferred from these sizes that Pseudocalanus and young stages of Calanus must have been of prime importance.


    (m) Other denzersal species Pseudocalanus has been identified in the gut contents of a number of

    other demersal species by Lebour (1918, 1919a, 1919b, 1920). Among these, the ling (Molva molva), common dab (Limanda Eimanda) and turbot (Psetta maxima) are of some commercial importance, producing a combined catch of some 91 x lo3 metric tons in 1973, mostly in the northeastern North Atlantic.

    2. Crustaceans No doubt Pseudocalanus is preyed upon by a variety of planktonic

    crustacea, but only euphausiids appear to have been implicated explicitly. Ponomareva (1 954) concluded that Pseudocalanus was about the right size among copepods of the Sea of Japan as food for Thysanoessa inermis, T . longipes and Euphausia pacifica. In the aquarium, euphausiids caught Pseudocalanus readily and ate out their soft parts, leaving the exoskeleton. In nature, parts of Pseudocalanw were regularly found in gut contents of euphausiids.

    3. Chaetognaths Chaetognaths are highly predaceous animals, eating many small

    animals of suitable size with which they come into contact. Since Pseudocalanus in its various stages is abundant and of suitable size, it is hardly surprising that it is eaten by chaetognaths. The most wide- spread chaetognath within the range of Pseudocalanus is Sagitta elegans (= Parasagitta elegans), but Sagitta setosa also occurs in the more southern parts of the range of the copepod.

    Adult female Pseudocalanus were prominent in the guts of 6-19 mm 8. elegans in the North and Celtic Seas in summer and the Irish Sea in winter, according to Rakusa-Suszczewski ( 1969). Pseudocalanus was evidently selected by small chaetognaths in preference to Calanus and Temora, even though Calanus was more abundant than Pseudo- calanus in the plankton.

    Rakusa-Suszczewski (1 969) found that most feeding on Pseudo- calanus took place at night. Pearre (1973), working with the same samples from Bedford Basin, Nova Scotia, from which vertical distributions of Pseudocalanus had been determined (Fig. 38) found that Pseudocalanw living near the surface in July were largely taken at night.

    McLaren (1969) gives a detailed account of the ways in which populations ofS. elegans in Ogac Lake, Baffin Island, depend on Pseudo- calanus. Adult chaetognaths produced eggs over a protracted period in


    spring, but recruitment of their young was only successful when the seasonal burst of nauplii of Pseudocalanw occurred. The sizes of the subsequent juvenile populations of chaetognaths were determined by the number of adult chaetognaths present at the times of these bursts of nauplii, but not on the number of nauplii present. McLaren also concluded that the overwinter survival of older S. elegans in Ogac Lake was dependent on accessibility of copepods, largely Pseudocalanus, in deeper water.

    Mironov (1960) studied the feeding of Sagitta setosa in the Black Sea in some detail. He found that Pseudocalanus was not very import- ant aa a food item in Sevastopol Bay in September 1961, but that it constituted about 77% of the daily ration of S. setosa by numbers and 97% by weight in offshore waters in February 1951. Rakusa- Suszczewski (1969) showed that Pseudocalanus was taken by S. setosa around the British Isles, but that it was never as important in the diet as was Temora.

    4. H ydromedwsae Lebour (1922) studied feeding of a number of species of hydro-

    medusans and recorded Pseudocalanus in the guts of the following species in samples from nature : Sarsia tubulosa, Rathkea octopunctata, Leukartiara octona (as Turris pileata), Phialidium spp. and Obelia spp.

    Although Pseudocalanus is eaten by Aglantha digitale in Ogac Lake, Baffin Island, McLaren (1969) found that recruitment of the tiny young of this hydromedusan appeared to be related to availability of phyto- plankton, and that its overwinter survival was unrelated to abundance of Pseudocalanw.

    It seems probable that, in general, hydromedusae are less important than chaetognaths as predators on Pseudocalanus.

    5. Ctenophores The tentaculatan ctenophore Pleurobrachia pileus occurs widely in

    northern waters and is known to be a predator on Pseudocalanw. Lebour (1923) found Pseudocalanus in a specimen of P. pileus from off Plymouth and Fraser (1970) included the " group Pseudocalanw and Paracalanus " as important to P. pileus in the North Atlantic. Carter (1965) considered that P. pilew had an important impact on Pseudo- calanus in Tessiarsuk, a landlocked bay on the coast of Labrador. We infer that P. pilewr feeds on Pseudocalanws in the Black Sea from Petipa et al. (1970).

    Two studies of predation by P. pileus give more details. Bishop (1968) studied feeding in the laboratory by P. bachei (= P. pilew of


    some authors) from waters of Washington State and found that they fed on adult and copepodid Pseudocalanus a t a rate of 1-7 copepods/ ctenophore/h, at a copepod density of 2511. of each stage. They fed more slowly on nauplii of Pseudocalanus (1.0 nauplii/ctenophore/h), but the significance of this difference cannot be ascertained (SD only given). Anderson (1974) found that 89% of gut contents of P. pileus in St. Margarets Bay, Nova Scotia, consisted of C V and adult copepods, including Pseudocalanus. He found that Temora and Centropages were about 10 times more likely than Pseudocalanus to be captured in the sea when the relative concentrations of the copepod species in the sea were taken into account. He attributes the relative invulnerability of Pseudocalanus to its manner of swimming (see p. 53). He also disputes Bishops (1968) rates of feeding of P. bachei (see above), suggesting that Bishops animals were feeding past satiation levels. However, Anderson does stress the great natural importance of P. pileus on copepods in general.

    The tentaculatan Bolinopsis microptera was also studied in the laboratory by Bishop (1968) in conditions as described above for P. bachei. He found that B. micropteya fed on Pseudocalanus of all stages at a rate of 0.9 copepods/ctenophore/h, somewhat lower than the rates for P. bachei. Anderson (1 974) found that Bolinopsis infundibulum also fed on Pseudocalanus, but preferred Oithona in particular.

    We conclude that ctenophores may be significant predators on Pseudocalanus, but probably less so than on some other species of copepods.

    C. Significance in the food web

    A species-by-species account of the species eaten by and the species that eat Pseudocalanus does not altogether fix its significance in the economy of the sea. Cushing (1970) and Steele (1974) are examples of the thrust toward systems analysis of production and the flow of matter or energy throughout the food webs of the sea.

    That Pseudocalanus is an important secondary producer in northern seas cannot be doubted. However, an initial note of caution must be made concerning the significance of this production in the food web. Recently Martens (1975) counted the numbers and estimated biomasses of dead Pseudocalanus sedimenting out of the water column and into collectors set in the western Baltic. He found that some 2.8 g C/m2/yr of Pseudocabnus was sedimented in this way. The figure compares with estimates of total production in some localities (see Section XIII). The great bulk of the Pseudocalanus carbon was sedimented in April-


    May, shortly after a numerical maximum in this copepod. It is possible that in regions with highly seasonal life cycles a major fraction of the production of Pseudocalanus can at times end up as detritus, even of spent adults, unused by predators. Martens work cries out for repetition elsewhere.

    One of the more detailed food chain analyses involving Pseudocalanm is presented by Petipa et al. (1970). They express on diagrams the standing crops and specific transfer rates (rates per unit of biomass) for the major components of the pelagic food web in the Black Sea (it should be noted that the captions in their Figs 1 and 2 are reversed). In the near-surface waters (the epiplankton ) older stages of Pseudo- calanus contribute little, although their young (grouped among nauplii) may be important as consumers of medium-sized phytoplank- ton. In deep water (the bathyplankton ) C IV-adults of Pseudo- calanus and Calanus are represented ashaving a dominant role, forming the largest standing crop among the herbivores and consuming much the greatest amount of the relatively common large phytoplankters at these depths. They conclude that at the herbivorous level the most powerful flow of matter and energy is through the migratory copepodites and adult large-sized copepods (Pseudocalanus and Calanus) .

    While it may rest on huge accomplishments in data acquisition and analysis, a detailed assessment of the flow of matter and energy through a food web is nothing more than descriptive science. However, steps are being made toward the study of food webs as a predictive science. The early systems analysis by Cushing (1959) included Pseudo- calanus among other copepods , but made no direct use of its para- meters of feeding, growth rates, etc. An example that explicitly contains parameters for Pseudocalanus is by Menshutkin et al. (1974). They developed a mathematical model of the pelagic ecosystem of the Sea of Japan, which includes Pseudocalanus as an important part of the mesoplankton component of the boreal epiplankton . They took into account all the variables of growth and advection that influenced the transfer functions of biomass (energy) through the food web, including such variables as currents, temperature, vertical migrations, etc. In this way they predicted the quantitative distributions of biomass (energy) of various categories throughout the Sea of Japan at various seasons. Although their results have not been fully tested, they do match fragmentary observations of the real patterns in the Sea of Japan.

    Another example is by Steele and Frost (1977), who construct a simulation model of nutrient-plant-herbivore-carnivore dynamics using parameters for small (= Pseudocalanus) and large ( = Calanus) cope-


    pods. Some of their assumptions match what we have shown: that there is an upper limit to assimilation and growth rates (set at a food level of 80 mg C/m3, which is probably too high, cf. p. 130), and that reproductive rate (as C) is the same as growth rate before maturity (see p. 131). Other assumptions about size-selection of food particles may be premature (see p. 63). Although their model produces some general results that match general observations, it fails in an attempt to simulate the seasonal cycle of Pseudocalanus in Loch Striven, Scotland. Steele and Frost conclude that this failure results largely from mis- assumptions about hydrographic restoration of nutrients, rather than from errors in the parameters of grazing and growth by copepods.

    D. Retrospects and prospects The importance of Pseudocalanus as a consumer, replenisher of

    nutrients and food base have been amply demonstrated. The genus is of particular significance to fish, and therefore to fisheries, of northern waters. Gulland (1970) notes " that the potential for great expansion of catches are among species lower in the ecological pyramid " ; that is, among fishes that feed on zooplankton. Lishev and Freimane (1970) have found high degrees of correlation between biomasses of Pseudo- calanus sampled at different times of year (see critical account of their work, p. 156). They argue that it should thus be possible to predict food supplies for planktivorous fishes. They also suggest that devia- tions from long-term regressions of population estimates of Pseudo- calanus at a given time of year on estimates at an earlier time of year (i.e. deviations from the usual mortality rate) may reflect differences in the amount consumed in the interval by plnnktivorous fishes. This in turn may give a new technique for estimating fish populations from the amount they consume. Altogether these possibilities, which stand apart from the main thrust of food-web studies in the sea, seem very worth exploring.

    A common aim of systems analyses of production in marine food webs is the substitution by general categories (e.g. trophic levels, biogeographic units, particle sizes) of the actual species involved. We hope that we have said enough in our lengthy review on the biology of Pseudocalanus to indicate that it may not be possible altogether to substitute somewhat abstract categories for the more objective realities of this interesting marine copepod.

    XVI. ACENOWLEDGEMENTS We are grateful to Dr R. J. Lincoln and the staff of the Crustacea

    Section, British Museum (Natural History) for allowing us the use of


    the section library, and also to Miss S. Fullerton and the staff of the Science Library, Dalhousie University, for much bibliographic assistance.

    The Trustees of the British Museum (Natural History) gave us permission to reproduce Fig. 39B, C and D. The Centre National de la Recherche Scientifique allowed us to reproduce Fig. 39A and Fig. 40.

    We are grateful to authors of theses who allowed us to make use of often previously unpublished material, and especially to Dr Brenda Thompson, whose thesis we have used so extensively.

    A large number of scientific colleagues throughout the world have given us advice, information and assistance throughout the preparation of this work. We are especially grateful to Robert Conover, Barry Hargrave, Kenneth Mann, the late Sheina Marshall, Georges Merinfeld, Eric Mills, Serge Poulet and Sharon Smith for reading the typescript of one or more sections and to Georges Merinfeld for bibliographic assist- ance. Despite their help, inadequacies remain for which we are entirely responsible.

    Our research has been supported by grants from the National Research Council of Canada to I.A.M.


    Ackefors, H. (1966). Plankton and hydrography of the Landsort Deep. Veroflent- lichwngen des Institutes fiir Meeresforschung i n Bremerhaven, Xonderbd., 2 ,

    Ackefors, H. (1 969a). Ecological zooplankton investigations in the Baltic proper, 1963-1966. Report. Institute of marine Reeearch Lysekil, Seriea

    Seasonal and vertical distribution of the zooplankton in the Ask6 area (northern Baltic proper) in relation to hydrographical conditions. Oikos, 20, 480-492.

    Adler, G. and Jespersen, P. (1920). Variations saisonnihres chez quelques cop& podes planctoniques marins. Meddelelser f ra Kommhsionen for Hawunder- segelser, Serie Plankton, 2(1), 1-46.

    Afrikova, S. G. (1975). Distribution of Pseudocalanus elongatus (Boeck) in the Black Sea. Gidrobiologicheskil zhurnal, 11(5), 92-97. (In Russian.)

    Afrikova, S. G. (1976). On the die1 vertical migration of Black Sea Pseudocalantia elongatus (Boeck). Biologiya Morya, Kiev, 37, 68-76. (In Russian.)

    Anderson, E. (1974). Trophic interactions among ctenophores and copepods in St. Margarets Bay, Nova Scotia. Ph.D. Thesis, Dalhousie University, Halifax, Nova Scotia.

    Andreeva, V. V. (1975). Basic features of the biology of some very abundant species of copepods of the Northern part of the Tatar Strait. I n Biologi- cheskie Resursy Morei Dalnego Vostoka (abstracts of an All-Union symposium, Vladivostok, Oct. 1976), pp. 13-16. Tikhookeanskii nauchno- issledovatelskii institut rybnogo khozyaistva i okeanografii (TINRO), Vladivostok. (In Russian.)


    Biology, 18, 1-139. Ackefors, H. (1969b).


    Andreeva, V. V. (1976s). Influence of temperature on the duration of develop- ment in Pseudocabnus elongatus (Boeck). I n gksperimentalnaya Ekolo- giya Morskikh Bespozvonochnykh (symposium held a t the Vostok Biological Station, 1976), pp. 17-18. Akademiya nauk SSSR, Vladivostok. (In Russian.)

    Production estimates for P8eUdOCdanUS elongatus Boeck in the Northern part of the Japan Sea. I n Vsesoyuznaya kon- ferentsiya molodykh uchenykh Nauchno-tekhnicheskii progress v Wbnoi promjkhlennosti , pp. 13-14. Ministerstvo rybnogo khozyaistva SSSR, Tsentralnj% nauchno-issledovatelskii institut infonnatsii i tekhniko- bkonomicheskikh issledovanii, Moscow. (In Russian.)

    Anraku, M. (1964a). Influence of the Cape Cod Canal on the hydrography and on the copepods in Buzzards Bay and Cape Cod Bay, Massachusetts. I. Hydrography and distribution of copepods. Limnology and Oceanography, 9, 46-60.

    Anraku, M. (1964b). Influence of the Cape Cod Canal on the hydrography and on the copepods in Buzzards Bay and Cape Cod Bay, Massachusetts. 11. Respiration and feeding. Limnology and Oceanography, 9, 195-206.

    Anraku, M. (1964~). Some technical problems encountered in quantitative studies of grazing and predation by marine planktonic copepods. Jaz~nzal of the Oceanographical Society of Japan, 20, 221-231.

    Preliminary survey of the relationship between the feeding habit and the structure of the mouth-parts of marine copepods. Limnology and Oceanography, 8 , 116-126.

    Apstein, C. (191 1). Parasiten von Calanus finmarchicus. Wissenschaftliche Meeresuntersuchunge?a der Kommission fur wissenschaftlichen Untersuchung der deutschen Meere. Abt. Kiel, 13, 205-223.

    Arashkevich, Ye. G . (1969). The food and feeding of copepods in the north- western Pacific. Oceanology, 9, 695-709. (English version.)

    Arndt, E. A. and Stein, H. (1973). Biologische Untersuchungen wlihrend des Internationalen Ostseejahres (International Baltic Year, IBY) 1969/70. 111. Das Zooplankton. Beitrme zur Meereskunde, 32, 33-35.

    Aronovich, T. M., Doroshev, S. I., Spectorova, L. V. and Makhotin, V. M. (1975). Egg incubation and larval rearing of navaga (Eleginw navaga Pall.), polar cod (Boreogadus saida Lepechin) and arctic flounder (Liopetta glacialis Pall.) in the laboratory. Aquaculture 6, 233-242.

    Bainbridge, R. (1952). Underwater observations on the swimming of marine zooplankton. Journal of the Marine Biological Association of the United Kingdom, 31, 107-112.

    Barnes, H. and Marshall, S. M. (1951). On the variability of replicate plankton samples and some applications of contagious series to the statistical distribution of catches over restricted periods. Journal of the Marine Biological Association of the United Kingdom, 30, 233-263.

    Beklemishev, K. V. (1954a). The discovery of siliceous formations in the epi- dermis of lower Crustacea. Dokladg Akademii nauk SSSR, 97,543-545. (In Russian.)

    Beklemishev, K. V. (1954b). Feeding of several common planktonic copepods in far eastern seas. Zoolog~chesk~~ zhurnal, 33, 1210-1230. (In Russian.)

    Beklemishev, C. W. [K. V.] (1962). Superfluous feeding of marine herbivorous ZOO- plankton. Rapport et procb-verbaw des rhunwns. Oonseil permanent inter- national pour lexploratirm. de la mer, 153, 108-113.

    hdreeva , v. v. (1976b).

    Anraku, M. and Omori, M. (1963).


    Bglehrhdek, J. (1935). Temperature and living matter. Protoplaama mono- graphien, 8, 1-277.

    Bigelow, H. B. (1926). Plankton of the offshore waters of the Gulf of Maine. Bulletin of the United States Bureau of FGheries, 40, 1-509.

    Bigelow, H. B. (1927). Physical oceanography of the Gulf of Maine. Bulletin of the United States Bureau of Fisheries, 40, 511-1027.

    Bishop, J. W. (1968). A comparative study of feeding rates of tentaculate ctenophores. Ecology, 49, 9 9 6 9 9 7 .

    Bjornberg, T. K. S. (1973). The planktonic copepods of the Marchile I Expedition and of the Eltanin Cruises 3-6 taken in the SE Pacific. Boletim de Zoologia e Biologia Marinha, N.S., 30, 245-394.

    The feeding of herring larvae and their ecology in relation to feeding. Report. California Cooperative Oceanic Fisheries Investi- gations, 10, 79-88.

    Oversigt over de ved Norges Kyster iagttagne Copepoder henherende ti1 Calanidernes, Cyclopidernes, og Harpactidernes Familier. Forhandlinger, Videnskabsselskabet i Kristiania, 7 , 2 2 6 2 8 2 .

    Boeck, A. (1872). Nye Slaegter og Arter af Saltvands-Copepoder. Forhandlinger, Videnskabsselskabet i Kristiania, 14, 35-60.

    Bogorov, B. :G. (1939). Sex ratio in marine copepods. (On the problem of the evaluation of plankton production). Dokladg Akademii nauk SSSR, 23, 706-709. (In Russian.)

    Bogorov, B. G. (1946). Peculiarities of diurnal vertical migrations of zooplankton in polar seas. Journal of Marine Research, 6 , 25-32.

    Borradaile, L. A., Potts, F. A., Eastham,.L. E. S. and Saunders, J. T. (1961). The Invertebrata . The University Press, Cambridge.

    Bottrell, H. H. (1975). The relationship between temperature and duration of egg development in some epiphytic Cladocera and Copepoda from the River Thames, Reading, with a discussion of temperature functions. Oecologia,

    The distribution of calanoid copepods off the south- eastern United States between Cape Hatteras and southern Florida. Smith- sonian Contributions to Zoology, 96, 1-58.

    Brady, G. S. (1863). Report of dredging operations on the coasts of Northumber- land and Durham in July and August 1863. Transactions of Tyneside Naturalists Field Club, 6 , 178-194.

    Brady, G. S. (1865). Report on the pelagic Entomostraca dredged off the coasts of Northumberland and Durham, 1862-64. Natural History Transactions of Northumberland Durham and Newcaatle-on-Tyne, 1, 29-40.

    Brady, G. S. (1878). A Monograph of the Free and Semi-parasitic Copepoda of the British Islands , Vol. 1. Ray Society, London.

    Bradley, B. P. (1975). The anomalous influence of salinity on temperature tolerance of summer and winter populations of the copepod Eurytemora afinia. Biological Bulletin, 148, 2 6 3 4 .

    Izvestiya Tikhookeanskogo nauchno-issledovatelskogo instituta ebnogo khozyabtva d okeanografii, 26, 3-130. (In Russian.)

    Brodskii, K. A. (1950). Calanoida of the Far Eastern Seas and Polar Basin of the USSR . (1967 transl. Israel Programme for Scientific Translations, Jerusalem.)

    Blaxter, J . H. S. (1963).

    Boeck, A. (1864).

    18, 63-84. Bowman, T. E. (1971).

    Brodskii, K. A. (1948). Free-living Copepoda of the Sea of Japan.


    Brodskii, K. A. (1956). The regional distribution of pelagic life in far eastern seas and adjacent waters of the Pacific Ocean as shown by a study of the copepod fauna (Calanoida). Trudg problemngkh i tematichkikh soves- hchanii. Zoologicheskii institut, 6, 22-35. (In Russian.)

    Plankton studies in relation to the western mackerel fishery. Journal of the Marine Biological Association of the United Kingdom,

    Butler, E. I., Corner, E. D. S. and Marshall, S. M. (1969). On the nutrition and metabolism of zooplankton. VI. Feeding efficiency of Calanus in terms of nitrogen and phosphorus. Journal of the Marine Biological Association of the United Kingdom, 49, 977-1001.

    Cairns, A. A. (1967). The zooplankton of Tanquary Fjord, Ellesmere Island, with special reference to the calanoid copepods. Journal of the Fkheries Research Board of Canada, 24, 555-568.

    On the feeding mechanism of the copepods Calanus jinmarchicua and Diaptomus gracilis. British Journal of Experimental

    Canu, E. (1892). Les cophpodes du Boulonnais. Morphologie, embryologie, taxonomie. Travaux du hboratoire de zoologie maritime de Wimereux- Ambleteuse (Pas-de-Calais) 6, 1-292. Also published as separate the&, Danel, Lille.

    Carlisle, D. B. and Pitman, W. J. (1961). Diapause, neurosecretion, and hormones in Copepoda. Nature, London, 190, 827-829.

    Carrillo B.-G., E., Miller, C. B. and Wiebe, P. H. (1974). Failure of interbreeding between Atlantic and Paciiic populations of the marine calanoid copepod Acartia clausi Giesbrecht. Limnology and Oceanography, 19, 452-458.

    The ecology of the calanoid copepod Pseudocalanus minutus Krrayer in Tessiarsuk, a ooastal meromictic lake of northern Labrador. Limnology and Oceanography, 10, 345-353.

    Cattley, J. G. (1948). Sex reversal in copepods. Nature, London, 161, 937. Caullery, M. (1910). Ellobiopsis clhattoni, n.g., n.sp., parasite de Calanus helgo-

    landicus Claus, appartenant probablement aux pdridiniens. Bulletin scientifique de la France et de la Belgique, 44, 201-214.

    Chatton, E. (191 1). Sur divers parasites de copBpodes pdlagiques observes par M . Apstein. Compte rendu hebdomadaire des Sdances de IAcaddmie des Sciences, 153, 474-476.

    Chatton, E. (1 920). Les peridiniens parasites. Morphologie, reproduction, Bthologie. Archives de Zoologie expdrimentale et gdndrale, 59, 1-475.

    Christiansen, F. E. (1968). Nitrogen excretion by some planktonic copepods of Bras dOr Lake, Nova Scotia. M.Sc. Thesis, Dalhousie University, Halifax, Nova Scotia.

    Ciszewski, P. and Witek, 2. (1975). Production of copepods Psedocalanzta elongatus and Acartia bi$losa in the Gdansk Deep area. 4th Symposium of Baltic Marine Biologists, Cfdhsk, Poland, 13-18 Oct. 1975, p. 22.

    Colebrook, J. M. (1964). Continuous plankton records : a principal component analysis of the geographical distribution of zooplankton. Bulletin of Marine Ecology, 6, 78-100.

    Colebrook, J. M. (1969). Variability in the plankton. Progressive Oceanography, 5, 115-125.

    Bullen, G. E. (1908).

    8, 269-302.

    Cannon, H. G. (1928).

    Biology, 6, 131-144.

    Carter, J. C. H. (1965).


    Colebrook, J. M., John, D. E. and Brown, W. W. (1961). Contribution towards a plankton atlas of the north-eastern Atlantic and the North Sea. Part I1 : Copepoda. Bulletin of Marine Ecology, 5, 90-97.

    Conover, R. J. (1959). Regional and seasonal variation in the respiratory rate of marine copepods. Limnology and Oceanography, 4, 259-268.

    Conover, R. J. (1974). Production in marine planktonic communities. Pro- ceedings Pirst International Congress of Ecology, The Hague, 8-14 Sept. 1974, 159-163.

    In Marine Ecology. Vol. IV, Dynamics (0. Kinne, ed.). Wiley, London.

    Rapports et prods-verbaw des r6unions. Conseil international pour Cexploration de la mer, 173.

    Conover, R. J. and Francis, V. (1973). The use of radioactive isotopes to measure the transfer of materials in aquatic food chains. Marine Biology, 18, 272- 283.

    Corkett, C. J. (1966). Studies on the biology of the marine planktonic copepods Psez~docalanus elongatus and Temora longicornis under laboratory conditions, t,ogether with morphological studies on the larval stages. Ph.D. Thesis, University of London.

    Observations sur les stades larvaires de Pseudocalanus elongatus Boeck et Temora longicornis 0. F. Miiller. Pelagos. Bulletin de llmtitut Ockanographipue dAlger, 8 , 51-67.

    Corkett, C. J. (1969). Reproduction and oil storage by Pseudocalanus in nature : an approach to copepod production. Unpublished report to Bedford Institute Oceanography, Dartmouth, Nova Scotia.

    Corkett, C. J. (1970). Techniques for breeding and rearing marine calanoid copepods. Helgolander wissenschuftliche Meeresuntersuchungen, 20, 3 18-324.

    Corkett, C. J. and McLaren, I. A. (1969). Egg production and oil storage by the copepod Pseudocalanus in the laboratory. Journal of Experimental Marine Biology and Ecology, 3, 90-105.

    Corkett, C. J. and McLaren, I. A. (1970). Relationships between development rate of eggs and older stages of copepods. Journal of the Marine Biological Association of the United Kingdom, 50, 161-168.

    Observations on the keeping of adult female Pseudocalanua elongatus under laboratory conditions. Journal of the Marine Biological Association of the United Kingdom, 48, 97-105.

    Corkett, C. J. and Zillion, E. J. (1975). Studies on the effect of temperature on the egg laying of three species of calanoid copepods in the laboratory. Bulletin of Plankton Society, Japan, 21, 13-21.

    Corner, E. D. S. and Cowey, C. B. (1968). Biochemical studies on the production of marine zooplankton. Biological Reviews, 43, 393-426.

    Corner, E. D. S. and Davies, A. G. (1971). Plankton as a factor in the nitrogen and phosphorus cycles in the sea. Advances in Marine Biology, 9, 101-204.

    Corner, E. D. S., Cowey, C. B. and Marshall, S. M. (1966). On the nutrition and metabolism of zooplankton. 111. Nitrogen excretion by Calanus. Journal of the Marine Biological Association of the United Kingdom, 45,

    Crawshay, L. R. (1915). Notes on experiments in the keeping of plankton animals under artificial conditions. Journal of the Mwine Biological Association of the United Kingdom, 10,665-676.

    Conover, R. J. (In press).

    Conover, It. J. (1978). Feeding interactions in the pelagic zone.

    Transformation of organic matter.

    Corkett, C. J. (1968).

    Corkett, C. J. and Urry, D. L. (1968).



    Curl, H. and McLeod, G. C. (1961). The physiological ecology of a marine diatom, Skeletonema costatum (Grev.) Cleve. Journal of Marine Research, 19, 70-88.

    Cushing, D. H. (1955). Production and a pelagic fishery. Pishery Investigations. Ministry of Agriculture, Food and Fisheries, 18, 1-104.

    Cushing, D. IT. (1959). On the nature of production in the sea. F i d e r y Investi- gations. Ministry of Agriculture, Fisheries and Food, Ser. 2, 22(6), 1-40.

    Cushing, D. H. (1970). Introduction. I n Marine Food Chains (J. H. Steele, ed.), pp. 69-73. Oliver and Boyd, Edinburgh.

    Dngg, M. (1977). Some effects of patchy food environments on copepods. Lim- nology and Oceanography, 22, 99-107.

    Davis, C. C. (1949). The pelagic Copepoda of the north-eastern Pacific Ocean. University of Washington Publications in Biology, Seattle, 14, 1-1 17.

    Davis, C. C. (1976). Overwintering strategies of common planktic copepods in some North Norway fjords and sounds. Astarte 9, 37-42.

    Deevey, G. B. (1952). Quantity and composition of the zooplankton of Block Island Sound, 1949. Bulletin of the Bingham Oceanographic Collection, Yale University, 13, 120-164.

    Deevey, G. B. (1956). Oceanography of Long Island Sound, 1952-1954. V. Zoo- plankton. Bulletin of the Bingham Oceanographic Collection, Yale University,

    Dewey, G. B. (1960a). The zooplankton of the surface waters of the Delaware Bay region. Bulletin of the Bingham Oceanographic Collection, Yale Uni- versity, 17, 5-53.

    Relative effects of temperature and food on seasonal variations in length of marine copepods in some eastern American and western European waters. Bulletin of the Ringham Oceanographic Collection, Yale University, 17, 54-84.

    The annual cycle in quantity and composition of the zooplttrikton of the Sargasso Sea off Bermuda. 1. The upper 500 m. TAmnology and Oceanography, 16, 219-240.

    Delalo, E. P. (1964). The die1 feeding rhythm in PseudocaEanw elongatus (Boeck). Trudg Sevastopolskoi biologicheskoi stantsii. A kademiya nauk SSSR, 15, 94-100. (In Russian.)

    The biology of the small planktonic copepods of Ply- mouth. Journal of the Marine Biological Association of the United Kingdom,

    Digby, P. 8. B. (1954). The biology of the marine planktonic copepods of Scoresby Sound, East Greenland. Journal of Animal Ecology, 23, 298-338.

    Digby, P. S. B. (1967). Pressure sensitivity and its mechanism in the shallow marine environment. Symposia of the Zoological Society of London, 19,

    Salmon of the North Review of oceanography of the subarctic Pacific

    Bulletin of the International North Pacific Fisheries Commission,

    Dissodinium pseudocalani sp. nov., ein parasitischer Dino- Helgolander wissenschaftliche Meeresunter-

    Entwicklung des Ektoparasiten Dissodinium pseudocalani Accompanying pamphlet for scientific film C 1069/1971,

    15, 113-155.

    Deevey, G. B. (1960b).

    Deevey, G. B. (1971).

    Digby, P. S. B. (1950).

    29, 393-438.

    159- 1 88. Dodimearl, A. J., Favorite, F. and Hirano, T. (1963).

    Pacific Ocean. Part 2. region. 13, 1-195.

    Drebes, G. (1969). flagellat auf Copepodeneiern. suchumgen, 19, 58-67.

    (Dinophyceae). Institut fur den wissenschaftlichen Film, CGttingen.

    Drebes, G. (1972).


    Dunbar, M. J. (1947). Note on the delimitation of the arctic and subarctic zones. Canadian Field Naturalist, 61, 12-14.

    Dunbar, M. J. and Harding, G. (1968). Arctic Ocean water masses and plankton -a reappraisal. I n Arctic Drifting Stations (J. E. Slater, coordinator), pp. 315-326. Arctic Institute of North America.

    Edinburgh Oceanographic Laboratory ( 1973). Continuous plankton records : 8 plankton atlas of the North Atlantic and the North Sea. Bulletin of Marine

    Edmondson, W. T., Comita, G. W. and Anderson, G. (1962). Reproductive rate of copepods in nature and its relation to phytoplankton population. Ecology,

    Eriksson, S. (1973a). The biology of marine planktonic Copepoda on the west coast of Sweden. Zoon, 1, 37-68.

    Eriksson, S. (1 97313). Preliminary zooplankton investigations in the dregrund Archipelago (southwestern Bothnian Sea) during the summer 1970. Zoon, 1, 95-111.

    Esterley, C. 0. (1916). The feeding habits and food of pelagic copepods and the question of nutrition by organic sitbstances in solution in the water. University of Calijornia Publications in Zoology, 16, 171-184.

    Evans, F. (1973). The permanent zooplankton of Northumberland coastal waters. Proceedings of University of Newcastle upon Tyne Philosophical Society, 2 , 25-68.

    Evans, F. (1977). Seasonal density and production estimates of the commoner planktonic copepods of Northumberland coastal waters. Estuarine and Coastul Marine Science, 5, 223-241.

    FA0 (1974). Yearbook of Fishery Statistics. Vol. 36. Catches and Landings, 1973. U.N. Food and Agriculture Organisation.

    Faber, D. J. (1966). Free-swimming copepod nauplii of Narragansett Bay with a key to their identification. Journal of the Fisheries Research Board of Canada, 23, 180-205.

    Falconer, D. S. (1960). Introduction to Quantitative Genetics . Ronald Press, New York.

    Farran, G. P. and Vervoort, W. (1951). Copepoda, sub-order: Calanoida; family: Pseudocalanidae. Fiches didenti,fication d u zooplankton, Conseil permanent international pour ZExploratwn de la Mer, No. 37.

    Fedorov, V. D., Zhitina, L. 5. and Polyakova, T. V. (1975). Daily production of mass species of White Sea zooplankton. Izvestiya Akademii Nauk SSSR, 8er. biol., 5, 719-726. (In Russian.)

    Fish, C. J. (1925). Seasonal distribution of the plankton of the Woods Hole region. Bulletin of the United States Bureau of Fisheries, 41, 91-179.

    Fish, C. J. (1936). The biology of Pseudocalanus minutus in tho Gulf of Maine and the Bay of Fundy. Biological Bulletin, 70, 193-216.

    Fives, J. M. (1969). Investigations of the plankton of the west coast of Ireland. 2. Planktonic surveys during the years 1958-63. Proceedings of Royal Irish Academy, 67, 233-259.

    Fleminger, A. (1967). Distributional atlas of calanoid copepods in the California Current region, Part 11. Culifornk Cooperative Oceanic Fisheries Inuesti- gations Atlas 7 , 1-213.

    Ecology, 7 , 1-174.

    43, 625-634.


    Fontaine, M. (1955). The planktonic copepods (Calanoida, Cyclopoida, Monstril- loida) of Ungava Bay, with special reference to the biology of Pseudocalanw minutus and Calanus finmarchicus. Journal of the Pishm%es Research. Bomd of Canada, 12, 858-898.

    The ecology of the ctenophore Pleurobrachia pileus in Scottish waters. Journal du Conseil. Conseil permanent international pour lexploration de la mer, Copenhague, 33, 149-168.

    Frost, B. W. (1974). Feeding processes a t lower trophic levels in pelagic food communities. In The Biology of the Pacific Ocean (C. B. Miller, ed.), pp. 59-77. Oregon State Univ.

    Friichtl, F. (1 920). Planktoncopepoden aus der nordlichen Adria. Sitzun.gs- berichte der Alcademie der Wwseiwchaften Wien, Math.-naturw&8. Kl., Abt.

    Furuhashi, K. (1961). On the possible segregation found in the copepod fauna in the deep waters off south-eastern coast of Japan, Publications of the Set0 Marine Biological Laboratory, 9, 1-13.

    Furuhashi, K. (1966). Studies on the vertical distribution of copepods in the Oyashio region east of Japan and in the Kuroshio region south of Japan. Publications of the Set0 Marine Biological Laboratory, 14, 295-322.

    Biologie des copepodes pelagiques du golfe de Marseille. Recueil des Travaux de la Station marine dEndoume, Pacult6 dea Sciences de Marseille, 42 (Bull. 47), 93-184.

    Gauld, D. T. (1951). The grazing rate of planktonic copepods. Journal of the Marine Biological Association of the United Kingdom, 29, 695-706.

    Gauld, D. T. (1964). Feeding in planktonic copepods. In Grazing in Terrestrial and Marine Environments (D. J. Crisp, ed.), pp. 239-245. Blackwell, Oxford.

    Gauld, D. T. (1966). The swimming and feeding of planktonic copepods. I n Some Contemporary Studies in Marine Science (H. Barnes, ed.), pp. 313- 334. Allen and Unwin, London.

    Gem, G. H. and Hargrave, B. T. (1966). Primary and secondary production in Bras dOr Lake, Nova Scotia, Canada. Verhandlungen Internationaleiz Vereinigung fur Theoretische und Angewandte Limnologie, 16, 333-340.

    Gibson, V. R. and Grice, G. D. (1977). Response of macro-zooplankton POpUlE- tions to copper: Controlled Ecosystem pollution experiment. Bulletin of Marine Science, 27, 85-91.

    Giesbrecht, W. (1881). Vorliiufige Mittheilung aus einer Arbeit uber die freileben- den Copepoden des Kieler Hafens. Zoologischer Anzeiger, 4, 254-268.

    Giesbrecht, W. (1882). Die freilebenden Copepoden der Kieler Foehrde. Bericht Kommision zur wissenschaftlichen Untersuchung des deutschert Meere, Kiel, 4, 85-168.

    Glover, R. S., Robinson, G. A. and Colebrook, J. M. (1974). Marine biological surveillance. Environment and Change, 2, 395-402.

    Gonnert, R. (1936). Sporodinium pseudocalani n.g., n. sp., ein Parasit aus Copepodeneiern. Zei&chr$t f u r Parasitenkunde, 9, 140-143.

    Grainger, E. H. (1959). The annual oceanographic cycle at Igloolik in the Canadian arctic. 1. The zooplankton and physical and chemical observa- tions. Journal of the Fisheries Research Board of Canada, 16, 453-501.

    Grainger, E. H. (1965). Zooplankton from the Arctic Ocean and adjacent Canadian waters. Journal of the Fisheries Reseamh Board of C a d a , 22,

    Fraser, J. H. (1970).

    1, 129, 463-509.

    Gaudy, R. (1962).




    Greze, V. N. (1970). The biomass and production of different trophic levels in the pelagic communities of south seas. I n " Marine Food Chains " (J. H. Steele, ed.), pp. 458-467. Oliver and Boyd, Edinburgh.

    Greze, V. N. (1973). Secondary production in southern seas. Oceanology, 13, 80-85. (English edition.)

    Greze, V. N., Baldina, E. P. and Bileva, 0. K. (1968). Production of planktonic copepods in the neritic zone of the Black Sea. Oceanology, 8 , 839-843. (English edition.)

    Calanoid copepods from equatorial waters of the Pacific Ocean. Fkhery Bulletin, Fish and Wildlife Service, United States Department of the Interior, 61, 171-246.

    Copepods collected by the nuclear submarine Seadragon on a cruise to and from the North Pole, with remarks on their geographic distribution. Journal of Marine Research, 20, 97-109.

    Grice, G. D. and Hulsemann, K. (1965). Abundance, vertical distribution, and taxonomy of calanoid copepods a t selected stations in the northeast Atlantic. Journal of Zoology, 146, 213-262.

    Grice, G. D., Wiebe, P. H. and Hoagland, E. (1973). Acid-iron wmtc as a factor affecting the distribution and abundance of zooplankton in the New York Bight. I. Laboratory studies on the effects of acid waste on copepods. Estuarine and Coastal Marine Science, 1, 45-50.

    Griffiths, A. M. and Frost, B. W. (1976). Chemical communication in the marine planktonic copepods Calanus paci$cus and Pseudocalanua sp. Cruatacmna,

    Gulland, J. A. (1970). Food chain studies and some problems in world fisheries. Oliver and

    " British Fresh-water Copepoda ", Vol. I. Ray Society,

    Grice, G. D. (1961).

    Grice, G. D. (1962).

    30, 1-8.

    I n " Marine Food Chains " (J. H. Steele, ed.), pp. 296-315. Boyd, Edinburgh.

    Gurney, R. (1931). London.

    Gurney, R. (1942). " Larvae of Decapod Crustacea ". Ray Society, London. Hansen, K. V. (1951). On the diurnal migration of zooplankton in relation to

    the discontinuity layer. Journal du conseil. Conseil permanent international pour I'Exploration de la Mer, Copenhague, 17, 231-241.

    Hansen, K. V. (1960). Investigations on the quantitative and qualitative distribution of zooplankton in the southern part of the Norwegian Sea. Meddelelser fra Danmrks Fiskeri- og Havundersegelser, N.S., 2(23), 1-63.

    Harding, G. C. H. (1966). Zooplankton distribution in the Arctic Ocean with notes on life cycles. M.Sc. Thesis, MoGill University, Montreal.

    Rarding, G. C. H. (1972). Ecological observations on North Atlantic deep sea copepods. Ph.D. Thesis, Dalhousie University, Halifax, Nova Scotia.

    Hardy, A. C. (1924). The herring in relation to its animate environment. Part 1. Fishery Investigations. Ministry of Agriculture, Food and Fisheries, Ser. 2 ,

    Hardy, A. C. (1956). " The Open Sea. Its Natural History. Part 1, The World

    Hargrave, B. T. (1966). Some aspects of phosphorus excretion by planktonic M.Sc. Thesis,

    Hargrave, B. T. and Geen, G. H. (1968). Phosphorus excretion by zooplankton.

    7(3), 1-53.

    of Plankton ". Collins, London.

    and benthic crustaceans of Bras d'Or Lake, Nova Scotia. Dalhousie University, Halifax, Nova Sootia.

    Limwlogy and Oceanography, 13, 332-342.


    Hargrave, B. T. and Geen, G. H. (1970). Effects of copepod grazing on two natural phytoplankton populations. Journal of the Fisheries R M ~ T C A Board of Canada, 27, 1395-1403.

    Harris, R. P. and Paffenhofer, G.-A. (1976). The effect of food concentration on cumulative ingestion and growth efficiency of two sniall marine plank- tonic copepods. Journal of the Marine Biological Association of the United Kingdom, 56, 875-888.

    Temperature acclimation and other influences on embryonic development in the copepod Pseudocalanus. Marine

    The life histories of plankton animals and seasonal cycles of plankton communities in the oceans. Journal du comeil. Conaeil permanent international pour IExploration de la Mer, Copenhague, 27, 15-24.

    Hessle, C. and Vallin, S. (1934). Undersokningar over plankton och dess viixlin- gar i Ostersjon under Bren 1925-1927. Svenska hydrografisk-bwlogislca kommissionens skrijter. Biologi. ( N . S.) 1(5), 1-132.

    Hirschfeld, H. S. (1974). Some observations on the breeding of Pseudoccllanwr in tho laboratory and comparisons with other calanoid species. B.Sc. Hons. Thesis, Dalhousie University, Halifax, Nova Scotia.

    Hjort, J. (1914). Fluctuations in the great fisheries of northern Europe viewed in the light of biological research. Rapport et Procka- Verbaux des Rdunwna. Conseil permanent international pour 1Exploration de la Mer, 20, 1-228.

    Huizinga, H. W. (1966). Studies of the life cycle and development of Contracaecum apiculigerum (Rudolphi, 1809) (Ascaroidea : Heterocheilidae) from marine piscivorous birds. Journal of the Elisha Mitchell Scienti,fic Society, 82,

    Hum, J. and Scotto di Carlo, B. (1968). Comparazione tra lo zooplancton del Golfo di Napoli e dellAdriatico meridionale presso Dubrovnik. I. Copepoda. Pubblicazioni della Stazione zoologica di Napoli, 36, 21-102.

    Copepodi pelagici dellAdriatico set- tentrionale nel periodo gennaio-dicembre 1965. Pubblicazioni della Stazione zoologica d i Napoli, 37, Suppl. 2, 173-195.

    Ikeda, T. (1970). Relationship between respiration rate and body size in marine plankton animals as a function of the temperature of habitat. Bulletin of the Faculty of Pisheries, Hokkaido University, 21, 91-112.

    Ikeda, T. (1974). Nutritional ecology of marine zooplankton. Memoirs of the Faculty of Fisheries, Hokkaido Univer&y, 22, 1-97.

    Itoh, K. (1970). A consideration on feeding habits of planktonic copepods in relation to the structure of their oral parts. Bulletin of Plankton Society of Japan, 17, 1-10. (In Japanese, English summary.)

    Jeffries, H. P. (1962). Copepod indicator species in estuaries. Ecology, 43, 730-733.

    Jeffries, H. P. and Alzara, L. (1970). Dominance-diversity relationships of the free amino acids in coastal zooplankton. Comparative Biochemistry and

    Jepps, M. W. (19378). Note on Apsteins parasites and some very early larval Platyhelminthes. Parmitology, 29, 554-558.

    Jepps, M. W. (193713). On the protozoan parasites of Calanue finmarchicus in the Clyde Sea area. Quarterly Journal of Microscopical Science, 79, 589-668.

    Jespersen, P. (1939). Investigations on the copepod fauna in East Greenland waters. Meddelelser om Grenland, 119(9), 1-106.

    Hart, R. C. and McLaren, I. A. (1978).

    Biology, 45, 23-30. Heinrich, A. K. (1962).


    Hum, J. and Scotto di Carlo, B. (1969).

    Phy~iology, 37, 215-223.


    Kaestner, A. (1970). Interscience, New York.

    Kamshilov, M. M. (1951). Determination of the weight of Calanus$nmarchicus Gunner, on the basis of body length measurements. Dokladfj Akademii muk SSSR, 76, 945-948. (In Russian.)

    Kamshilov, M. M. (1961). Data on the biology of Pseudocalanus elongatus Boeck in the Barents and White Seas. I n " Hydrological and Biological Features of the Inshore Waters of Murman" (M. M. Kamshilov, ed.), pp. 109-126. Murmanskoe Knizhnoe Izdatel'stvo, Murmansk. (In Russian.)

    Katona, S. K. (1973). Evidence for sex pheromones in planktonic copepods. Limnology and Oceanography, 18, 574483 .

    Katona, S. K. and Moodie, C. F. (1969). Breeding of Pseudocalanus elongatus in the laboratory. Journal of the Marine Biological Association of the United Kingdom, 49, 743-747.

    Kimor, B. and Wood, E. J. F. (1975). A plankton study in the eastern Mediter- ranean Sea. Marine Biology, 29, 321-333.

    Klyashtorin, L. B. and Yarzhombek, A. A. (1973). Energy consumption in active movements of planktonic organisms. Oceanology, 13, 575-580. (English edition.)

    Kolosova, Ye. G. (1975). Effect of temperature on the distribution of mass species of zooplankton in the White Sea. Oceanology, 15, 92-95. (English edition, published in 1976.)

    Size composition of planktonic copepods at various depths in the Black Sea. Gidrobiologicheskii zhurnal, 3(3), 74-77. (In Russian.)

    On the size of the pelagic copepods in the Black Sea, Mediterranean Sea, and Adriatic Sea in relation to habitat conditions. I n " Biological Investigations of the Black Sea and its Biological Resources " (V. A. Vodyanitskii, ed.), pp. 63-66. Nauka, Moscow. (In Russian.)

    Kraefft, F. (1910). mer das Plankton in Ost- und Nordsee und den Verbindungs- gebieten mit Besonderer Beriicksichtigung der Copepoden. Wissenschaft- liche Meeresunterwchungen der Iiornmksion zur Wissenschaft,?ichen Unter- auchung der deutschen Meere, Abt. Kiel, 11, 29-107.

    Kraneis, W. and Martens, P. (1975). Ecological studies on the plankton in the Kiel Bight 11. Zooplankton. 1Merentutkimuslaitoksen Julkaisu, 239, 187-194.

    Kreyer, H. (1842-45). Plate 41, fig. 4. I n " Voyages de la Commission Scienti- fique du Nord en Scandinavie, en Laponie, au Spitzberg et aux FBroe pendant les annBes 1838-40, sur la corvette La Recherche commandbe par M. Fabvre. Zoologie, Atlas " (P. Gaimard, ed.). Paris.

    Kreyer, H. (1 848). Karcinologiske Bidrag. Naturhiatorisk Tidsskrqt, Ser. 2,

    Krylov, V. V. (1968). Relation between wet formalin weight of copepods and copepod body length. Oceanology, 8, 723-727. (English edition.)

    Kuznetsov, V. V. (1973). Copepod fauna of the brackish water zone of the Laptev Sea. Nauchnfje dokladg vfjsshet ahkolfj, Biologicheskie nauki, 16(5), 22-24. (In Russian.)

    Lacroix, G. and Filteau, G. (1971). Les fluctuations quantitatives du zooplankton de la Baie-des-Chaleurs (Golfe du Saint-Laurent). 111. Fluctuations des copBpodes autres que Calanus. Natu~aliste Canadien, 98, 775-8 13.

    Laurence, G. C. (1976). Caloric values of some North Atlantic calanoid copepods. Fishery Bulletin, U.S. National Marine Fisheries Service, 74, 218-220.

    " Invertebrate Zoology ", Vol. 111.

    Kovalev, A. V. (1967).

    Kovalev, A. V. (1968).

    2, 527-609.


    Lawson, T. J. and Grice, G. D. (1977). Zooplankton sampling variability: controlled ecosystem pollution experiment. Bulletin of Marine Science, 27,

    Lebour, M. V. (1918). The food of post-larval fish. Joztrnal of the Marine Bio- logical Association of the United liingdom, 11, 433-469.

    Lebour, M. V. (1919a). Feeding habits of some young fish. Journal of the Marine Biological Association of the United Kingdom, 12, 9-21.

    Lebour, M. V. (1919b). The food of post-larval fish. I1 (1918). Journal of the Marine Biological Association of the United Kingdom, 12, 22-47.

    Lebour, M. V. (1920). The food of young fish. I11 (1919). Journal of the Marine Biological Association of the United Kingdom, 12, 261-324.

    Lebour, M. V. (1922). The food of plankton organisms. Journal of the Marine Biological Association of the United Kingdom, 12, 644-677.

    Lebour, M. V. (1923). The food of plankton organisms. 11. Journal of the Marine Biological Association of the United Kingdom, 13, 70-92.

    LeBrasseur, R. J., Barraclough, W. E., Kennedy, 0. D. and Parsons, T. R. (1969). Production studies in the Strait of Georgia. Part 111. Observations on the food of larval and juvenile fish in the Eraser River plume, Eebruary to May, 1967. Journal of Experimental Marine Biology and Ecology, 3,

    Lee, J. W. and Williamson, D. I. (1976). The vertical distribution and diurnal migration of copepods a t different stations in the Irish Sea. Journal of the Oceanographical Society of Japan, 31, 199-21 1.

    Lee, R. F., Takahashi, M., Beers, J. R., Thomas, W. H., Seibert, D. L. R., Koeller, P. and Green, D. R. (1977). Controlled ecosystems: their use in the study of the effects of petroleum hydrocarbons on plankton. J n Physiolo- gical Responses of Marine Biota to Pollutants (F. J. Vernberg, A. Cala- brese, F. P. Thurberg and W. B. Vernberg, eds.), pp. 323-342. Academic Press, New York, London.

    Legar6, J. E. H. and Maclellan, D. C. (1960). A qualitative and quantitative study of the plankton of the Quoddy region in 1957 and 1958 with special reference to the food of the herring. Journal of the Fisheries Research Board of Canada, 17, 409-448.

    Lishev, M. N. and Freimane, S. 0. (1970). The use of correlation analysis for studying the life cycle of Pseudocalanus elongatus Boek and Limnocalanus grimaldii Guerne. Trudg Bctltitskogo nauchno-issledouatelskogo instituta morskogo rgbnogo khozyattua i okeanogra$i, 4, 68-78. (In Russian.)

    Lock, A. R. (1968). A laboratory and field study of the role of temperature in vertical migrations of the copepod Pseudocalanus minutus. M.Sc. Thesis, Dalhousie University, Halifax, Nova Scotia.

    The effect of varying and constant temperatures on size of a marine copepod. Limnology and Oceanography,

    Loeblich, A. R., I11 (1976). Dinoflagellate evolution : speculation and evidence.

    Lowe, C. W. (1936). Observations on some Pacific diatoms as the food of copepods

    Lowndes, A. G . (1935). The swimming and feeding of certain calanoid copepods.



    Lock, A. R. and McLaren, I. A. (1970).

    15, 638-640.

    Journal of Protozoology, 23, 13-28.

    and fishes. Journal of the Biological. Board of Canada, 3, 12-19.

    Proceedings of the Zoological Society of London for 1935, 687-716.


    Mackas, D. and Bohrer, R. (1976). Fluorescence analysis of copepod gut con- tents and an investigation of die1 feeding patterns. Journal of Experimental Marine Biology and Ecology, 25, 77-85.

    Malikowski, W. and Ciszewski, P. (1962). The vertical migration of the Baltic zooplankton in a 24-hour cycle in the various seasons of the year. Rapport et ProcBs-verbaux des Riuniona. Conseil permanent international pour 1Exploration de la Mer, 153, 220-221.

    Marak, R. R. (1960). Food habits of larval cod, haddock, and coalfish in the Gulf of Maine and Georges Bank area. Journal du Conseil. Conseil permanent international pour 1Exploration de la Mer, 25, 147-167.

    Marshall, S. M. (1949). On the biology of the small copepods in Loch Striven. Journal of the Marine Biological Association of the United Kingdom, 28,

    Marshall, S. M. (1963). ;In Scottish Marine Biological Association Annual Report

    Marshall, S . M. (1973). Respiration and feeding in copepods. Advances in Marine

    Marshall, S . M. and Orr, A. P. (1 652). On the biology o f Calanw finmarchicus. VII : Factors affecting egg production. Journal of the Marine Biological Association of the United Kingdom, 30, 527-547.

    Marshall, S. M. and Om, A. P. (1954). Hatching in Calanzcsfinmarchicus and some other copepods. Journal of the Marine Biological Association of the United Kingdom, 33, 393-401.

    Marshall, S. M. and Orr, A. P. (1955). The Biology of a Marine Copepod Calanus finmarchicus (Gunnerus) . Oliver and Boyd, Edinburgh.

    Marshall, S. M. and Orr, A. P. (1966). Respiration and feeding in some small copepods. Journal of the Marine Biological Association of the United King- dom, 46, 513-530.

    Marehall, S. M., Nicholls, A. G . and Orr, A. P. (1934). On the biology of Calanus ]%&marchicus. V. Seasonal distribution, size, weight, and chemical composi- tion in Loch Striven in 1933, and their relation to the phytoplankton. Journal of the Marine Biological Association of the United Kingdom, 19, 793-827.

    Martens, P. (1972). Zur Charakterisierung der Kotballen von vier dominierenden Copepodernarten der Kieler Bucht. Diplomarbeit Thesis, Christian- Albrechts University, Kiel.

    Martens, P. (1975). uber die Qualitfit und Quantitlit der Sekundar- und Tertiar- produzenten in einem marinen Flachwasserokosystem der westlichen Ostsee. Doctoral Thesis, Christian-Albrechts University, Kiel.

    Larval mortality in marine fishes and the critical period concept. In The Early Life History of Fish (J. H. S. Blaxter, ed.), pp. 3-19. Springer-Verlag, New York.

    Mayr, E. (1963). Animal Species and Evolution . Harvard University Press, Cambridge, Massachusetts.

    McAllister, C. D. (1969). Aspects of estimating zooplankton production from phytoplankton production. Journal of the Fakheries Research Board of Canada, 26, 199-220.

    McLaren, I. A. (1963). Effects of temperature on growth of zooplankton and the adaptive value o f vertical migration. Journal of the Fisheries Research Board of Canada, 20, 685-727.

    4 6-1 22.

    for 1963, p. 19.

    Biology, 11, 57-120.

    May, R. C. (1974).


    McLaren, I. A. (1965). Some relationships between temperature and egg size, body size, development rate and fecundity, of the copepod Pseudocalanwr. Limnology and Oceanography, 10, 528-538.

    McLaren, I. A. (1966). Predicting development rate of copepod eggs. Biological Bulletin, 131, 457-469.

    McLaren, I. A. (1969). Population and production ecology of zooplankton in Ogac Lake, a landlocked fiord on Baffin Island. Journal of the Fisheries Research Board of Canada, 26, 1485-1559.

    McLaren, I. A. (1974). Demographic strategy of vertical migration by a marine copepod. American Naturalist, 108, 91-102.

    McLaren, I. A. (1976a). Inheritance of demographic and production parameters in the marine copepod Eurytemora herdmani. Biological Bulletin, 151,

    Ecological and genetical strategies in Pseudocalanw, production. International Council for the Exploration of the Sea, Plankton Committee, document C.M. 1976/L : 5, 1-8.

    McLaren, I. A., Woods, S. M. and Shea, J. R. (1966). Polyteny : a source of cryptic speciation among copepods. Science, New York, 153, 1641-1642.

    McLaren, I. A., Walker, D. A. and Corkett, C. J. (1968). Effects of salinity on mortality and development rate of eggs of the copepod Pseudocalanw minutus. Canadian Journal of Zoology, 46, 1267-1269.

    McLaren, I. A., Corkett, C. J. and Zillioux, E. J. (1969). Temperature adaptations of copepod eggs from the arctic to the tropics. Biological Bulletin, 137,

    Mednilrov, B. M. (1961). On the sex ratio in deep water Calanoida. Crz&meana,

    Menshutkin, V. V., Vinogradov, M. Ye. and Shushkina, E. A. (1974). Mathematical model of the pelagic ecosystem in the Sea of Japan. Oceanology, 14, 717- 723. (English edition.)

    Meshcheryakova, I. M. (1964). The quantitative distribution of plankton in the southeastern Bering Sea in the summers of 1958 and 1959. In Soviet Fisheries Investigations in the Northeast Pacific (P. A. Moiseev, ed.), Part 11, pp. 141-150 (Trudg Vsesoyuznogo nauchno-wsledovatelakogo tutu rgbnogo khozyaistva i okeanografii, 49, and Izvestiya Tilchookeanskogo nauchno-iaaledovatelskogo instituta rgbnogo kiiozyaistva i okeanograji, 51.) (In Russian.)

    Miller, A. (1969). Circadian rhythm of feeding of sprat (Clupea sprattus balticus) from the Baltic Sea. Izvestiya Akademii nauk &stonskoi SSR, Ser. biol., 18(1), 16-28. (In Estonian.)

    Minoda, T. (1967). Seasonal distribution of Copepoda in the Arctic Ocean from June to December, 1964. Record of Oceanographic Works in Japan, 9,

    Minoda, T. (1971). Pelagic Copepoda in the Bering Sea and the north-western North Pacific with special reference to their vertical distribution. Memoir8 of the Faculty of Fisheriea, Hokkaido University, 18, 1-74.

    Minoda, T. and Osawa, K. (1967). Plankton in the sonic scattering layer in the Okhotsk Sea, summer 1963. Bulletin of the Faculty of Fiaheries, Hokkaido University, 18, 9-19. (In Japanese.)

    Mironov, G. N. (1960). The feeding of plankton predators. 11. The feeding of sagittae. Trudg Sevaatopolskoi biologicheskoi stantsii. Akademiya nauk SSSR, 13, 78-88. (In Russian.)

    200-213. McLaren, I. A. (1976b).


    3, 105-109.



    Mori, T. (1937).

    Morioka, Y. (1973).

    The Pelagic Copepoda from the Neighbouring Waters of Japan , published by the author (reprinted 1964, the Soyo Co., Tokyo).

    The occurrence of cold-water calanoid copepods in the coastal waters of the Sanin District, Japan Sea. Bulletin of the Japan Sea Regional Fwheries Research Laboratory, 24, 77-84.

    Motoda, S. and Minoda, T. (1974). Plankton of the Bering Sea. In Oceano- graphy of the Bering Sea (D. W. Hood and E. J. Kelley, eds), pp. 207-241. Institute of Marine Science, University of Alaska, Fairbanks.

    Muhammad, M. (1965). Succinic acid dehydrogenase activity and oxygen uptake in zooplankton of Bras dOr Lake, Cape Breton Island, N.S. B.Sc. Hons. Thesis, Dalhousie University, Halifax, Nova Scotia.

    Mullin, M. M., Sloan, R. R. and Eppley, R. W. (1966). Relationship between carbon content, cell volume, and area in phytoplankton. Limnology and Oceanography, 11, 307-311.

    The chemical composition, volume, weight and size of the important marine plankton. Tokai regional fisheries research Laboratory, special Publication, 5, 12-24.

    Nguyen,V. K., Drzycimski, I. and Chojnacki, J. (1972). Feeding and food com- position of sprat from Bornholm Depth. Acta ichthyologica et piscatoria, 2, 55-66.

    Nilritine, B. (1 929). Les migrations verticales saisonnieres des organismes plank- toniques dans la mer Noire. Bulletin de 1Institut Oc&anographique, Monaco,

    Nival, P., Malara, G., Charm, R., Palazzoli, I. and Nival, S. (1974). &ude de la respiration et de lexcr6tion de quelques cop6podes planctoniques (Crus- tacea) dans la zone de remont6e deau profonde des c6tes marocaines. Journal of Experimental Marine Biology and Ecology, 15, 231-260.

    Norris, D. E. and Overstreet, R. M. (1976). The public health implications of larv a1 Thynnascaris nematodes from shellfish. Journal of &!ilk and Food Technology, 39, 47-54.

    Oberg, M. (1906). Die Metamorphose der Plankton-Copepoden der Kieler Bucht. Wissenschaftliche Meeresuntersuchungen der Kommission zur wissenschaf t- lichen Utatersuchung der deutschen Meere, Abt. Kiel, 9, 37-103.

    Ogilvie, H. S. (1938). The food of post-larval haddock with reference to the annual fluctuations in the haddock broods. Rapport et procbs-verbaux des rbunions. Conseil permanent international pour IExploration de la Mer.

    Ogilvie, H. S. (1953). Copepod nauplii (1). Fiches didentiJication du zooplancton. Conseil permanent international pour 1Exploration de la Mer, No. 50.

    Okada, S. and Taniguchi, A. (1971). Size relationships between salmon juveniles in shore waters and their prey animals. Bulletin oj the Faculty of Fisheries, Hokkaido University, 22, 30-36.

    Omori, M. (1965). The distribution of zooplankton in the Bering Sea and northern North Pacific, as obRerved by high-speed sampling of the surface waters, with special reference to the copepods. Journal of the Oceanographic Society of Japan, 21, 18-27.

    IZlstvedt, 0.-J. (1955). Zooplankton investigations from Weather Ship M in the Norwegian Sea, 1948-49. Hvalrddets Skrijter, 40, 1-93.

    Owre, H. B. and Foyo, M. (1967). Copepods of the Florida Current . Fauna Caribaea No. 1. Institute of Marine Science, University of Miami.

    Nakai, Z. (1955).

    26, NO. 540, 1-24.

    107, 57-66.

    A.M.B.-15 10


    Paffenhofer, G.-A. and Harris, R. P. (1976). Feeding, growth and reproduction of the marine planktonic copepod Psewlocalanus elongatus Boeck. Journal of the Marine Biological Association of the United Kingdom, 56, 327-344.

    Parsons, T. R. and LeBrasseur, R. J. (1970). The availability of food to different trophic levels in the marine food chain. I n Marine Food Chains (J. H. Steele, ed.), pp. 325-343. Oliver and Boyd, Edinburgh.

    Parsons, T. R., LeBrasseur, R. J. and Fulton, J. D. (1967). Some observations on the dependence of zooplankton grazing on the cell size and concentration of phytoplankton blooms. Journal of the Oceanographic Society of Japan,

    Parsons, T. R., LeBrasseur, R. J., Fulton, J. D. and Kennedy, 0. D. (1969). Production studies in the Strait of Georgia. Part 2. Secondary production under the Fraser River plume, February to May 1967. Journal of Experimen- tal Marine Biology and Ecology, 3, 39-50.

    Pavlova, E. V. (1975). On certain factors influencing rate of oxygen consumption of marine planktonic animals. Biologiya Morya, Kiev, 33, 73-78. (In Russian. )

    Comparison of the relative role of living and non-living organic matter in the nutrition of Pseudocalanus elongatus (Boeck). Biologiya Morya, Kiev, 34, 66-70. (In Russian.)

    History of investigations on plankton in the Norwegian Sea and the main results of Soviet investigations. Proceedings of the Royal Society of Edinburgh, B, 73, 267-278.

    Pearre, S. (1973). Vertical migration and feeding in Sagitta elegam V e r d .

    Pearse, A. S . (1936). Estuarine animals at Beaufort, North Carolina. Journul of the Elisha Mitchell Scientijk Society, 52, 174-222.

    Peterson, W. T. and Miller, C. B. (1975). Year-to-year variations in the plank- tology of the Oregon upwelling zone. Fishery Bulletin. Fish and Wildlye Service. United States Department of the Interior, 73, 642-653.

    Origin and classification of certain ecological types of feeding of Calanoid Copepoda. Biologiya Morya, Kiev, 33, 27-49. (In Russian.)

    Petipa, T . S., Sazhina, L. I. and Delalo, E. P. (1963). Vertical distribution of Zooplankton in the Black Sea. Trudfj Sevastopolskoi biologicheskol stanti% Akademiya nauk SSSR, 16, 119-137. (In Russian.)

    Petipa, T. S., Pavlova, E. V. and Mironov, G. N. (1970). The food web structure, utilization and transport of energy by trophic levels in the planktonic communities. In Marine Food Chains (J. H. Steele, ed.), pp. 142-167. Oliver and Boyd, Edinburgh.

    Pinhey, K. F. (1927). Entomostraca of the Belle Isle Strait Expedition 1923 with notes on other planktonic species. Part I. Contributions to Canadh Biology and Fisheries, 3, 179-234.

    Oxygen consumption by some planktonic organisms from the White Sea. Zhurnal obshchel biologii, 31, 450-458. (In Russian.)

    Feeding of the larvae and fry of the arctic cod (Boreogadus saida Lepechin) in the Barents and Kara Seas. Materia@ rfjbokhozyahtvenngkh issledovanii severnogo bamelna, 10, 20-27. (English transl. Bureau of Sport Fisheries and Wildlife, Narragansett, Rhode Island.)

    23, 10-17.

    Pavlovskaya, T. V. and Pechen-Finenko, G. A. (1975).

    Pavshtiks, E. A. and Timokhina, A. F. (1972).

    Ecology, 54, 300-314.

    Petipa, T. S. (1975).

    Polyakova, T. V. and Perueva, F. G. (1976).

    Ponomarenko, V. P. (1967).


    Ponomareva, L. A. (1954). On the feeding by euphausids of the Sea of Japan on copepods. Dodladg Akademii nauk SSSR, 98,153-154. (In Russian.)

    Popova, T. I. and Valter, E. D. (1965). On the elucidation of the life cycle of the fish nematode Contracaecum aduncum (Rudolphi, 1802) Baylis, 1920 (Ascari- data). I n Material9 nauchnoi konferentsii Vsesoyuznogo obshchestva gelmintologov, 1965 (V. G. Gagarin, ed.), Part 1, pp. 175-178. (English transl. Fisheries Research Board of Canada, no. 1797.)

    Porumb, F. I. (1971). Sur la biologie des copbpodes pblagiques des eaux rou- maines de la mer Noire. Cercetciri marine, 1, 129-147.

    Porumb, F. I. (1972). Contributions B la connaissance de la dynamique des populations et B la production de cop6podes dans les eaux roumaines de la mer Noire. Cercetiiri marine, 4, 57-94.

    Porumb, I?. I. (1973). Recherches sur le zooplankton au-dessus des fonds rocheux du littoral roumain de la mer Noire (aspect printanier). Rapport et procks- verbaux des rdunions. Commission internationale pour lexploratwn scientifique de la Mer Mdditerrande, 21, 533-535.

    Porumb, I. I. (1969). Contributions h16tude de la biologie de Sardina pilchardus sardina. La nourriture devant le littoral roumain de la mer Noire. Lucrcirile statiunii de cercetari marine Prof. Ioan Borcea , Agigea, 3, 101-112.

    Poulet, S. A. (1973). Grazing of Pseudocalanwr minutus on naturally occurring particulate matter. Linznology and Oceanography, 18, 564-573.

    Poulet, S. A. (1974). Seasonal grazing of Pseudocalanus minutus on particles. Marine Biology, 25, 109-123.

    loulet, S. A. (1976). Feeding of Psezldocalanus minutus on living and non-living particles. Marine Biology, 34, 117-125.

    Poulet, S. A. (1977). Grazing of marine copepod developmental stages on natur- ally occurring particles. Journal of the Fisheries Research Board of Canada,

    Poulet, S . A. and Chanut, J. P. (1975). Non-selective feeding of Pseudocalanus minutus. Journal of the Fisheries Research Board of Canada, 32, 706-713.

    Prbfontaine, G. and Brunel, P. (1962). Liste dinvert6br6s marins recueillis dans lestuaire du Saint-Laurent de 1929 B 1934. Naturaliste canadien, 89, 237- 263.

    Raymont, J. E. G. (1959). The respiration of some planktonic copepods. 111. The oxygen requirements of some American species. fimnology and Oceano- graphy, 4 , 479-491.

    Rakusa-Suszczewski, S. (1969). The food and feeding habits of Chaetognatha in the seas around the British Isles. Polskie archiwum hydrobiologii, 16,

    Reeve, M. R., Gamble, J. C. and Walter, M. A. (1977). Experimental observa- tions on the effects of copper on copepods and other zooplankton : Controlled Ecosystem Pollution Experiment. Bulletin of Marine Science, 27, 92-104.

    Robertson, A. (1968). The Continuous Plankton Recorder : a method for studying the biomass of calanoid copepods. Bulletin of Marine Ecology, 6 , 185-223.

    Robertson, S. B. and Frost, B. W. (1977). Feeding by an omnivorous planktonic copepod Aetideus divergene Bradford. Journal of experimental marine Bio- logy and Ecology, 29, 231-244.

    The vertical distributions and diurnal migrations of calanoid copepods collected on the SOND Cruise, 1965. I. The total popu- lation and general discussion. Journal of the Marine Biological Aasociation of the United Kingdona, 52, 277-314.

    34, 2381-2387.


    Roe, H. S. J. (1972).


    IZoquette, M. de la (1842). Notice annuelle des progrds des sciences g6ographiques et des travaux de la Soci6t6 de geographie pendant l'ann6e 1842. Bulletin de laSocidtd de Gkographie. Paris [2] 18, 397-621.

    Russell, F. S. (1934). The study of copepods as a factor in oceanic economy. Proceedings of the fifth. Pacific Science Congress, 1933, 3, 2023-2034.

    Russell, F. S., Southward, A. J., Boalch, G. T. and Butler, E. I. (1971). Changes in biological conditions in the English Channel off Plymouth during the last half-century. Nature, London, 234, 468-470.

    Ruud, J. T. (1929). On the biology of copepods off Mare, 1925-27. Rapport et Procbs- Verbaux des Reunions. Conseil permanent international pour I'Explora- tion de la Mer, 56, 1-84.

    Sars, G. 0. (1899). " An Account of the Crustacea of Norway ". Vol. 11. Bergen Museum, Bergen.

    Sars, G. 0. (1900). The Norwegian North Polar Expedition 1893-1896 (F. Nansen, ed.), Vol. I , 1-137.

    Sars, G. 0. (1903). " An Account of the Crustacea of Norway ". Vol. IV. Bergen Museum, Bergen.

    Savage, R. E. (1926). The plankton of a herring ground. Fishery Investigations. Ministry of Agriculture, Food and Fisheries, Ser. 2 , 9( l ) , 1-35.

    Savage, R. E. (1931). The relation between the feeding of herring off the east coast of England and the plankton of the surrounding waters. Fishery Investigations. Ministry of Agriculture, Food and Fisheries, Ser. 2, 12(3),

    Sazhina, L. I. (1968). On individual fecundity and duration of development of certain mass pelagic Copepoda of the Black Sea. Bidrobiologicheskit zhurnal, 4(3) , 69-72. (In Russian.)

    Sazhina, L. I. (1971). Fecundity of mass pelagic Copepoda in the Black Sea. Zoologicheskit zhurnal, 50, 586-588. (In Russian.)

    Sazhina, L. I. (1974). Rate of reproduction of pelagic Copepoda of the Black and Mediterranean Seas. I n " Biological Production of Southern Seas " (T. G. Kondratskaya, ed.), pp. 175-182. Naukova Dumka, Kiev. (In Russian.)

    Schnack, S. (1975). Untersuchungen zur Nahrungsbiologie der Copepoden (Crustacea) in der Kieler Bucht. Doctoral Thesis, Christian-Albrechts University, Kiel.

    Scott, A. (1922). On the food of young plaice (Pleuronectes platessa). Journal of the Marine Biological Association of the United Kingdom, 12, 678-687.

    Sewell, R. B. S. (1948). The free-swimming planktonic Copepoda. Geographical distribution. John Murray Expedition. Science Reports, B.M. (N.H.) , 8,

    Sewell, R. B. S. (1951). The epibionts and parasites of the planktonic Copepoda of the Arabian Sea. John Murray Expedition. Science Reports, B .M. (N .H. ) ,

    Dates of publication of the zoological and botanical portions of some French voyages. Part 11. Annuls and Magazine of Natural History, Ser. 7, 8, 491-494.

    Vertical movements of zooplankton during a solar eclipse. Nature, London, 227, 1156-1158.

    Size selectivity of the Gulf I11 and Bongo zooplankton samplers. Research Bulletin of the International Corn- mission for the Northwest Atlantic Fisheries, 8, 45-48.

    Part V, Crustacea. Scientific Results.



    9, 255-394. Sherborn, C. D. and Woodward, B. B. (1901).

    Sherman, K. and Honey, K. A. (1970).

    Sherman, K. and Honey, K. A. (1971).


    Shushkina, E. A., Kislyakov, Yu. Ya. and Pasternak, A. F. (1974). Estimating the productivity of marine zooplankton by combining the radiocarbon method with mathematical modelling. Oceanology, 14, 259-265. (English edition.)

    Skud, B. E. (1968). Responses of marine organisms during the solar eclipse of July 1963. Pishery Bulletin. Fish and Wildlije Service. United States Department of the Interior, 66, 259-271.

    Smayda, T. J. (1969). Some measurements of the sinking rate of fecal pellets. Limnology and Oceanography, 14, 621-625.

    Smith, L. R., Miller, C. B. and Holton, R. L. (1976). Small-scale horizontal distribution of coastal copepods. Journal of Experimental Marine Biology and Ecology, 23, 241-253.

    Smith, S. L. (1975). The role of zooplankton in the nitrogen dynamics of marine systems. Ph.D. Thesis, Duke University, Chapel Hill, North Carolina.

    Snodgrass, R. E. (1956). Crustacean metamorphosis. Smithsonian naiscellaneow Collections, 131(10), 1-78.

    Sournia, A., Cachon, J. and Cachon, M. (1976). Catalogue des especes et taxons infraspecifiques de dinoflagellbs marins actuels publies depuis la revision de J. Schiller. 11-DinoflagellBs parasites ou symbiotiques. Archiv fiir Protistenkunde, 117, 1-19.

    Steele, J. H. (1974). The Structure of Marine Ecosystems . Harvard Uni- versity Press, Cambridge, Massachusetts.

    Steele, J. H. and Frost, B. W. (1977). The structure of plankton communities. Philosophical Transactions of the Royal Society of London. B. Biological Sciences, 280, 485-534.

    Sullivan, B. K., Miller, C. B., Peterson, W. T. and Soeldner, A. H. (1975). A scanning electron microscope study of the mandibular morphology of boreal copepods. Marine Biology, 30, 175-182.

    Bioener- getics of migrations of Pseudocalanus elongatua (Boeck, Biologiya Morya, Vladivostolc, No. 6, 41-49. (In Russian.)

    Thompson, B. M. (1976). The biology of Pseudocalanus elongatus (Boeck). Ph.D. Thesis, University of East Anglia, Norwich.

    Tregouboff, G. and Rose, M. (1957). Manuel de Planctonologie m6diter- raneenne . I, 11. Centre National de la Recherche Scientifique, Paris.

    Urry, D. L. (1964). Studies on the food, feeding and survival of Pseudocalanus elongatus Boeck under laboratory conditions, with observations on other genera of Copepoda. Ph.D. Thesis, University of London.

    Observations on the relationship between the food and survival of Pseudocalanus elongatus in the laboratory. Journal of the Marine Biological Association of the United Kingdom, 45, 49-68.

    Ussing, H. H. (1938). The biology of some important plankton animals in the fjords of East Greenland. Meddelelser om Grenland, 100(7), 1-108.

    Valter, E. D. (1968). On the hosts of Contracaecum aduncum (experimental infection of animals with larvae of the parasite). I n Sedmaya sessiya Uchenogo soveta PO probleme Biologicheskie resursg Belogo morya i vnutrennikh vodoemov Karelii , Mart, 1968 goda. Tezisy dokladov. Petro- zavodsk. (English transl. Pisheries Research Board of Canada, no. 2031 .)

    Vane, F. R. (1952). The distribution of Blastodinium hyalinum in the North Sea. Challenger Society, 3(4), 23-24.

    Svetlichnyi, L. S., Zagoradnyaya, Yu. A. and Stepanov, V. N. (1977).

    Urry, D. L. (1965).


    Vervoort, W. (1965). Notes on the biogeography and ecology of free-living, marine Copepoda. Monographiae biologicae, 15, 381-400.

    Vinogradov, M. E. and Voronina, N. M. (1963). Distribution of plankton in the waters of the Equatorial Current of the Pacific Ocean, I. Distribution of biomass of plankton and horizontal occurrence of certain species. Trudg Instituta okeanologii. Akademiya nauk SSSR, 71, 22-59. (In Russian.)

    Vives, F. (1967). Los cop6podos plancthicos del mar Tirreno en septiembre y octubre de 1963. Investigacidn pesquera, 31, 539-583.

    Vives, F. (1970). Distribuci6n y migracih vertical de 10s cop6podos plancthicos (Calanoida) del SO. de Portugal. Investigacion pesquera, 34, 529-564.

    Vutieti6, T. (1957). Zooplankton investigations in the sea water lakes Malo Jezero and Veliko Jezero on the island of Mljet (1952-1953). Acta Adriatica, 6(4), 1-51.

    Vertical distribution of zooplankton in the bay Veliko Jezero on the island of Mljet. Acta Adriatica, 6(9), 1-20.

    The production of zooplankton in the Oslo Fjord in 1933-34, with special reference to the copepods. Hvalrcidets Skrqter, 21,

    Wiborg, K. F. (1944). The production of zooplankton in a landlocked fjord- the NordQsvatn near Bergen in 1941-42. Fiskeridirektoratets skrifter. Serie Havunders0kelser, 7(7), 1-85.

    Wiborg, K. F. (1948). Investigation on cod larvae in the coastal waters of northern Norway. Fiskeridirektoratets skrvter. Serie Havundersekelser, 9( 3),

    Wiborg, K. F. (1949). The food of cod (Gadus cullarias L.) of the 0-11-group from deep water in some fjords of northern Norway. Fiskeridirektoratets skrifter. Serie Havundersekelser, 9(8), 1-27.

    Investigations on zooplankton in coastal and offshore waters of western and northwestern Norway. Fiskeridirektoratets skrvter. Serie Havundersekelser, 11( l ) , 1-246.

    The copepods of the plankton gathered during the last cruise of the Carnegie. Publications, Carnegie Institution of Washington, No. 536.

    Wilson, C. B. (1950). Copepods gathered by the United States Fisheries Steamer Albatross from 1887-1909, chiefly in the Pacific Ocean. Bulletin. United States National Museum, 14(4) No. 100, 141-441.

    Winberg, G. G. (ed.) (1971). Methods for the Estimation of Production of Aquatic Animals . Academic Press, London, New York.

    Wing, B. L. (1975). New records of Ellobiopsidae (Protista (incertae sedis)) from the North Pacific with a description of Thalassomyces albatrossi n.sp., a parasite of the mysid Stylomysis major. Fishery Bulletin, U.S. National Marine Fisheries Service, 73, 169-185.

    With, C. (1915). Copepoda I. Calanoida Amphasoandria. Danish Ingo2f Expedi- tion, 3(4), 1-260.

    Woods, S. M. (1969). Polyteny and size variation in the copepod Pseudocalanus from two semi-landlocked fiords on Baffin Island. Journal of the Fisheries Research Board of Canada, 26, 643-556.

    Wright, R. R. (1907). The plankton of eastern Nova Scotia waters. An account of floating organisms upon which young food-fishes mainly subsist. Contri- butions to Canadian Biology, 1902-1905, 1-19.

    VuEetib, T. (1961).

    Wiborg, K. F. (1940).



    Wiborg, K. F. (1954).

    Wilson, C. B. (1942).


    Zagorodnyaya, Yu. A. (1974). Nutrition and migration o f Black Sea Pseudo- calanus elongatus (Boeck) in the winter period. Gidrobiologicheskii zhurnal, 10(6), 49-56. (In Russian.)

    Zagorodnyaya, Yu. A. (1975). Vertical migration and daily ration of the copepod Pseudocalanus elongatus (Boeck) in the Black Sea. Biologiya Morya, Kiev, 33, 11-17. (In Russian.)

    Zagorodnyaya, Yu. A. (1977). Estimation of the value of the die1 phytoplankton grazing by the copepod Psezdocalanus elongatus (Boeck) on the basis of a physiological calculation of its ration. Biologiya Morya, Kiev, 42, 95-1 00. (In Russian.)

    Zagorodnyaya, Yu. A. and Svetlichnyi, L. S. (1976). Die1 dynamics of the specific gravity and vertical distribution of Pseudocalanus elongatus (Boeck). Biologiya Morya, Kiev, 39, 39-42. (In Russian.)

    Mass occurrence of Pseudocalanus elongatus Boeck (Copepoda) in the coastal area of eastern Murman in 1956 and its causes. In " Hydrological and Biological Features of the Shore Waters of Murman ", pp. 127-135. AkademiyaNauk SSSR, Kol'skii Filial S. M. Kirova, Murmansk. (In Russian.)

    Zelikman, ?. A. (1966). Notes on composition and distribution of zooplankton in the southeast part of the Barents Sea in August-October, 1959. In '' Composition and Distribution of Plankton and Benthos in tho Southern Part of the Barents Sea ", T r u d g Murmanskogo morskogo biologicheskogo instituta, 11(15), 34-44. (In Russian.)

    Zelickman, E. A. and Golovkin, A. N. (1972). Composition, structure and pro- ductivity of neritic plankton communities near the bird colonies of the northern shores of Novayrt Zemlya. Marine Biology, 17, 265-274.

    Zelikman, ?. A. (1961).


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