[Advances in Marine Biology] Advances in Marine Biology Volume 11 Volume 11 || Respiration and Feeding in Copepods

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  • Adv. mar. Biol., Vol. 11, 1973, pp. 57-120

    RESPIRATION AND FEEDING IN COPEPODS

    SHEINA M. MARSHALL Institute of Marine Resources, University of California,

    and

    University Marine Station, Millport, Isle of Cumbrae, Xcotland

    I. Introduction . . .. . . . . . . . . . . 11. Respiration . . . . .. .. .. . . . .

    A. Effect of Crowding . . . . .. .. . . B. Effect of Time after Capture . . .. . . . . C. Variation with Season . . D. Relation to Size. . ..

    F. Effect of Temperature . . G . Effect of Salinity . . H. Effect of Pressure . . I. Effect of Oxygen Content J. Effect of Feeding . .

    A. Feeding Mechanisms . . B. Food . . . . .. C. Experimental Feeding . .

    IV. Conclusion . . . . . . . .

    VI. References . . . . . . . .

    E. Effect of Light . . . .

    111. Feeding . . . . . . . .

    V. Acknowledgements . . . .

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    I. INTRODUCTION Copepods are perhaps the most numerous animals in the world

    (Fig. 1). They form the bulk of most zooplankton hauls, they inhabit the vast expanse of the oceans and may be abundant to a depth of several hundred metres, so it is not surprising that they outnumber all other kinds of animal, even the insects, which may have more species but fewer individuals. Copepods are small, rarely exceeding 10 mm in length and usually much smaller ; many measure less than 1 mm. They are found in both fresh and salt water, near the coasts and in the open ocean, floating near the surface or crawling in the seashore sand. They are important in the sea because they are the main convertors of the phytoplankton into food suitable for higher organisms. For this reason a knowledge of their feeding habits and the amount of food they require is essential for an understanding of the processes of production in the sea.

    57

  • 58 SHEINA M. MBRSKALL

    FIQ. 1. Living copepods; different stages of Calanua helgolandicus. Photo: D. P. Wilson.

  • XESPIRATION AND FEEDING IN COPEPODS 59

    In recent years the breeding and rearing of marine pelagic copepods in the laboratory has led to greater possibilities for the accurate measurement of food ingested throughout the life cycle. Methods of measuring both feeding and respiration rates have also been improved and diversified. Nevertheless, the species of copepods used remain much the same. The large and easily obtainable genus Calanus heads the list among marine forms, Diaptomus and Cyclops among fresh- water forms. In the following pages the name Calanus (C. Jinrnarchicus (Gunnerus), C. helgolandicus (Claus), C. paci$cus Brodsky", C. hyper- boreus ( K r ~ y e r ) ) will occur over and over again, whereas observations on other genera are scattered and sporadic. It is not safe to conclude, however, that what is true of one species will necessarily be true of another, even closely related, species ; the behaviour of copepods differs from one species to another, even from one individual to another. There remains a great deal to be done before we have a body of in- formation about, for instance, the feeding and metabolism of predatory copepods comparable to that which we have now for a few CaEanus species.

    11. RESPIRATION

    Putter (1925) made some measurements on the respiration of copepods in bulk but, apart from a single experiment on Calanus hyperboreus (Ostenfeld, 1913), work on an individual species, Calanus Jinmarchicus, did not begin until the 1930s (Marshall et al., 1935; Clarke and Bonnet, 1939) ; it has now been extended to many different species of varying size from both salt and fresh water.

    The methods most often used have been estimations of oxygen consumption by either the Winkler method, the manometric respiro- meter or modifications of these. The polarographic oxygen electrode (Kanwisher, 1959; Teal and Halcrow, 1962; Nival et al., 1971) has more recently come into use.

    To obtain a measurable result in a short time (3-6 h) it is necessary to have a large number of copepods in a small bottle (Winkler) or, what in terms of the environment may come to the same thing, give each copepod only a small volume of water (respirometry). When a small number of animals are used and the time is prolonged, antibiotics must be added to prevent bacterial respiration interfering with the results. Penicillin cannot be used with the Winkler method since it reacts with the iodine in the final stages of the estimation, but strepto-

    * Following Fleminger, the form off the Californian coast is recognized as the species, C. pncijiczcs.

  • 60 SREINA M. MARSHmL

    mycin and chloromycetin have often been used in combination. The last, however, is injurious to some copepods (Berner, 1962) and was found to decrease feeding in Calanus (Marshall and Orr, 1961). Bernard (1963a) found that penicillin and streptomycin were injurious to cope- pods (she used them in high concentrations) but that sulfamethopyra- zine was harmless.

    Among the factors influencing respiration which have been considered are crowding, time after capture, season, size, light, temperature, salinity, pressure and the oxygen content of the water.

    A. Effect of crowding

    The effect of crowding has been considered by several workers with varying results. Some (Marshall and Orr, 1958 ; Comita and Comita, 1964; Conover and Corner, 1964) found that it made no appreciable difference; Satomi and Pomeroy (1965) found that it did. Zeiss (1963) made the most detailed experiments on the subject. To reduce the effect of any increased metabolites in a crowded culture he enclosed several copepods in short tubes, closed at each end with bolting silk, and suspended these in the experimental bottles. Using these the volume per Calanus finmarchicus seemed to make no significant difference to its oxygen consumption, although with Daphnia magna Straus there was a decided increase of oxygen uptake in this type of experiment. Increasing the number of Calanus in the experimental bottle did, however, decrease the oxygen consumption. This might be caused by the increased concentration of metabolites and Zeiss thought that the effect might vary between different types of crustaceans, relating it to their concentration in natural waters.

    B. Effect of time after capture

    It has often been observed that oxygen uptake is higher during the first hours after capture than subsequently (Marshall et al., 1935; Berner, 1962; Zeiss, 1963; Bishop, 1968) and to avoid this period experiments are often made on animals which have been kept 24 h or so in the laboratory. It is not certain whether the excitement of capture and handling raises oxygen uptake above normal, or whether under laboratory conditions there is a decline from normal values ; the first of these alternatives is usually assumed. S. K. Katona (personal communication) has stated that male Eurytemora aginis Poppe do not behave normally until one or two days after being isolated from a laboratory population into a separate vial.

  • RESPIRATION AND FEEDING IN COPEPODS 61

    C. Variation with season

    There is a marked seasonal variation in oxygen consumption (Fig. 2). From a low value in winter months there is a sharp rise (per individual) in spring (Marshall and Orr, 1958; Conover, 1959; Haq, 1967 ; Gaudy, 1968). Several factors may be responsible for this. In spring most copepods are at their maximum size and have a plentiful

    3 c

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    m

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    2 ( Oi

    0 :

    r , B p 0 ; s 5 8 01: 0"

    rn

    V

    c

    * 0 I(

    0 0:

    ( a 1

    \ O\ 0 1957

    -0

    I I I I I I I I I 0 .

    &- Feb I Mar I Apr I May I June

    ( c , l

    I 1 I I Mar Apr May June July

    I 1 I I Mar Apr May June July

    0-30

    m 5

    0 2 0 s r"

    0 10

    FIG. 2. Seasonal changes in oxygen consumption in various copepods. (a) Length of metasome in mm of ripe female CalanusJinmurchicus in 1957. (b) Oxygen consump- tion of ripe female C. Pnmurchicus in 1956 and 1957. (c,) oxygen consumption of PseudocaZunua elongatus (open circles), Temora Zongicornis (closed circles) and Acartia cZuusi (triangles) in 1956; (cii) Centropuges hamatus (open circles) Metridia Zucens (closed circles) and Oithona similis (closed triangles) all in 1956; 0. sirnilis (open triangles) in 1965.

  • 62 SHEINA M. MARSHALL

    food supply ; they are also reproducing actively. Temperature is rising although the maxima of temperature and respiration do not coincide, the first continuing to rise after the second has begun to decline. Oxygen consumption rises even when calculated per unit weight (Anraku, 1964a) so that it is not caused only by increased size (Fig. 2). It is less in pre-adult stages, less in males than in females and in immature than in ripe females. The proportion of actively respiring tissue in ripe females must, because of the mass of large eggs in the oviducts, be higher than in males or Stage V which contain relatively more fat, and this may be one cause. Ripe females in summer, however, do not consume so much oxygen as ripe females in spring. Vollenweider and Ravera (1958) observed that egg-carrying Cyclops strenuzls Fischer females used more oxygen than non-egg-carryin g, but Coull and Vernberg (1970) found consumption lower in gravid than in non-gravid females of Longipedia helgolandica (Klie) ; they attributed this to lessened activity. After the spring rise, consumption in ripe female Cabnus declines gradually to minimal winter values.

    D. Relation to size As one might expect the larger copepods use more oxygen but when

    uptake is expressed per unit of dry body weight the small forms are usually found to be more metabolically active. The same tendency is seen when the developmental stages of a single species are compared. Coull and Vernberg (1970), however, found that in benthic harpacticids, the activity of the animal mattered more than its size. Males and females have often been used together but, as mentioned above, their oxygen consumption is not always the same. The whole developmental range has been covered only in Calanus finmarchicus (Marshall and Orr, 1958), Acartia clausi Giesbrecht and A . latisetosa Kritcz (Petipa, 1966). The results are shown in Table I and Fig. 3, p. 69.

    E. Effect of light Full sunlight is lethal to Calanus as to many other marine animals

    (Huntsman, 1925). The effect of keeping C. finmarchicus at constant temperature in bright sunlight or even in shade out of doors on a bright day is to raise oxygen consumption considerably as well as to damage the animals. When the copepods are suspended in glass bottles in the sea (Marshall et al., 1935) the effect is not measurable below 2.5 m. Most respiration experiments are carried out in shade indoors or in darkness to avoid this effect, but Bishop (1968) states that sunlight had no effect on the oxygen consumption of some freshwater copepods (Diaptomus and Cyclops spp.).

  • TABLE I. OXYGEN C o m s ~ ~ ~ a r o x IN YOWNC STAGES or Acartia cla-i AND CaZanrur~Zmnaarchiclls

    Dura- Oxygen consumption Number Dry wt Tt:p' tion expt. pllcopepodlday pllmg dry wtlday Location Source

    ( h ) Range Mean Range Mean used Range Mean Species Stage

    Acartia clausi, P + 2 212 4.3-10.2 8.8 15-26 Most 24 0.9- 3.4 1.61 126- 525 214 \ \ 45 4.3- 5.9 5.0 23-25

    6 28 2.6- 5.4 4.6 7-24 A. clausi, small ? 95 1.P 1.9 1.7 2&26

    d 63 1 . P 1.6 1.5 24-26

    A. clausi, young C V 13 1.8 24-26

    large ?

    c I V (+ I11 and V) 16 1.0 25

    C I V and V 16 1.5 2 P 2 6 c I11 44 0.6 25-26 c I1 24 0.3 24

    C I and I1 25 0.6 25 N V and V I 24 0.1 24

    Calanus ? 386 (176) 10

    191 (242) 10 ?

    c3 213 (203) 10

    c v 519 (240) 10 c I V 73 10 c I11 70 10 c I1 36 10 C I 4 10

    Pnrnarchicus (June-Mar.)

    (Apr. May)

    N V I 4 N V 2 N I V 4 N I11 28

    I1 and I11 874 N 1-11 720

    N I1 and

    10 10 10 10

    10 10

    7-24 0.4- 2.7 1.28 89- 595 267 8-24 1.2- 4.6 2.87 211-1 295 753

    16-24 0.3- 2.0 0.91 153-1 770 632 24 0.7- 1.4 0.98 483- 950 676

    24 2.02 1050

    15 0.34 336 24 1.51 1008

    15-24 0.3- 1.0 0.67 1108 24 0.24 800 17 0.27 446 24 0.10 1056

    c.48

    c.48

    c.48

    c.48 19-48 19-48 19-48 19-48

    19-48 19-48 19-48 19-48

    19-48 19-48

    6.0-13.9 7.6 (43)

    10.3-17.8 15.1 (62)

    6.8-12.4 10.4 (27)

    2 4 7 9.3 5.5 (23) 1.4- 4.0 3.1 0.9- 1.9 1.4 0.5- 1.3 0.9 0.3- 0.9 0.6

    0.7- 0.8 0.2- 1.9 0.2- 0.8

    0.19 0.19

    0.07-0.09 0.08 0.05 0.05

    Black Sea

    Firth of Clyde

    Petipa (1966)

    Marshall and Orr (1958)

    Dry weights of Acartia calculated, according to Petipa, as 16% wet weight. Calanus dry weights in brackets averaged from 112 samples taken throughout the years 1933 and 1961-64. The averages of the two

    sets of samples agreed well.

  • TABLE 11. OXYGEN CONSUMPTION OF Calanus spp., FEMALE

    (7. jinmarchicus

    r - - 320 May 4-6 8-24 (15.2) 47.4 Gulf of Maine

    19 - 213 Aug. 7.5 8-48 9.1 42.4 Gulf of Maine 5 - 129 Aug., Dec. 8 24 2.9 24.5 Buzzards Bay

    and Cape Cod Bay

    and Cape Cod Bay

    5 - 152 May, June 8 24 7.2 50.0 Buzzards Bay

    386 2.37 176* June-Mar. 10 48 7.6 43.2* Firth of Clyde

    I 9 1 2.79 242* Apr., May 10 48 15.1 B2.4* Firth of Clyde

    5 - 141 Aug., Dec. 15 24 5.9 41.7 Buzzards Bay and Cape Cod Bay

    Bay

    5 - 136 May, June 15 24 9.0 62.3 Buzzards Bay and Cape Cod

    35 2.45 - Aug., Sept. corr. 3 19.2 - Firth of Clyde

    - - Aug. 20 4 18.8 - Firth of Clyde to 17

    240 i

    ca x Conover and E

    Conover, 1960 w Anraku, 1964a P

    5

    b

    Corner, 1968

    !d Anraku, 1964a

    E Marshall and Orr,

    Marshall and Orr,

    Anraku, 19648

    1958

    1958

    Anraku, 1964a

    Raymont and Gauld, 1951

    Marshall et aZ., 1935

  • I :: C. hyperboreus { - C. gracilis

    133

    158

    -

    80

    (204)

    (204)

    -

    - 2 332

    3 650

    -

    0ct.-Dec. 8 24 (6.8) 51.5

    Mar.-Sept. 8 24 (11.9) 75.5

    0ct.-Apr. 10 48 9.2 -

    Jan.-Feb. 15 4-8 8.7 108.5

    - 10 22-29 9.0 (44.1)

    - 15 22-29 11.7 (52.5)

    Dec. 3-7 - 13.5 - Apr. 3-7 - 27.5 - Apr. P 6 8-24 28.0 11.2

    Aug.

  • 66 SHEINA M . MARSHALL

    F. Effect of temperature

    Temperature is the factor which has perhaps been most studied, since it is continually varying in the environment (Gauld and Raymont, 1953; Comita, 1968; Anraku, 1964a). Oxygen uptake rises with rising temperature up to a maximum which varies from copepod to copepod and, in the same species, from one season to another. A temperature which is high enough to be injurious in winter can be endured without harm in summer (Halcrow, 1963; Anraku, 1964a; Gaudy, 1968). In some of these cases the copepod may belong to a different generation but some acclimatization can take place. Since experiments are usually made near the environmental temperature of the copepod being studied it is difficult to compare results, but Table I1 gives measurements for a number of Ca1anu.s species, a t varying temperatures from about 5-20C. The temperature-respiration curve is rarely linear, usually rising more steeply a t the upper end and falling as the lethal temperature is approached. Qlo varies considerably from 2.0 (Comita and Comita, 1964; Comita, 1965, 1968) and in one copepod, Pseudocalanus minutus (Kraryer) (Anraku, 1964a), varied from 1.33 in February to 3-72 in August. A factor which may affect the results in short-term experiments is that, after changing the temperature, " overshoot " may take place (Grainger, 1956, working on Diaptomus gracilis G. 0. Sars and other crustacea; Halcrow, 1963, working on Calanus), and there are minor oscillations before a steady state is reached.

    G. Effect of salinity

    The effect of lowered salinity has been measured in a few copepods. In Calanus finmarchicus (Marshall et al., 1935 ; Anraku, 1964a) and in Centropages hamatus (Lill jeborg) (Anraku, 1964a) oxygen uptake is lower in diluted sea water. I n Acartia tonsa Dana, a euryhaline species common in estuaries but found occasionally in hyper-saline lagoons, lowering the salinity increased oxygen uptake so that at 90% sea water it increased by 0.08 pl/mg dry wt and a t 30% sea water by 16-1 p1. Acclimatization for 24 h made little difference (Lance, 1965). The difference in behaviour may be because the euryhaline animal uses energy in osmotic regulation, whereas forms like Calanus are simply injured by the lowered salinity and oxygen consumption is therefore reduced (Schlieper, 1958), but this is questioned by Wolvekamp and Waterman (1960). Tide pool harpacticids can stand large variations in salinity, both high and low, but the effect on respiration is not known.

  • RESPIRATION AND FEEDING I N COPEPODS 67

    H. Effect of pressure The effect of change in pressure is most likely to be felt by vertically

    migrating copepods but few experiments have been made on this. Bishop (1968) studied a population of migrating copepods (three species of Diaptomus and three of Cyclops) in a freshwater lake and found that increasing pressure depressed respiration but that temper- ature, being higher in the upper layers, raised it ; the overall effect was towards a slightly higher respiration in the upper layers. Experiments showed that the animals were less affected by changes within their normal range than outside it. Macdonald et al. (1972) found that activity in several copepods was much reduced a t a pressure of 500 atm and this would affect oxygen consumption. Deep-living forms (Mega- calanus longicornis G. 0. Sars, Euaugaptilus magna (Wolfenden), Pareuchaeta gracilis (G. 0. Sars) and Pleuromamma robusta Dahl) were less sensitive than the surface-living Anomalocera patersoni Templeton. Napora (1964), however, found that, in the prawn Systellapsis, increased pressure led to increased metabolism and low temperature decreased it so that, within its normal range, metabolism remained fairly constant. On the other hand, Pearcey and Small (1968) found that pressure had no effect on the respiration of some larger migrating crustaceans (Euphausia, Thysanoessa, Sergestes).

    I . Effect of oxygen content The oxygen content of the water affects Calanus Jinmarchicus only

    when it falls very low ; below 3 ml 02/1 the respiration fell off rapidly (Marshall et al., 1935). Nevertheless, Calanus has been recorded at the limiting depth for plankton in the Black Sea where the oxygen content was only 1 ml/l (Nikitin, 1931). Some copepods, however, e.g., adults of Cyclops varicans (G. 0. Sars), can withstand complete anaerobiosis for as much as 36 h (Chaston, 1969). They probably build up an oxygen debt. Their recovery time depends on the hours of anaerobiosis ; after 1-15 h they take 5-8 min to recover; after 36 h, 6-10 h. Their normal respiratory rate is 11-5 pl O,/mg dry wt/day but after anaero- biosis it may rise to 23.5 p1 02. Caligus diaphanus Nordmann (Krish- naswamy, 1960) can also exist without oxygen for up to 9 h but its respiration was not measured.

    J. Effect of feeding The effect on respiration of feeding and starving copepods has been

    variously assessed. In general, respiration is lower in copepods living in water with an inadequate supply of food, than in the same species

  • 68 SHEINA M. MARSHALL

    living in a nutrient rich environment (Marshall and Orr, 1958, for Calanus in winter ; Haq, 1967 for Metridia longa (Lubbock) living in deep water in spring ; Comita, 1968, for Diaptomus siciloides Lilljeborg in barren pond water; Omori, 1970, for Calanus cristatus Kr0yer in deep barren water off Japan) but under experimental conditions feeding sometimes raises oxygen consumption (Conover, 1956 for Acartia ; Corner et al., 1965 for Calanus ; Raymont, 1959 for Centropages hamatus ; Comita, 1968 for Diaptomus leptopus Forbes and D. siciloides) and sometimes has no effect (Raymont and Gauld, 1951 for Centropages typicus Krcayer ; Marshall and Orr, 1958, for Calanus finmarchicus ; Raymont, 1959, for Pseudocalanus minutus ; Richman, 1964, for Diaptomus oregonensis Lilljeborg ; Comita (1 968) for D. oregonensis and D. clavipes Schacht). Ikeda (1971a and b) found that, under starvation conditions the oxygen consumption of Calanus cristatus rose for the first six days and then fell considerably. The variable results may depend on the general level of feeding and the length of time since the copepod has fed. Table I11 gives the oxygen consumption of a variety of copepods from different places and at different temperatures.

    Many attempts have been made to find a constant relationship between oxygen uptake and some measurement of the copepod body, length, surface area, or weight. The equations most often used are: R = kL2 or R = kW0'667 where R is metabolic rate (or respiration) and k is a constant of proportionality. Surface area is taken to vary as L2, and volume (or weight) as L3, and oxygen uptake is assumed to occur through the surface of the copepod. The usual measurement of length is that of the metasome and it is not likely to give a very accurate estimate of total surface area since it omits the limbs; indeed it has been found that in a copepod with a shape of metasome different from a cylinder (e.g., Temora, Raymont and Gauld, 1951) a different value of L must be used. Conover (1959) has found that oxygen consumption is directly related to weight, although later (1960) he used log-trans- formed data.

    Many authors have measured respiration in copepods of varying size and have calculated regression equations either directly (Conover, 1959; Berner, 1962) or after a log transformation (Raymont and Gauld, 1951 ; Gauld and Raymont, 1953; Conover, 1959, 1960; Comita, 1965, 1968 ; Comita and Comita, 1964), when the " simple " equations become log R = log k + 2 log L and log R = log k + 0.667 log W . The figures calculated from experiments vary considerably among themselves and the regression coefficient in the second may vary in different species (Conover, 1969, 1968) from 0.622-1.06. The average value of b for seven species of small neritic copepods was 0.86 (Conover,

  • RESPIRATION AND FEEDING IN COPEPODS 69

    E:

    U

    5

    0 m

    1959), for four species of marine copepods (Raymont and Gauld, 1951) 0.73 and for seven freshwater diaptomid species (Comita, 1968) 0.658, compared with the theoretical 0.667. It may also be lower than the theoretical figure, e.g. in Metridia longa and M . lucens Boeck (Haq, 1967) it was 0-37-0.48, varying with temperature. Figure 3 shows the oxygen consumption of most of the copepods of Table 111, selected to cover a wide range of size especially those which have been measured a t different seasons and in different areas. The regression equation for this graph is Y = 2.44 - 0.36 X

    *

    + *o\o 0 + + \ I -

    I I I I I 2 3 4

    log dry weight in pg

    01

    FIG. 3. Oxygen consumption of a variety of copepods according to weight. + Culaaus spp: Observations by Conover, 1956, 1959, 1960, and Conover and Corner, 1968; 0 by Nival et al., in press; by Anraku, 1964a, Comita, 1968, and Petipa, 1966.

    In measuring the oxygen consumption rates of a number of zoo- plankton crustaceans (including eight species of copepods) Conover (1960) found that carnivores had a higher rate than herbivores. This is understandable since they must move more actively than herbivores to capture their prey. Raymont (1959) had already noted that Tortanus discaudatus (Thompson and Scott) (a carnivorous copepod) had a higher respiration than would fit into the equation he calculated for seven mainly herbivorous species.

    Temperature having a considerable effect on respiration, Comita (1968) calculated a regression equation which includes this variable as well as length or weight for freshwater diaptomids. Conover (1968) has used this equation and compared the results with his measurements

  • 70 SHEINA M. MARSHALL

    of oxygen uptake in ten marine copepods. On the whole the equation over-estimated oxygen consumption, sometimes considerably, but statistically the two sets of values were not significantly different. As Conover (1960) points out, it is not realistic to expect close agreement, since the above equations have not been proved to apply to copepods in more than a rough way. Nor can the curves drawn from the cal- culated regression equations have much predictive value, since the metabolic rate of copepods is affected not only by their size but by their shape, feeding habits, reproductive state, and by seasonal change.

    The main object of these measurements was to assess the food requirements of the copepods and to compare them with the food available in the sea. For this purpose the amount of food required has sometimes been expressed as the percentage of body weight used daily. This differs, of course, with the substrate used and may be expressed in terms of fat, protein, or carbohydrate, the first giving the lowest percentage while the others are about equal. For Calanus Jinmarchicus, Marshall and Orr (1958) found that values varied from 3.9% (fat) to 7.2% (protein or carbohydrate) body weight per day for females at 10C in summer and 2-8-6.7% a t 10" in winter. For Stage V such values were 2.3-3.1% and 1.4-3.3%. For Calanus cristatus Stage V in summer the value was 7% (Ikeda, 1971b). The values per unit wt, however, are higher for small copepods because of their greater metabolic rate (see p. 62; they have been estimated a t 10C (Marshall and Orr, 1966) for Pseudocalanus elongatus Boeck as 4.3-11.9% ; for Centropages hamatus as 6.9-14.5% ; for Temora longi- cornis (Muller) 3.0-6*4% ; for Acartia clausi 4.8-10-2% and for Oithona similis Claus 10.0-21.17(0. Petipa (1966) gives some estimates for Acartia, calculated on wet weight and at considerably higher temper- atures which will partly account for the higher figures, e.g. for A. clausi adults at 16"C, 13.6%; at 20.5", 15.6-25.2%; a t 25", 16.3%; and for A. latisetosa a t 25-26"C, 17-3-61-5y0. These figures cover only main- tenance ; they do not allow for reproduction and such extra energy as is required for vertical migration. It is to this last that Petipa ascribes most of the difference between the amount of food calculated as necessary from oxygen consumption figures and the much greater amount she has estimated from measurements of food eaten in the sea.

    It is interesting to compare, in individual experiments, the food calculated as necessary from oxygen consumption with that actually taken in; this has been done in several cases apart from Petipa's results. Gaudy (1968) working on Centropages typicus in the Mediter- ranean found that the number of Skeletonema cells eaten was just enough to cover respiratory needs, but not growth or reproduction.

  • RESPIRATION AND FEEDING IN COPEPODS 71

    In experiments on Netridia (Haq, 1967) the phytoplankton food taken in was much below respiratory requirements. With Artemia nauplii as food, M . lucens easily satisfied requirements but M . longa did not. Diaptomus oregonensis (Richman, 1964), although having a very low filtering rate in experiments with Chlorella, did cover its respiratory needs. These results perhaps indicate only that a copepod in the laboratory does not always behave normally.

    111. FEEDINQ It is now generally recognized that most pelagic copepods are neither

    purely herbivorous nor purely carnivorous but can change from one mode of feeding to the other. Thus the mainly herbivorous Calanus hyperboreus will choose Artemia nauplii from a mixture of Artemia and smaller diatoms (Mullin, 1963) and the mainly carnivorous Anomalocerapatersoni is occasionally found with a few diatom cells in the gut (Gauld, 1966), although it is possible that these have entered in the gut of its prey. Nevertheless, the difference between carnivorous and herbivorous forms is not confined to their food but extends to the structure of their limbs, their larval development, and their oxygen consumption.

    Of the three main groups of copepods (parasitic forms are not dealt with here) the Calanoida have been most studied and the Cyclo- poida come next; comparatively little is known about the food and feeding of the Harpacticoida. The Calanoida are, however, the most important since they are the main primary consumers in the sea and so form an essential link in its productivity.

    A. Peeding mechanisms

    There are three types of swimming in the Calanoida-the rapid leaps and twirls of an escape reaction, a smooth gliding motion, and a jerky progression. All the appendages can be used in swimming but the antennules are used only for the rapid escape movements and the thoracic feet and the urosome for this and for changing direction. The antennules are set on the first segment of the head region (cephalosome) and take no direct part in feeding. The mouth parts follow in sequence : antennae, mandibles, maxillules, maxillae and maxillipeds. Of these, the most important in swimming are the antennae and it is differences in these which make the difference between smooth and jerky progression. In Calanus and in most families of the Calanoida (Gauld, 1966) the exopod and endopod are of about equal length and each is provided with a fan of long plumose setae. In Calanus, the limb not only beats to and fro, providing the forward propulsion, but has also a rotatory movement ;

    A.P.B.-II 4

  • 72 SHEINA M. M A R S U L

    exopod and endopod beat alternately so that the backward thrust is continuous and smooth gliding results (Fig. 4a). In Rhinculunus msutus Giesbrecht and Eucalunus bungii Giesbrecht, however, their smooth motion must be attained in a different way for in the antennae of both the endopod is much shorter than the exopod. Huloptilis ucutifrons Giesbrecht, however (Bernard, 1963a), continually moves its appendages but stays in one place. In Culunus the mandible and maxillule are also provided with fans of long plumose setae and they also beat to and fro, the former with a slight rotatory movement, but their movements are smaller and less effective. This kind of swimming produces swirls and eddies below and on either side of the moving copepod (Fig. 5 ) and it is these eddies which are used in filter-feeding.

    FIQ. 4. Swimming strokes of copepod antennae. (a) 1-6, Culunus; (b) 1-4, Acartiu. Propulsive strokes indicated by heavy, and recovery strokes by light arrows. (After Gauld, 1966.)

    The maxillae with their screens of long plumose setae form the walls of a filtering chamber whose roof is the body wall and whose floor is formed of the tips of the first pair of swimming feet and according to Gauld (1966), one group of maxillary setae (Figs 6, 9). The maxillary screen is the main filtering surface and remains more or less stationary but the outward sweep of the long setae at the tip of the maxillipeds reinforces the eddy formed by the swimming movements and water is drawn through the screen so that particles are filtered off on the maxil- lary setae. As the maxilliped finishes its stroke, the long maxillulary setae begin their return movement, and also help to draw water through the filter. The spines on the basal endites of the maxillule scrape off the food particles and push them towards the mouth (Gauld, 1966). Figure 6 is a diagram, according to Cannon (1928) of the basic water currents and limb movements in feeding.

  • RESPIRATION AND FEEDING IN COPEPODS 73

    Although they have not been examined in such detail most of the copepods with a smooth gliding motion probably produce similar eddies and have a similar filtering mechanism. Those which swim jerkily produce no such eddies and must collect their food in a different way. In them the exopod of the antennae is shorter than the endopod and both work together in the propulsive stroke ; the paddle-like action which ensues gives them their jerky motion (Fig. 4b). Acartia, Alzomalocera, Labidocera, Parapontella and Canducia swim like this. It

    FIQ. 5. Swimming vortex of Calanus, from the side. (After Gauld, 1906.)

    was Conover (1956) who first observed that in Acartia the maxillae were not held stationary but were used as a '' scoop net " below the mouth to catch diatoms and other small food particles. In Acartia end several more of this type of copepod the maxillipeds are reduced in size, set close together, and so block up the posterior end of this scoop net, which can not only be used for automatically gathering food but also to capture individual larger or active organisms sensed by the copepod (Fig. 7). Gauld (1966) suggests that it is so used not only in the copepods which normally feed this way but in the Calanus-type

  • 74 SHEINA M. MARSHALL

    copepods which usually hold their maxillae stationary. Petipa (1965b) observed such movements in Calanus.

    By a close examination of the maxilla itself a good deal can be learned about the kind of food a copepod depends on. The limb consists of a basal part (coxa and basipod), usually with four endites,

    FIQ. 6. Diagram of water currents on the left and limb movements on the right in the anterior region of CaZanus, with acknowledgements to Cannon, 1928. The endopod of the antennae, the mandibular palps and the distal part of the maxillules have been removed. The position of the swimming feet is indicated by the shaded area inside the dotted line. On the right side of the figure the limb movements are indicated, on the left the water currents. ant.1, antennule; ant.2, antenna; ant.2 ex.r., rotation path of tip of exopod of antenna; f.ch., Glter chamber; lbr, labrum; mdb, mandible; mxl, maxillule; mxl. ex.r., rotation path of tips of setae of maxillulary exite; mx2, maxilla; mxpd, maxilliped; mxpdx., rotation path of tip of maxilliped; s.ch., suction chamber.

    each bearing long setae and a 5-segmented endopod, also bearing long setae. The long aetae are all aetulate and the distance apart of these setules gives some idea of the size of particle the a t e r can retain. It has been examined in Calanus (C. finmarchicus, C. helgolandicus, C. plumchrus Marukawa), Neocalanus robustior (Giesbrecht), Pseudo- calanus elongatus, Euchaeta wovendeni A. Scott, Temora longicornis,

  • 75 RESPIRATION BND FEEDING IN COPEPODS

    Centropages hamatus, Acartia clausi, A . tonsa and Oithna similis (Ussing, 1938 ; Conover, 1956 ; Heinrich, 1963 ; Gauld, 1964 ; Marshall and Orr, 1956, 1966). The distance is variable, being usually least near the base of the setae and at the proximal part of the limb, greatest near the tip of the setae and on the most distal of the endopod setae. In Calanus jinmarchicus (Fig. 8) it varies from 2-12 p on the basal setae

    FIQ. 7. Maxilla and maxilliped of Acartia, showing relative size and position. (After Gauld, 1966.)

    and from 2-22 p on the endopod setae. It is slightly greater in C. helgolandicus than in C. jinmarchicus (in the Clyde sea area, where the first is slightly larger than the second) and slightly less in early cope- podid stages than in Stage V and adults, as Heinrich has also observed. She finds the smallest gap between setules to be 1.5 ,u in both tropical and boreal species although there are more Calanids with this minimal distance in the tropics. The Euchaetidae, Aetidaeidae, Pontellidae and Augaptilidae have only spinules and coarse, widely-set setules.

    In the smaller copepods the distance is, rather surprisingly, very much the same as in Calanus. Centropages hamatus is an exception for

  • 76 SEEINA M. MARSHALL

    the setules are from 5-17 p apart on the basis and from 17-30 p on the endopod. In Long Island Sound (Conover, 1956) Acartia seems to be an exception too for the distance apart in A . tonsa was 7-8 p, that in A . clausi 4-5 p in summer, 9-10 p in winter. No seasonal variation was found in the Clyde sea area where the range of distances was consider- ably greater.

    FIG. 8. Maxilla of Cdanw, finmarchicus, showing the setm and their setulation.

    The maxillary setae are not all of one type. In Calanus (Fig. 8) there are 29, all but one on the anterior edge, and they can be divided into several groups (Marshall and Orr, 1956; Gauld, 1966). For the f i s t group, consisting of the posterior seta and one small smooth seta at each end of the filtering screen, no function has been suggested. The next group, all long, regularly setulose setae, 10 on the basis and

  • RESPIRATION AND FEEDING IN COPEPODS 77

    7 slightly longer, on the endopod, form the main filtering screen. There is a shorter seta on each of the four basal endites with irregular setules pointing in all directions, and five shorter setae on the endopod, one with close opposite setules like a feather and four irregularly setulate. Gauld (Fig. 9) states that the five irregular setae on the endopod, together with some on the basis of the maxilliped, spread out to form a floor to the filtering chamber and that the shorter setae on the basipod spread out behind the main filter and form a screen which prevents large particles (over 40 p) from reaching the filter. These he supposes to be caught by using the maxilla, or at least the long setae on the endopod as a scoop net as in Acartia (Fig. 9). Conover (1966a) suggests a different function for some of these setae. He supposes

    f \

    FIG. 9. Diagram of filter apparatus and use of maxillary setae according to Gauld, as seen from below. (a) feeding swirl; (b) guard setae; (c) filter setae; (d) distal setae; (e ) outflowing current produced by (f), maxillulary exite.

    that they interdigitate with four setae on the base of the maxilliped and are used for orientating large particles and pushing them forward. Interdigitation will of course reduce the size of the filtering mesh and this in itself will affect feeding. Petipa (1965b) describes Calanus helgolandicus as making gathering or grasping movements with the maxillae to catch large diatoms and Conover (1966a) observed that individuals of C . hyperboreus, fed only on large cells, did not filter these but actively seized them. In Calanus the long setae on the basis and endopod are of nearly equal length but in many copepods those on the endopod are decidedly longer and in carnivorous forms such as Candacia, Labidocera and Tortanus (Fig. 10) are modified into strong grasping organs. Wickstead (1962) says that in deep-water carnivorous copepods the long setae of maxillae and maxilliped form a continuous screen and are used in sweeping movements below the mouth, rather

  • 78 SHEINA Bf. MARSHALL

    as in Acartia. In the Scolecithricidae and Diaixidae the end segments of the maxilla carry '' sensory " setae quite different from ordinary setae (Sars, 1903; Arashkevich, 1969) but their function has not been described.

    Even in species which are only partly carnivorous one or two of the maxillary setae are often much stronger than the rest and provided with stronger setules which are probably used for grasping (Fig. lOb,c). Such setae can be found on the first segment of the endopod in T e m r a longicornis and Centropages (C. hamatus, C. typicus) and on the last endite of the basis in Acartia clausi. Centropages typicus has been seen to seize other copepods with these long grasping setae (Anraku and Omori, 1963). When this difference between the setae of basis and endopod exists, the former are much more finely setulate than the latter and are still used for filtering.

    Jsrgensen (1966) suggests that cells below 30-50 p are filtered whereas larger cells are seized raptorially. Gauld (1964) too, believes that particles larger than 40 p are not filtered but excluded'from the filter chamber by the short maxillary setae. If a Calanus is filter- feeding in a suspension of cells of mixed size, with the maxilla held stationary and a current passing through it, it is difficult to believe that it will frequently interrupt this process to seize individual cells with the endopod. Indeed Conover (1968) has found that in Calanus hyperboreus " encounter )' feeding and " filter ') feeding are separate and mutually exclusive processes, the one used depending partly on the cells available and partly on what the Calanus has been feeding on previously. Further observations on this point in other copepods would be useful.

    The mandible, maxillule and maxilliped are also important in feeding. The cutting edge of the mandibular gnathobase varies greatly in different species (Beklemishev, 1959; Anraku and Omori, 1963; Arashkevich, 1969). In herbivores the teeth are blunt and strong, suitable for crushing (Fig. 10a); in carnivores they are sharp and pointed (Fig. 1Oc). In some species and on some teeth a layer of silica is deposited during development (Beklemishev, 1959). There are no siliceous crowns on the teeth of the adults in those species which do not feed as adults (Calanus plumchrus, C. cristatus). The functions of the maxillule have already been mentioned. The maxilliped is very variable in size, sometimes much larger, sometimes much smaller than the maxilla in both herbivores and carnivores. It may have long set* which help in producing currents (CaZartus), it may block the back of the scoop net (Acartia) (Rg. 71, or it may form part of it (Euchaeta, Wickstead, 1962). In carnivorous species it is often very large having

  • / I -

    ' / / '

    FIQ. 10. The mandible, maxilla and maxilliped of three types of copepod. (a) mainly herbivorous, Calanua $inmarchicus; (b) omnivorous, Centropages hamatus; (c) carnivorous, Tortanua discaudatua. Details of the structure of the gnathobase are also shown at twice the magnification of the main figure.

  • 80 SHEINA M. MARSHALL

    a reflexed endopod furnished with strong grasping setae or spines (Pareucheta norvegica Boeck). Figure 10 shows the mandible, maxilla and maxilliped in copepods of three types, herbivorous, omnivorous and carnivorous.

    Even copepods which usually feed by filtering, e.g. Pseudocalanzcs (Cushing, 1955) and Calanzcs (Conover, 1964; Petipa, 1966b) have been seen to seize individual organisms or to follow them when presented on the point of a needle. It is not known what sensory apparatus enables them to do this. Cushing (1959) supposed it to be contact with sensory setae on the antennules but it has been found that the removal of these limbs makes no difference to normal feeding (Mullin and Brooks, 1967 in Rhincalanus w u t z c s ; Conover, 1964 in Calanus hyperborezcs). Conover (1966a) has found that organisms have to be within a circumscribed area around the ventral side of the mouthparts of C. hyperboreus before they can be sensed and captured. Arashkevich (1969) and Arashkevich and Timonin (1970) deduced the type of feeding in a number of copepod families from an examination of the mouthparts, particularly mandible, maxillule, maxilla and maxilliped. Particular stress was laid on the kind of teeth on the mandibular gnathobase and the setulation of the other limbs. In some species these deductions were confirmed by an examination of gut contents and by experimental feeding with 14C labelled food. Most species id a family were found to feed in a similar way. It was concluded that the Calanidae, Eucalanidae, Paracalanidae and the genus Pseudo- calanus were filter feeders, the Euchaetidae, Phaennidae, Augaptilidae, Heterorhabdidae, Candaciidae and the genus Bathycalanus were predatory and the Aetidaeidae, Scolecithricidae, Metridiidae, Luci- cutidae and deep water genera of the Pseudocalanidae were mixed feeders. Temora discaudata Giesbrecht was put among the filter feeders but the genus Temora is usually considered to be omnivorous.

    Most cyclopid copepods are benthic (or parasitic) and not much work has been done on their food and methods of feeding in the sea. Fryer (1957a, b), however, has studied food and feeding in a number of freshwater species and finds that most eat both animal and vegetable food but that some are mainly herbivorous, others mainly carnivorous. The structure of the mouthparts was, nevertheless, similar in all those examined. The antenna has no exopod and swimming is therefore of the jerky type. It is noteworthy that Fryer describes, in Eucyclops macruroides (Lilljeborg), a slow swimming movement carried out by the first pair of swimming legs only, the others being flexed back and held motionless. The mandible is a simple limb, the shaft bearing the masticatory process being twisted so that the teeth actually lie inside

  • RESPIRATION AND FEEDING M COPEPODS 81

    the mouth. The basal part bears two extremely long setae whose function is not mentioned. The maxillules, maxillae and maxillipeds are similar in that, although there are a few setae proximally, most of the armature is concentrated distally where there are numerous strong, stout, spines used for grasping and holding. There is nothing in the way of a filtering screen even in herbivorous forms. The strong spines on the maxillule are the main organs used for seizing the food ; those on the maxilla and maxilliped help in holding and manipulating it and the mandibles tear it and push it into the oesophagus. The species studied in most detail were Macrocyclops albidus (Jurine), M . fuscus (Jurine) and Acanthocyclops viridis (Jurine).

    Oithona similis is a marine pelagic cyclopid and although the mouthparts show no filtering screen they differ considerably from those of the freshwater cyclopida just described. The setae of the maxilla and maxilliped and the setules on them are few in number but some of them are stout and strong. Gauld (1966) says that the two limbs act together as a scoop net but that the great distance apart of the setules means that the copepods can take only comparatively large diatoms and flagellates. Marshall and Orr (1966) found that they could eat only fairly large phytoplankton organisms and very little even of them ; the very stout setae suggest that they may aIso capture animal food.

    Little is known about feeding in the Harpacticoida. Somd of those living interstitially in sand are said to scrape off the diatoms, flagellates and bacteria attached to the grains. Larger forms, e.g., Asellopsis intermedia (T. Scott) living in burrows in the sand may do the same (Lasker et al., 1970). Others filter suspended material (Nicholls, 1936). Two species, Miracia efferata Dana and Macrosetella gracilis (Dana), have been described (Bjilrnberg, 1966) living pelagically, the first clinging to lumps of detritus, the second to the Oscillatoria (Tri- chodesmium) filaments on which it feeds. The adults and copepodites are attached by hooks on the maxilla and maxilliped, the nauplii by hooks on the antennules. Morphologically adapted for benthonic existence, Macrostella gracilis thus contrives to live in the plankton by finding a floating substratum.

    Specialized structures axe occasionally to be found on the feeding limbs. In the copepods which bore into the tissues of seaweeds some of the setae on the antennule are modified into structures like fir-cones with small spines instead of scales (Harding, 1964; Green, 1968). No function has been suggested for these. On the setae of the maxilla and maxilliped of some of the Euaugaptilidae (Sewell, 1947) there are, instead of setules, curious button-like structures carried on

  • 82 SHEINA M. MARSHALL

    a small peduncle. These have been fully described for Centraugaptilzcs by Krishnaswamy et al., (1967). The flattened part of the button is crescentic in shape and contains fibres but there is no cellular structure discernible. They are covered with cuticular material, possibly originating from the cuticle of the seta. The authors suggest that, although they lack any muscular tissue, they may be used as adhesive discs for holding prey close to the mandibles. Sewell has described the gradual transition from setules to buttons in various members of the genus Euaugaptilus.

    Few copepods have been observed feeding naturally and in only a few has there been a critical examination of the function of the mouthparts in the living animal. The figures of these in Sam (1903- 1918) great treatise on Copepoda make a fascinating study but much work is needed before we can understand the function of the astonishing variety of form displayed there.

    Gauld (1959) has studied feeding in a number of copepod nauplii. In both calanids and cyclopids (Oithona) the process is much the same. In the calanids there are two types of swimming, a sudden leap with the help of the antennules and smooth gliding without their use. In Oithna the antennules are always used and swimming is jerky as in the adult. In all the nauplii observed the antennae were the main propulsive and the mandibles the main food-collecting limbs. This remains true throughout nauplius life for, although the other limbs appear in sequence during nauplius development up to the first and second pair of swimming legs, they are weak and not functional. No feeding currents were produced (contrary to what had been described by Storch in 1928). The mandible at the beginning of its backward stroke forms a curved surface facing back and slightly downwards. It rotates as it moves and finishes up as a concave surface facing the ventral surface of the body, with the long setae lying behind the mouth and forming a basket in which small particles are trapped. Probably the spines on the basal segment push the food forward and the basal spines of the antennae push it into the mouth.

    The specialized harpacticids (Thalestris rhodymeniae (Brady) and Dactylopusioides macrolabris (Claus)) have nauplii with a, strongly developed gnathobase on the antenna (Harding, 1954 ; Green, 1958) with which they excavate their burrows in seaweeds.

    B. Food Only a few observers have been able to watch copepods actually

    feeding in more or less natural conditions, usually when swimming freely in small dishes in the laboratory.

  • RESPIRATION AND FEEDING IN COPEPODS 83

    Conover (1966a) has watched Cabnus hyperboreus (sometimes slowing down their movements with tricaine methane sulphonate) bring a large Coscinodisczcs cell into its filter chamber, orientate it and push it against the mouth, then break it up with the mandibles and ingest it. The copepod might also bring a faecal pellet to the mouth, taste it and reject it. In the rejected pellets the peritrophic mem- brane had been torn open. Individual animals showed great variation- some rarely lost a cell once seized, others had difficulty in manipulating it so as to bring it to the mouth while some brought it to the mouth and then discarded it. Cushing (19%) has seen a Pseudoculanus take a Bid- dulphia sinensis Greville almost as big as itself, break it, and filter off some of the contents. Petipa (196Sb) has watched Cabnus helgo- landiczcs catch large organisms with grasping movements of the maxilla and maxillule and then break them up with maxillulary spines and mandibular teeth. It will also follow a Coscinodiscus held on the point of a needle and gradually withdrawn.. She says that only about one third of the contents of a Coscinodiscus cell was ingested. Nicholls (1935) has watched the interstitial harpacticid copepods Longipedia scotti G. 0. Sars and L. minor (T. and A. Scott) lying on their side or back and filter feeding. Diatom chains were passed into the mouth end-on but Phaeocystis colonies were first broken up by the mandibles ; much was lost.

    On the whole copepods are too small and move too rapidly for these sorts of observation to be easy. The food ingested in nature has been studied mainly by examination of the gut contents or of faecal pellets. Of course, what is recognizable is only the indigestible remains of the food; soft-bodied organisms, or those without a skeleton, such as naked flagellates and ciliates are more rarely seen and, since they are an important part of the plankton, they are probably an important part of the food. On the whole the gut contents of a filter-feeding copepod are a good reflection of the microplankton present in the sea at the time it was feeding.

    Among the factors important in deciding whether or not an organism is a suitable food, are size and shape, availability and chemical composition.

    1. Size of food In marine pelagic herbivores the size of the food ranges from small

    flagellates such as coccolithophores and silicoflagellates up to large diatoms and dinoflagellates such as Coscinodiscus, Rhizosolenia, and Biddulphia or Ceratium, Peridinium and Noctiluca (the last an important food for CaZanus in the Black Sea, Petipa, 1960) which may

  • 84 SHEINA M. MARS-

    be up to several hundred p in length or diameter. The skeletons of the smaller organisms are found complete in the gut and faecal pellets. Those of the larger are in fragments, having been broken by the mandibular teeth, after which the copepod can ingest the pieces or suck out the contents. Spines are sometimes considered to act as a deterrent (Harvey, 1937; Parsons et al., 1967) but Chaetoceros spp. were often found in the gut of Ca1anu.s by Marshall (1924) and so were the centres of the radiolarian Acanthonia, with the spines broken off and lying separately. Petipa (1965b) distinguishes between " brittle " and " horny '' spines. The former, such as those of diatoms and radio- larians are easily broken by the mandibular teeth but the latter, such as the horns of Ceratium are tough, tend to get entangled in the setae of the mouthparts, and are not easily dealt with. However, Ceratium is occasionally eaten (Petipa, 1964c, 1965b ; Butler et al., 1970) although not so much as one would expect from its abundance in the sea.

    In herbivorous copepods there are definite limits to the size of food taken. The minimum depends partly on the distance apart of the setules on the filtering screen (see p. 75) which means that cells only a few p in diameter will pass through the mesh. Calanus and other I copepods have nevertheless been kept alive in the laboratory on small flagellates of about this size (Raymont and Gross, 1942), but only when the concentration of cells was much above that found in natural waters, so that the filter was probably clogged up. In experiments using as food diatoms and flagellates labelled with 32P Marshall and Orr (1955a) found that cells smaller than about 10 p were less efficiently filtered than larger cells and that the minute Nannochbris oculata Droop (2-4 p), Chromulina pwilla Butcher (1-3 p ) , Dicrateria inornata Parke (3-5.5 p ) and Chlorella stigmatophora Butcher (2-5 p) were hardly eaten at all (see also p. 95). Bernard (1963a) states that Mediterranean copepods are smaller and eat, not diatoms, but small flagellates and coccolithophores which may be found as deep as 1000 m. Their filtering appendages were not examined.

    The upper limit of size is much vaguer. As already mentioned, it may in filter feeding be about 50 p but when grasping or pursuing individual particles may be much larger. Petipa (1965b) says that the eggs of the rockling are bulky and too awkward to deal with, but Calanus helgolandicus will bite the heads and tails off the slow moving larvae. Many other instances are known of copepods attacking fish larvae (Davis, 1959 ; Lillelund, 1967 ; Lillelund and Lasker, 1971).

    There are only scattered observations on the food of carnivorous copepods but it seems to be mostly crustacean. Pareuchaeta norvegica, for instance, lives on copepods, mainly Calanus (Lowndes, 1935).

  • RESPIRA!ITON AND FEEDZNQ IN OOPEPODS 85

    Those copepods living below 1 000 m are held to be mainly carnivorous (Chindonova, 1959 ; Vinogradov, 1962 ; Wickstead, 1969, 1962) but few observations have been made on gut contents. Copepods living at 400 to below 1000 m off Zanzibar and in the Northwest Pacific, and aarrying out active vertical migration into the euphotic zone at night, were mixed feeders ; the remains of diatoms, radiolarians, foraminiferans tintinnids, jelly-fish, copepods, copepod nauplii, and other crustacea and of polychaete worms, were found in the guts. It is possible that copepods living below 1 000 m undertake diurnal vertical migration so as to feed on these copepods above that level during the day; and the faecal pellets of the latter may play a part in deep water food chains. Bernard (1963a) considers that Scolecithricella dentata (Giesbrecht), Phaenna spinifera Claus, Oncuea media Giesbrecht and Xanthocalanus are really benthonic copepods and feed in bottom sediments, being found in the plankton only because of their vertical migrations. Vinogradov states that the number of deep zooplankton is correlated with the amount of surface plankton above it and postulates a " ladder of migrations " whereby food is carried from the surface into deep water (Wheeler, 1967). Wickstead has also studied the habits of copepods belonging to the Oncaeidae and Cyclopidae living off Zanzibar. They live in the surface plankton during the day but disappear at night because they have attached themselves to their prey-appendi- cularians, salps, euphausiids, penaeids, or post-larval fish. It is easy to understand how such behaviour passes over into parasitism.

    Young stages of marine pelagic herbivores on the whole eat much the same as the adults but are less able to catch large or thick-shelled organisms. In all nauplius stages only the antennule, antenna, and mandible are functional (see p. 82) and the teeth of the last do not acquire their siliceous crowns until an early copepodid stage (Petipa, 1964b). The filtering screen in early copepodites is of much the same mesh-size as in adults but the mouthparts are weakly developed. Marshall and Orr (1966) found that, in Calanus jinmarchicus, Coscino- discw centralis Ehrenberg (about 100 p in diameter) could not be taken till copepodite 11. Ditylum brightwellii (West) (20-60 p diameter) not before copepodite I, and Prorocentrum micans Ehrenberg (43-27 p) not till nauplius V. Nauplius I11 could eat Prorocentrum triestinum Schiller (10 x 14 p) and Cricosphaera elongata (Droop) Braarud (18-30 x 12 p). Nauplius I and I1 did not feed. Mullin and Brooks (1970a) found that Calanus pacijicus nauplii could not be reared on Ditylum brightwellii whereas Rhincalanus nasutus nauplii could.

    The larvae of carnivorous copepods are sometimes herbivorous, e.g., Acunthocyclorps viridis (Smyly, 1970), Eucheta japonicu Marukawa

  • 86 SHEINA M. MARSHALL

    (Lewis, 1967), and Labidocera aestiva Wheeler (A.. Barnett, personal communication) but are more often non-feeding, or carnivorous like their parents. The eggs of carnivorous copepods are laid with a large quantity of yolk and as a consequence the numbers laid are fewer than with herbivores. The nauplius stages are passed through quickly and at a temperature of 166C copepodite I is reached in four days by Pareuchaeta norvegica, Euchaeta marina (Prestandrea), Candacia armata Boeck and C . bipinnata Giesbrecht (Bernard, 1965). The nauplii may not feed at all. This is a faster rate of development than in herbivorous or omnivorous copepods so far investigated, e.g., 12-14 days in Calanus jinmarchicus (Marshall and Om, 195513) and 18-22 days for Pseudocalanus elongatus at 15OC (Katona and Moodie, 1969). Bernard also states that the eggs and nauplii have a different astaxanthine cycle from that of the herbivores and tend to be deeply coloured. She thinks that the lack of feeding in the nauplius stages may be because their limbs would be too feeble to catch living prey. Lewis (1967) and Lewis and Ramnarine (1969), however, suggest that in Euchaeta japonica both pre-feeding and feeding nauplii rely on the absorption of dissolved organic matter.

    Matthews (1964) studied the development of several copepods from depths of 150-240 m in a Norwegian fjord. These were Chiridiw armatus (Boeck), Bradydius bradyi Sars, Aetideus armatus (Boeck), and Xanthocalanus fallax G. 0. Sars all living near the bottom and all carnivores or scavengers. In the first, and probably also the second, at a temperature of 10-12OC eggs took 8-10 days to hatch and a further 1 P 1 6 days to reach nauplius IV, from which they moulted direct to copepodite I. Aetideus armatus lives slightly further from the bottom and its eggs took three days to hatch and the nauplius 12 days to complete the normal six nauplius stages. In Xanthoculanw fallax also, the nauplii do not feed and the number of stages may be reduced. Matthews suggests that the lack of feeding may be because the nauplii live below the photosynthetic zone or because the breeding periods of the copepod do not coincide with times of phytoplankton abundance.

    It must be remembered that nauplius feeding has been investigated in only a very few species, even among those in which the adult food is known and that the stage at which feeding begins varies greatly. It is, for instance, nauplius I in Pseudodiaptomus coronatus Williams (Jacobs, 1961) and Euterpina acutifrons (Dana) (Bernard, 1963b), nauplius I1 in Rhincalanus nasutus (Mullin and Brooks, 1967) and Pontellopsis regalis (Dana) (Bernard, 1968), nauplius I11 in Calanus finmarchicus, C . helgolandicus (Marshall and Orr, 1956) and Euchaeta

  • RESPIRATION AND FEEDING IN COPEPODS 87

    japonica (Lewis and Ramnarine, 1969), nauplius V in Calanus hyper- boreus (Conover, 1962), and copepodite I in Pareuchaeta norvegica and numerous other carnivorous copepods (Matthews, 1964).

    Among freshwater copepods, diaptomids, which are mostly herb- ivorous (Vetter, 1937; Fryer, 1954; Frey, 1965), and cyclopids, which are both herbivorous and carnivorous, have been most studied. It is sometimes assumed that, at least in fresh water, size of body is correlated with size of food and that whereas small copepods can eat only small food particles, large copepods can eat both small and large (Hutchinson, 1951 ; Cole, 1961 ; Brooks and Dodson, 1965). This hypothesis has not often been supported by examination of the food, but Fryer (1954) on one occasion in Lake Windermere, found the larger Diaptomus laticeps Sars coexisting with the smaller D. gracilis and feeding almost exclusively on Melosira italica Kutz while Diaptomus gracilis was eating much smaller algae and detritus. He states (19578) that cyclopid herbivores are smaller than cyclopid carnivores. Bernard (1963b) also says that small Mediterranean copepods eat small food organisms. It is doubtful if this is generally true for marine copepods; there are certainly many exceptions, e.g. the large and mainly herbivorous Calanus hyperboreus and Eucalanus bungii, the small but more pre- daceous Acartia and Candacia. In lakes and ponds there is a variety of habitats possibly not found in the open ocean, but in the example given above the diaptomids were taken together in open water. However, in a study of the vertical distribution of tropical cyclopid copepods, the samples being taken within narrow depth limits, Zalkina (1970) found that each species occupied a slightly different range of depth and migrated at a slightly different time and he thought that these differences separated off ecological niches. Mullin and Brooks (1970a) on the other hand suggested that a separation through food preferences might occur in nauplii rather than adults, e.g. Rhincalanus nauplii can exist on larger diatoms than can Calanus nauplii (see p. 85).

    The food of the freshwater herbivores consists of diatoms, desmids, filamentous algae, various flagellates and detritus. Some animal food, e.g. rotifers, is often found as well (Fryer, 1957a; b). The herbivores studied by Fryer were Eucyclops agilis (Koch, Sars), E. macruroides, E. rnacrurus (Sars), E. gibsoni (Brady), E. dubius (Sars), Acantho- cyclops bisetosus (Rehberg), A. languidus (Sars) and Microcyclops spp. It is a curious fact that the enzymes of the cyclopid gut seem unable to deal with the gelatinous sheath in which the algae are often encased. This is sometimes torn open by the mouthparts and the contents pushed or sucked into the gut, which is very expansible, but if the alga is ingested whole the cells or the filament go through undigested, as do

  • 88 SHEINA M. MARSHALL

    the naked chloroplasts of Spirogyra. Fryer suggests that their food is so abundant that a considerable loss does not matter.

    The food of carnivorous cyclopids consists of other copepods, cladocerans, insect larvae, oligochaetes and rotifers. The algae often found were probably present in the guts of the prey. Cyclopids are also well known to attack fish and fish larvae; Mesocyclops edax (S. A. Forbes) (Davis, 1969) will jump at passing fish larvae and bite pieces out of the fins and tail. Fryer studied the species Macrocyclops albidus, M . fuscus, Acanthocyclops viridis, A. vernalis Fischer, Cyclops strenuus, C. abyssorum Sars and Mesocyclops leuckarti (Claus). Where several species occupied the same habitat their food preferences differed. Thus, when the first three were living together, M . albidus took more calanoid and other copepods, M . fuscus more chydorid cladocerans and A . viridis larger organisms such as dipteran larvae and oligochaetes.

    Cyclopids are voracious and it has been estimated (McQueen, 1969) that one species, Cyclops bicuspidatus thomasi Forbes, could eat nearly one third of the standing stock of both Diaptomus spp. and the other Cyclops spp. present in Marion Lake, B.C. Another estimate (Confer, 1971) was that Mesocyclops edax, feeding selectively on Diaptomus floridamus Marsh in two lakes in Florida could remove 1% and 6% of the standing crop per day.

    There has been much discussion about the use of bacteria as food for both marine and freshwater planktonic copepods. In the free state bacteria are usually scarce and could not form an important part of the diet ; in any case, they would slip through the filtering mesh of most herbivores. It is only when aggregated into particles large enough to be retained that they could be ingested in quantity. Detritus particles are often colonized by bacteria and indeed the chief value of detritus as food may lie in its bacterial content. Experimental feeding of Calanus on bacteria has long been unsuccessful (Fuller and Clarke, 1936) but more recently (Butler et al., unpublished observations) bacterial film seemed to have some nutritive value. Zhukova (1963) considers that even in pelagic copepods bacteria form an important part of the diet. Seki and Kennedy (1970) have calculated that through the winter in the Strait of Georgia the clumps of aggregated bacteria were enough to sup- port growth and maintenance of the filter feeding zooplankton. This, however, is a coastal phenomenon and would not apply to open waters.

    In fresh water there are many records of bacteria in the food of copepods (e.g., Nauwerck, 1962). Diaptomus gracilis and D. graciloides are said to be unable to ingest dispersed but to ingest aggregated bacteria (Monakov and Sorokin, 1960 ; Malovitskaya and Sorokin, 1961a, b, quoted in Jmgensen, 1966) ; the nauplii, however, can ingest

  • RESPIRATION AND BEEDING IN UOPEPODS 89

    and grow on natural concentrations as can the nauplii of non-filter- feeding cyclopids.

    In bottom-living and interstitial harpacticids bacteria may form an important part of the diet (Noodt, 1957; McIntyre, 1969). Some- times, e.g. in Tachidius discipes Giesbrecht, sand grains are held and turned while diatoms and bacteria are scraped off; in other species, e.g. Nitocra spinipes Boeck, they were found to be necessary in the diet (Muus, 1967). Gray (1968) has described how Leptastacw con- strictus Lang finds sands with bacteria more attractive than sands without and can even distinguish between different species of bacteria. On the other hand, Perkins (1958) found that among 70 benthic harpacticids examined most had diatoms and " detritus '' in the gut. When kept in a wheat infusion containing protozoa'and bacteria they lived for some months but did not reproduce.

    Something must be said about the use of detritus as food. In winter in temperate and polar regions most of the particulate organic matter in suspension in sea water is in the form of detritus and because at that time food in the form of phytoplankton is very scarce it has often been suggested that detritus is what the herbivores mainly feed on in winter. Cowey and Corner (1963) analyzed detritus from the English Channel and found that the composition of its organic matter showed much the same spectrum of amino acids as that found in phytoplankton and in copepods. Jmgensen (1955, 1962, 1966) has calculated that in ocean water somewhat less than half the primary production turns eventually into detritus and has a turnover time of about 2-7 months. Since this detritus will be made up of degraded chlorophyll, remains of chitinous and siliceous exoskeletons, and the indigestible remains of plants and animals from faecal pellets, it is not likely to be very nutritious : however, bacteria aggregate on suspended particles and vitamins are absorbed on them (Shiraishi and Provasoli, 1959) so that their value will be enhanced. Detritus has often been described in the gut of copepods but this is usually only a name for any unrecognizable debris found there.

    Paffenhafer and Strickland (1970) have experimented on feeding Calanus pacificus on several types of detrital material, senescent diatom culture, natural detritus filtered from deep ocean water and faecal pellets from Calanus itself. The filtration rate on a fresh growing culture of Chuetoceros cwrvisetus Cleve was 60 ml/copepod/day, that on senescent Ditylum and Skeletonemu cultures 31 and 54 ml respectively, that on faecal material 10 ml/day. Natural detritus was not filtered a t all. They did not attempt to find out if this intake was of any nutritional value. Later, however Paffenhofer (personal communication)

  • 90 SHEINA M. MARSHALL

    raised Calanus from copepodite I11 to adult on a diet of faecal pellets. Similar experiments (unpublished), using as a criterion of nutritional value the production of eggs by ripe female C. finmarchicus or an increase in weight or nitrogen content, led to the conclusion that detritus was of little or no food value except possibly in the form of faecal pellets or bacterial aggregates.

    The organic flakes produced from dissolved organic matter in the sea by the action of rising bubbles or turbulence (Riley, 1963) were used as a food for Artemia nauplii (Baylor and Sutcliffe, 1963), but its role in the sea as a whole is not sufficiently well known to assess its value as cope- pod food. The value of detritus as a winter food remains to be proved.

    It should be mentioned that copepods have occasionally been successfully fed on completely unnatural diets. Bernard (1963a) has used a commercial preparation, Infusyl, made from dried infusorian culture with added carotene, to feed pelagic and carnivorous copepods, and Egami (1951) fed Tigriopus sp. on dried and pulverized mulberry leaves. Nauwerck (1962) has kept Eudiqtomus gracilis, normally a nanoplankton feeder, alive and reproducing on a diet of ground-up zooplankton, mainly Diaptomus.

    2. Selection of food It has become clear from the work of many observers (Harvey,

    1937; Anraku and Omori, 1963; Mullin, 1963; Petipa, 1959, 19f35b; Mullin and Brooks, 1967 ; Haq, 1967 ; Richman and Rogers, 1969) that, altogether apart from the efficiency of the filtering process, copepods feeding in a mixture of different sizes of food organisms tend to take the larger. Harvey observed this first with Calanus helgolandicus feeding in a mixture of Ditylum, a large, and Chaetoceros, a small, diatom. He found by cell count that only Ditylum was eaten and, further, that the volume of water filtered was greater than when the animals were feeding in cultures of small cells only. Many experiments have since been made on feeding mixtures of different sized food organisms to copepods but it is not always clear that the foods offered were equally available to the copepods. Numbers of cells varied greatly and the volumes offered of large and small cells were not always equated ; apart from volume, cells may differ from each other in ways (e.g. specific gravity, reaction to light, or mobility) which make it dificult to assess their availability.

    Mullin (1963) observed that size of the food organism was one of the factors which affected the feeding of Calanus; C. helgolandicus would select the longest chains of Asterionella and C. hyperboreus the broadest cells of Rhizosolenia. Later, Mullin and Brooks (1967) found

  • RESPIRATION AND FEEDING IN COPEPODS 91

    that the early stages of Rhincalanus nasutus, reared in the laboratory, usually selected the larger of the foods offered and that the size of the particles selected increased with the growth and increasing size of the copepod. Mullin (1966) examined a number of mostly omnivorous copepods from the Indian Ocean and fed them on mixtures of Artemia nauplii (9 x lo6 p3 in volume) and one or more of three different sized diatoms, the largest being Coscinodiscus perforatus Ehrenberg (8 x lo5 p3), the next Thalassiosira juviatilis Hustedt (3.6 x lo3 p 3 ) and the smallest Cgclotella nana Hustedt (1.6 x lo2 p 3 ) at concentrations of 1, 2, 2 000 and 18 000/ml respectively. Females, males and a few copepodid stages of the following copepods were used : Neocalanus gracilis (Dana), Nannocalanus minor (Claus), Rhincalanus cornutus (Dana), Eucalanus attenuutus (Dana), Pleuromamma abdominalis (Lubbock), P. xiphias (Giesbrecht), P. gracilis (Claus), P. piseki Farran, Euchirella bella Giesbrecht, E . curticauda Giesbrecht, Chirundina indica Sewell, Scolecethrix dame (Lubbock), Lophothrix latipes (Scott), Ewhaeta marina, E. acuta Giesbrecht, Labidocera acutifrons (Dana), Candacia aethiopica (Dana) and Haloptilus ornatus (Giesbrecht). Several of these were found with diatoms and microplankton (e.g. radiolarians, forminiferans) in the gut and had the mouthparts of herbivores, i.e., stout, blunt mandibular teeth and long setulose setae on the maxilla, but in spite of this most selected Artemia nauplii from the experimental mixtures. Euchirella spp., Euchaeta spp., Labidocwa, Candacia, and Haloptilus have carnivorous mouthparts and ate few or no diatoms from the mixtures. The results were variable, however, and the copepods did not always behave in the same way; Euchirella bella (Copepodite 111) in one experiment, for instance, took consider- able quantities of diatoms. When Artemia was absent from the mixture feeding was poorer and some copepods ate nothing. It should be noted that Brooks (1970) thinks that Artemia nauplii, because they are so slow moving, should be considered as large inert particles rather than as animal prey and if this is so not all the above copepods are necessarily carnivores.

    Haq (1967) also presented a variety of foods of different sizes (Artemia nauplii, large and small diatoms and flagellates) to two species of Metridia, one ( M . lucens) more predatory than the other ( M . longa). As a rule more of the larger than of the smaller cells were taken by both. Artemia nauplii were selected particularly by M . lucens which could eat up to 34 a day.

    Petipa (1965b) says that when Calanus helgolandicus is feeding in a mixture of phytoplankton (1-30 large cells and 1 000-8 000 small cells/ml) it will select the large cells, but when feeding actively in the

  • 92 SHEINA M. MARSHALL

    sea it does not show much discrimination but takes most of what predominates in numbers or biomass. She has also measured selectivity in laboratory experiments. The index of selectivity is based on the ratio of a given cell to the total number of cells in the environment before and after feeding, and varies from - 1 to + 1. The Calanw helgolandicus used selected for Melosira, Cerataulina and Coscinodiscw, against Nitzschia seriata Cleve and Prorocentrum micans, and were neutral to Chaetoceros curvisetus. P. micans has, however, been found by other workers and by herself to be a good food for Calanw. She also found that Acartia clazcsi in a mixture of cells of different sizes removed 6-8 p flagellates slowly, and 16 p (Gymnodinium) and 39 p (Prorocen- trum) cells rapidly. Anraku and Omori (1963) also found that in Centropages typicus, the rate of filtration was lower for small particles than for large (see below, however, p. 93).

    Perhaps the most convincing observations on size selection are those made by Richman and Rogers (1969) who used one species of diatom, Ditylum brightwellii, in rapidly dividing cultures so that what was offered to the copepods (Calanus pacijcus) was a choice between two sizes of the same food species. Filtering rate was measured by cell counts made three times during the 24 h of the experiment. Diatom cell division was synchronized and when it occurred during the dark, filtering rates showed no light-dark change for single cells, but a marked increase for double (dividing) cells during the dark. In un- synchronized cultures filtering rates for single cells remained constant, but those for double cells was correlated with their increase in number. This is taken to mean that the increased rate of feeding often found at night is caused by phytoplankton cell division rather than by a diurnal feeding rhythm. When the number of double cells is below 20%, filtering rate remains constant, above this it rises exponentially with increase in their number up to about 40% and above this becomes constant again. The authors conclude from their results that although single cells are caught by passive filtration the larger cells are actively hunted and grasped.

    There are a few observations which point in the opposite direction. Curl and McLeod (1961) noted that, when a tow-netting rich in a mixture of diatoms (Skeletonema, Guinardia, Chaetoceros, Rhizosolenia, Thalassionema and Nitzschia) was set aside, the copepods in it (mainly Pseudocalanzcs and Acartia tonsa) rapidly reduced the numbers of Skeletonema leaving the larger Rhizosolenia to increase and become the dominant form. McQueen (1970) found that Diaptomus oregonensis filtered greater volumes of small than of larger food cells.

    Some experiments on size selection were made by Marshall and Orr

  • RESPIRATION AND FEEDINQ IN OOPEPODS 93

    (1955a) using culture labelled with 32P to feed female Calanw. In one of two parallel sets of experiments a large radioactive diatom (Ditylurn) was used in a mixture with a small non-radioactive one (Chaetoceros). An attempt was made to equate the volume of the two foods offered. In the second set the small diatom was radioactive, the large one not. If the Calanw had selected large cells the radioactivity of its body after feeding should have been higher in the first than in the second set but the average of the six or seven Calanus used in each set was very much the same.

    Conover (1966a), working on Calanus hyperboreus, found that they tended to take the food they had been feeding on even when larger particles were presented. Marshall and Orr (1955a) also noted that if two sets of C. Jinmrchicus were fed on different species of food and then put into a mixture of the two, they did for a short time, eat more of the food to which they were accustomed.

    The species mentioned up till now have been marine and pelagic but selection has also been observed in freshwater diaptomids and cyclopids, although here the habit seems to have developed so that species living in the same habitat would not interfere with one anothers feeding (see p. 88). This involves selection of small as well as large particles. Lowndes (1935) found that Diaptomus gracilis would feed off the bottom even when the water was rich in a green flagellate RirchnerelEa or with Volvox and Ceratium. However, the gelatinous covering or the horny spines of the unwanted species may account for this preference. Rylov (1930), quoted in Jorgensen (1966), found that Diaptomus coeruleus Fischer removed from a suspension particles of 5-20 p rapidly, particles of 40-50 p slowly, and those above 50 p not at all. Epischura baicalensis Sars seized living and rejected dead cells or detritus and selected Cyclotella baicalensis even when other diatoms predominated in the plankton (Kozhova, 1953, 1956, quoted from Jsrgensen, 1966).

    It is clear then that copepods can and do select particular foods but they do not do so all the time, and their preferences may change. It depends on the composition of the plankton they are feeding on and, to some extent, on what they have previously been eating. Marine copepods may tend to select the larger of the foods presented to them, but the preferences of freshwater copepods seem to depend more on ecological factors.

    3. Quality of food

    as food. Particles do not seem to be rejected simply because they are useless

    Copepods will ingest, and form faecal pellets from, such

  • 94 SHEINA M. MARSHALL

    intractable material as Indian Ink (Marshall and Orr, 1952) or poly- styrene pellets (PaffenhGfer and Strickland, 1970).

    Provasoli and his co-workers (Provasoli et al., 1959; Shiraishi and Provasoli, 1959 ; Provasoli et ab., 1970) have stressed the quality of the food necessary for crustaceans, especially with regard to fertility and fecundity. They have done some very interesting work by feeding the tide-pool harpacticids Tigriopus californicus (Baker) and T. japonicus Mori on various bacteria-free cultures of flagellates. The Tigriopus were also bacteria-free so that the food was purely algal. Although most algae would allow growth of the copepods through several generations, all eventually failed. Development began to take longer, mortality in the larval stages increased, and infertile adults were produced. These effects could be prevented by: (1) the presence of bacteria-one Platymonas sp. for instance, allowed reproduction through eight generations only, but Tigriopus grew for three years in a bacterized culture of the same species ; (2) the use of two algal foods together, since, although Rhodomonas lens Pascher et Ruttner allowed copepods to reach the fifth and Isochrysis galbana Parke the eighth generation when used singly, when used together they allowed repro- duction to go on indefinitely (up to 250 generations in ten years) ; and (3) the addition of a mixture of vitamins or of glutathione. It seems clear that the copepod needs some nutrient for reproduction of which it cannot build up a big enough store from any one flagellate. The addition of vitamins or glutathione to the culture medium increases the supply of this unknown nutrient in the alga or alters its composition, so increasing its nutritive value to the copepod. The copepod does not absorb it direct from the medium : crustacea are extremely inefficient in the uptake of solutes (DAgostino and Provasoli, 1970).

    In natural waters the food supply is usually mixed and bacteria are present and it is improbable that herbivores will suffer from an inadequate diet, but this may not be so when copepods in the laboratory are fed on a single species of food.

    Smyly (1970) did some experiments on feeding a mainly carnivorous cyclopid Acanthocyclops viridis on a variety of diets to find their effect on fecundity and longevity. His diets were : (1) algae (mainly Scene- desmus) ; (2) protozoa (mainly ciliates but including flagellates and a few rotifers; (3) cladocerans both large and small species; (4) newly hatched Artemia nauplii, and mixtures of any two of these. The different foods had different effects on the copepods. Development took place more rapidly in any of the animal foods than on algae alone and this was true of both larval and reproductive development. The copepod produced the greatest number of egg sacs and the largest

  • RESPIRATION AND FEEDING! IN COPEPODS 96

    number of eggs on Artemia, nearly as many on cladocerans and few on protozoa or algae. It survived longest on cladocerans and for t.he shortest time on Artemia.

    Nassogne (1970) reared the harpacticid Euterpina acutifrons on a variety of algal cells and found that they ate more and laid more eggs on some species than others, and did best in mixtures. Paffenhofer (1970) also found that in Calanus paci$cus fed on the same quantity of food (expressed as pg C/1) different species of algae have different effects on time of development, mortality and sex ratio.

    Apart from nutritional deficiencies some algae are definitely toxic or produce toxic metabolites. Some flagellates have been found poisonous to fish (e.g. Cymnodinium veneficum Ballantine and Prym- nesium parvum Carter). The first was fed to Calanus which died after one or two days in rich culture, i.e. much more slowly than did the fish (Marshall and Orr, 1955a). The Cymnodinium lost its toxicity after some months of culture in the laboratory and then had no harmful effect on Calanus, or Pseudocalanus (Urry, 1965).

    Some algae, although they do not cause death, are little eaten and digested (Marshall and Orr, 1955a; Urry, 1965). Such are Chlorella stigmatophora, Chromulina pusilla, Nannochloris oculata, Dicrateria inornata and Amphidinium sp. In some cases this is probably because they are too small to be efficiently filtered (see p. 74) but in others because they have a deleterious effect (Dicrateria, Chlorella and Amphidinium); the length of life of Pseudocalanus in these three cultures was decidedly shortened. Urry found that adding cell-free filtrate from a Chlorella culture to a culture of Isochrysis in which Pseudocalanus was living reduced its life span from 52 to 30 days. Much work is needed before it can be known whether the unsuitability of some algal foods is due to nutritional deficiencies or to toxicity and whether the effects are the same for all species of copepod.

    C. Experimental feeding

    The quantity of food which a copepod needs or takes in daily has been the subject of much research. Measurements were first made on mainly herbivorous copepods and since it was then supposed that they were almost entirely filter-feeders the results were usually expressed as volume of water filtered, or swept clear, daily. This expression has little meaning if the copepod feeds raptorially part of the time and it is now more usual to express quantities in terms of weight (or carbon or nitrogen) taken in per copepod or per unit body-weight (or carbon or nitrogen content).

  • 96 SHEINA M. NARsHrlIL

    1. Methods and results in the laboratory

    It is possible to count organisms in the gut or faecal pellets so long as the skeleton remains unbroken. In laboratory experiments Marshall and Orr (1 955a) counted skeletons of Prorocentrum triestinum in the faecal pellets of Calanus Jinmarchicus; these skeletons may separate into two halves, but remain unbroken. The culture of Pro- rocentrum was radioactive and the cells eaten were also assessed by measuring the radioactivity of the culture and of the copepod's body and faecal pellets; the two estimates agreed fairly well, 1 204, 1 655 and 324 cells eaten per day by the first and 865, 1 573 and 252 by the second method. There are, however, few cells which can be counted so easily (see Petipa, 1964a). Attempts have been made to measure food uptake by counting the faecal pellets produced by Calanus. Faecal pellets vary much in size and shape on different foods (being long and pale on diatoms, short and dark on flagellates) so that this is only a rough assessment ; in any case what is measured is uptake and not nutritional value.

    One of the simplest and most often used methods of measuring uptake is to keep the copepod in a known concentration of food cells and to count these after a lapse of time, comparing the number with that in a control vessel with no copepod. A number of precautions must be taken in any such feeding experiment. The food culture should be selected with regard to its age and the size of the cells. Age of culture is a factor whose importance has only recently been f d y realized (Mullin, 1963). Paffenh6fer (1971a) found that Calanus nauplii were killed by feeding, even if only for two or three days, on a 12-21-day-old culture of Lauderia. The concentration of food cells should be adjusted so that the amount the copepod will remove is much larger than the error of counting. The experimental flask should be kept gently stirred, for in most cultures the cells tend to settle out. This occurs less with young rapidly growing cultures. Experiments are usually carried out in the dark, partly because it has been found (Marshall and Orr, 1965a; Anraku, 1964a) that Calanus feeds rather better in the dark, partly to avoid, as far as possible, reproduction in the algal culture. The size of the experimental vessel has been found to affect feeding but not, at least in Pseudocalanus (Corkett and Urry, 1968), survival. Too small a volume certainly restricts feeding but the actual volume necessary to allow normal feeding has been variously measured. For one Calanws it has been estimated at 75-100 ml (Marshall and Orr, 1955a), over 100 ml (Anraku, 1964b), up to 4 1 (Gushing, 1969) and about 50 in 7 1 (Paffenhdfer, 1970) ; for Acartia clausi, 66 ml (Anraku,

  • RESPIRATION AND FEEDING IN COPEPODS 97

    1964b) ; for Temora longicornis, 7 ml limiting, 35 ml enough (Marshall and Orr, 1966) and 500 ml (Cushing, 1959); and for Anomalocera patersoni, 2-5 1 (Cushing, 1959). It should be noted that the large volumes thought necessary by Cushing have not been confirmed by other workers. The question of crowding is different from that of total volume, possibly because the main damage is caused by copepods bumping against the walls of the confining vessel. Mullin (1963) has found that 18 Calanus in 950 ml are not restricted in feeding, and Anraku (1964b) that raising the number of Acartia tonsa from 6 to 10 in the experimental bottle made little difference to grazing rate. Paffenhbfer, however, stresses the importance of large volumes. Geen and Hargrave (1966) found that, whereas in bottles in the laboratory a mixture of Temora tongicornis, Pseudocalanw minutw and Acartia tonaa, the last being the main species, filtered 5-6 ml/day, in large plastic cylinders, closed top and bottom by nylon net, and suspended in a lake, the copepods filtered 30 ml/day. Some workers (Anraku, 1962; Mullin, 1963) have found that feeding is sometimes greatest during the first hour or two of a feeding experiment although Paf- fenh6fer (1971a) did not confirm this. The duration of an experiment may therefore have to be taken into account in comparing results. Since the sexes and the different developmental stages feed differently, the ideal is to sort the copepods into sex and stage before experiment but this entails more handling and examination. They should in any event be sorted after the experiment. A temperature within the normal range of the copepod should be chosen. Even with all these factors adjusted it must be admitted that the results will still be variable; copepods show a great deal of individual variation and their metabolism differs according to the season of the year. Table IV gives the results, expressed as ml swept clear in 24 h and measured in the laboratory, of a variety of copepods. For Calanus (C. Jinmarchicw, C. helgolandiczcs or C. paciJicus) they vary considerably. Gauld (1951) using a culture of Chlamy&monas found in a long series of experiments an average of 84 ml and a maximum of 101. Marshall and Orr (1955a, 1962), using a variety of diatoms and flagellates, found a maximum of 151 ml but their figures were usually much less than this and often below 10 ml; Cushing (1959) found 1 200 ml; Corner (1961) using feeding in natural sea water found 10-36 &/day from May to September. Anraku (1 964b) using mainly Thalassiosira Jluviatilis in 6-h experiments, 200 ml; Paffenhofer (1971a) up to 1428 ml in females feeding on Gymnodinium splendens Lebour, Corner et al. (1972), 700 ml when feeding on Biddulphia sinensis. For Pseudocatanus (P . elongatw or P. minutw) adults, Gadd found a maximum of 8.6 ml, Anraku of

  • TABLE IV. IN~ESTION OF FOOD BY A VARIETY OF COPEPODS

    ml Jilteredlday

    mllcopepod mllmg dry wt FOOd Method Source Total length (mm)

    Species

    Calanus finmarchicus

    C. Jinmarchicus late stage C. Jinmarchicus 9

    C. jinmarchicus ? C. Jinmarchicus ? C. helgolandicus ? c. pacijicus Q C. pacijicus 0 C . pacijicus ? C. hyperboreus ? C. glacialis ? Neocalanus gracilis Q Nannocalanus minor Rhincalanus nasutus Q R . nasutus ? R . cwnutus 9 Eucalanus attenuatus Pseudocalanw minutus 9 P. minutus ? P. elongatus ? Chirundina indica ? Euchirella curticauda E . bella Q Ewhaetcc acuta 0 Swlecithrix danae 0 Lophthrix lutipes 9 Centropages tyg&wr 9 a. typicua

    (3-4) Cells < 10 p diam. Cells > 10 p diam. Nat. sea.

    24-4.3 Thal. 2.7-4 Var. phyto.

    (c. 3) Nat. sea. - Dit., Go.

    L. - Gym.

    6.3-8.5 Var. phyto. 44-52 Var. phyto. 3-0-3.7 COB., Thal., Art. 14-1.9 Cos., Thal., Art. 3.8-4.3 Art.

    3.1-3.4 Thd., Art.

    -

    - Thal., Art.

    3.8-5.8 Thal., Art. 1.2-1-6 Thal. - Flag.

    (1.4) Var. phyto. 3.3-3.9 Thal., Cy., Art. 3.6-3.7 Art. 3.1-3.9 Art. 3.2-3.9 Art. 1-7-2.0 Art. 2-9-3.1 Cos., Art.

    (1.3-1.8) Thal. - Diatoms

    0 4 0-84 1-52

    36-190 5-164

    10-36 68-123

    316-1428 0-329 9 4 4 8

    20-222 18-22

    17 98-669 16-120 15-101 6-40 6-6 0-12

    49-197 264 232

    85 118

    31-58 5-50 0-1 1

    201-835

    - 750-3500 -

    - 30-540 -

    32P

    32P

    Chlor.a, at sea Cell count Cell count Cascade expt. Cell count Cell count Cell count cell count Cell count Cell count cell count count Count count count Cell count Cell count 32P

    count count , count count count Count Cell count Cell count

    Marshall and OIT, 1955a Marshall and OIT, 1955a Adams and Steele, 1966 Anraku, 1964a Mullin, 1963 Corner, 1961 Mullin, 1963 Paffenhofer, 1971 Paffenhofer, 1971 Mullin, 1963 Mullin, 1963 Mullin, 1966 Mullin, 1966 Mullin, 1966 Mullin and Brooks, 1967 Mullin. 1966 Mullin. 1966 Anraku, 1964a Geen and Hargrave, 1966 Marshall and Orr, 1966 Mullin, 1966 Mullin, 1966 Mullin, 1966 Mullin, 1966 Mullin, 1966 Mullin, 1966 Anraku and Omori, 1963 Gaudy, 1968

  • C. hamatua C . hamatua Diaptomua wegonenais D . oregonensis Temora longicmnis T . longicornis T . longicornis Metridia h e n s M . lucens M . lucens M . longa M . longa Pleuromamina xiphiaa P . abdominalia P . gracilis P . piseki Labidocera acutifrons L . aestiva Acartia tonsa A . tonsa A . clauai A . clam' A . clauei Tortanwr discadatus

    0

    0

    ? ?

    ? 0 ? 0 ? P ? 0 ? Q

    (1.4) Thal. - Var. phyto.

    - Flag. nat. phytopl.

    - Var. phyto. - Flag.

    (2-5-3) Ch. Cri. - Mix. phyto. - Mix. phyto., Art.

    (4-4.6) Mix. phyto. - Mix. phyto., Art.

    4.2-5 Art. 3-3.4 Art.

    1-7-1.8 Art. 1.7-1.8 Art.

    (1.3-1.5) N ~ o .

    (1-1.5) Skel.

    3'33.9 Art. 1-8-2.0 Art. (1-1.2) Skel. - Thal.

    (1.2-1.3) Thal. - Var. phyto - nrtt. phyto 2-2.3 M .

    1-15 0-6

    0-13 1-27 0-2 1 5 6

    04-1.3

    18-31 1-5 3-7 520 210

    73 110 80

    8-25 1-105 3-20 &11 5-6

    < 1-2.5

    1-15

    -

    -

    Cell count 32P

    14c

    Cell count 32P

    3aP cell count 3aP Cell count count Count count Count count count count count count cell count Cell count Cell count 32P

    Cell count Count

    Anraku and Omori, 1963 Marshall and Orr, 1966 Richman, 1964 McQueen, 1970 Berner, 1962 Marshall and Orr, 1966 &en and Hargrave, 1966 Marshall and Orr, 1966 Haq, 1967 Haq, 1967 Haq, 1967 Haq, 1967 Mullin, 1966 Mullin, 1966 Mullin, 1966 Mullin, 1966 Mullin, 1966 Anraku, 1964a Conover, 1956 Anraku, 1964a Anraku, 1964a Marshall and Orr, 1966 Geen and Hargrave, 1966 Anraku and Omori, 1963

    Where total length is not given by the authors, it is taken from Sara (1903) or Wilson (1932) and enclosed in brackets. Abbreviations for foods : Nat. sea. -natural seawater

    Var. phyto.-various phytoplankton cultures Mix. phyto.-mixtures of phytoplankton cultures

    Nano. -nanoplankton Flag. -flagellates Art. -Artemia nauplii cos. -Coscinodkcus sp. CY. -Cyclotella sp,

    L. -Laderia borealis Skel. -Skeletonema costatum Thal.-Thalassio&-a jEuviatilis Ch. -Chaetoceros sp. Dit. -Ditylum brightwellii Gym.-Gymnodinium splendens Go. -Gonyaulax sp. Cri. -Cricosphaera elongata

  • 100 SHEWA M. MARSHALL

    42 ml and Marshall and Orr (1966) 11.6 ml. For Centropages hamatzLs, Gauld found a maximum of 15 ml, for C. typicus Anraku found 44 ml. For Temora Zongicornis aduIts, Gauld found a maximum of 11.6 ml, Berner (1962) of 27.2, Cushing of 150 ml, Marshall and Orr of 20.5. For Acartia clawi Conover (1956) found a maximum of 10.4 ml, Anraku one of 23 ml, Marshall and Orr 11.2 ml, and for A . tonsa Conover found a maximum of 25.1 ml and Anraku 60 ml. (See also Geen and Hargrave (1966) above.)

    Counting cells gives a measure of food ingested ; it does not measure the nutritive value to the copepod. Conover (1962) improved on the method by collecting faecal material and estimating its organic content. Since it is difficult to be sure of recovering all faeces he later (1966b) developed a method obviating their complete recovery by measuring the ratio of total to ash-free dry weight in both food and faecal pellete. The method depends on the assumption that only the organic fraction of the food is assimilated. The assumption has not been specifically tested but Conovers calculations of assimilation by ratio agreed well with those obtained by collecting all faecal pellets. Corner (1961), however, suggested that Calanus selected organic-rich particles preferentially.

    Marshall and Orr (1955a, 1956, 1966) and Berner (1962) used radioactive phosphorus (3aP) to label food cultures before feeding them to copepods and the results from their experiments are included in Table IV. The calculations of volume filtered per day were made from measurements of the radioactivity of the food culture and, at the end of the experiment, that of the body of the copepod (and of any eggs produced) and of the faecal pellets; this also allowed an estimate of assimilation. The results give filtration figures much lower than those from cell counts and this is at least partly because no account was taken of liquid excretion ; this can cause a considerable error in short-term experiments. The 32P does not get into equilibrium with the P in the body until the animal has fed for some days (Marshall and Orr, 1961) ; there is a rapid turnover of part of the phosphorus in the body and a fraction of the newly ingested 32P is lost within a few hours by excretion. The calculation of total food ingested and the estimate of assimilation are therefore too low. Nevertheless, the radioactive method is very sensitive and allows one to study individual copepods, to locate in the body the position of newly ingested 3aP and to find the proportion of the 32P which goes into egg-laying (Marshall and Orr, 1965a, 1961). Lear and Oppenheimer (1962) fed Tigriopus californiczcs on P l a t y m o w cells labelled with and gOYt and assessed the numbers eaten both by cell count and radioactive count. The f i s t method gave higher

  • RESPIRATION AND FEEDING IN OOPEPODS 101

    figures, 24 000 as against 15 000, but they thought that this was due to radioactive decay.

    Corner (1961) estimated food uptake in female Galanus helgo- landicus by measuring the amount of organic matter in natural sea water before and after it had flowed through a vessel containing a number of the copepods. The calculated volume filtered daily varied from 10-36 ml. The experiments were done during the summer ; the results were compared with respiration measurements and it was concluded that by filtering this volume they could cover their require- ments as measured by their respiration.

    2. Comparison of field and laboratory experiments A different approach was made by Gushing (1953, 1955, 1958,

    1959, 1968; Gushing and Vu6eti6, 1963) when he calculated the volume filtered by measuring the decrease in a phytoplankton patch in the North Sea over successive periods from March to June, assuming that this was caused solely by grazing. Calanus was the most abundant grazer and the other zooplankton organisms were calculated as Calanus " units " according to their size. From this assessment a Calanw would have to sweep clear 1-5 1 daily to deal with the chlorophyll which had disappeared between cruises. These volumes are obviously much too great to be dealt with by a filtration method of feeding and Cushing therefore developed (1959, 1968) an " encounter theory " of grazing according to which copepods obtain their food by tactile encounter as they move steadily through the water. For this assessment, the size of the copepod, the length of the antennular sensory hairs, the speed of swimming and the time taken to convey a food cell to the mouth and to eat it, must all be estimated. The importance of the antennular sensory hairs disappeared when it was found that copepods (see p. 80) could feed equally well with and without antennules, but the rest of the theory still stands since a copepod may sense its food in other ways. The sensillae in pits distributed over the copepod body, recently described by Fleminger (unpublished) could possibly be used in this way. In an interesting discussion of his theory Gushing (1968) uses it to explain variations found in " volume filtered " with increasing algal densities and with different sizes of prey, and brings into consideration the " perceptive range " of a species, which is not accurately known for any species (see, however, Petipa, 1965b ; Conover 1966a). Gushing (1964) explains the great discrepancy between food uptake as calculated by his methods and by laboratory experiment by the hypothesis of " diatom spoliation " ; he thinks that diatoms are often broken open before ingestion and part of the contents spilled.

  • 102 SHEMA M. MARSHALL.

    This happens to some extent when a copepod is dealing with large cells which cannot be taken into the mouth intact (Conover, 1966a) but it seems unlikely to happen with small cells which can be ingested whole; measurements by Corner et al. (1965) and observations by Paffenhijfer have not confirmed it. Conover (1966a) using Calanus hyperborezcs feeding on Thalassiosira Juviatilis puts the loss at 15%. In some recent experiments (Corner et al., 1972) with Calanus helgo- tad icus feeding on the large diatom Biddulphia sinensis, there was no chemical evidence that any of the cell contents had been lost, nor were broken frustules found after the copepods had fed. Cushing has also expressed his results as the percentage of body weight ingested daily, the daily ration (Cushing and VuOeti6, 1963 ; Cushing, 1964), and this, for Calanus jinmarchicus may come to as much as 390%, a value confirmed by Petipa in the Black Sea. She made (1964a, 1965a, b, 1966; Petipa, et al., 1968) an extensive series of observations there in June on the feeding and biology of the copepods at a time when the phyto- and zooplankton were in equilibrium and there was little predation on the copepods. Larvae and small species of copepods remained in the top 25 m, larger copepods (later stages of Calanus helgolandicus and Pseudocalanus elongatus) migrated daily to and from below 100 m. Counts were made of the phytoplankton at a series of depths, and samples of all stages of copepods were taken at the same depths for measurement of length and weight and for assessment of the number and weight of food organisms in the gut. The size of the fat bolster was also measured at different depths and times of the day. She concludes that there is a diurnal feeding rhythm, non-migrating stages feeding more by day than by night and migrating stages more by night than by day because of the extra energy required for vertical migration.

    Two methods of calculating the daily ration were used. In the first, the quantity and the kind of food in the gut at each depth, the speed at which food passed through the gut, and the time the animals remained at each depth were all assessed ; a calculation was then made of the total food ingested. It should be noted that the speed of passage through the gut when food was at its richest was taken as 20 min (12 faecal pellets/h). This was the maximum speed found by Marshall and Orr (1955a) in high concentrations of algal culture, whereas the maximum number of algae in the Black Sea was comparatively low, only 4*5/ml. The second method was to measure the size of the fat bolster at its maximum and minimum and, from a knowledge of the food eaten and its fat content, to calculate the wet weight of all food eaten. The assumptions were made that : (1) all the fat in the bolster

  • RESPIRATION AND FEEDING IN COPEPODS 103

    comes from the food (she states that it can be seen passing in 0.5 p droplets through interepithelial canals in the gut wall) ; (2) that 90% of the food is digested ; and (3) that all the fat is first deposited in the bolster. The second method gave results from one to ten times higher than the first and was taken as more reliable. The assessments are not such as can be made with great accuracy and results based on them must be rather speculative, but at least they are on animals under natural conditions.

    The average daily ration was found to be 130% but varied from 60-313%. The 313% was for males (which are usually poor feeders) and the next highest was 183% for copepodite 111. Non-migrating forms (e.g. Calanus copepodites I and I1 and Acartia) needed much less. On the whole, considering the assumed rate of digestion and the speed of movement of the food through the gut, it seems likely that these are overestimates although Petipa considers them under- estimates.

    It is clear from morphological considerations and from the numerous observations and experiments which have been made, that many copepods feed by mechanical filtration part of the time, and among these is the important genus Calanus. There still remains a great gulf between results based on natural populations at sea and those based on laboratory experiment. In an attempt to bridge this gulf Adams and Steele (1966) carried out an extensive series of experiments on board a vessel in the North Sea, using I4C methods and chlorophyll measurements to assess the phytoplankton present and assuming the zooplankton present (mainly Calanus) to be acting as grazers. The calculated volume swept clear varied from 1-38 ml daily, thus confirm- ing some laboratory work. They also found that at low algal con- centrations (less than 25 pg chlorophyll all) filtration was reduced, usually to below 15 mllday, which is the opposite of what one would expect on the " encounter " theory. They think the reduced feeding is ecologically important, since it will allow phytoplankton regeneration and that at such times Calanus may turn carnivorous. At concentra- tions of 270-300 pg organic carbonll, present at their site in the North Sea from May till August, CaEanzLs could store fat and the females lay eggs. If 50% of the carbon measured is taken as phytoplankton these results agree fairly well with those of Paffenhhfer (personal com- munication). On a suitable food (Qmnodinium splendens, Gonyaulax polyedra Stein) he found that C. pacijicus laid eggs at 100 pg C/1 and that there was fat accumulation, at a lower level, 50 pg C/1, on G. polyedra and Prorocentrum micans. It is noteworthy that with Chaetoceros curvisetus there was no egg laying even in high concentra-

    A.Y.B.--II 5

  • 104 SHEINA M. MARSHAIL

    tions. Paffenhsfer (1970) also found C. pacz@us grazing on Gymno- dinium splendens down to a level of 15 pg C/1 and on Skeletonema costatum (Greville) Cleve down to 30 pg C/1; he therefore thinks that the kind of food influences the concentration at which grazing is reduced.

    The same type of experiment as those of Adams and Steele was carried out over a wider range of plankton in the Strait of Georgia, B.C. (Parsons et al., 1967, 1969; Parsons and Le Brasseur, 1970). These experiments were integrated with observations on the fish, zooplankton and phytoplankton and with an examination of the gut content of predators. The whole plankton biomass was expressed as a continuous size spectrum calculated from the number and volume of each organism as counted by a Coulter Counter (Sheldon and Parsons, 1967). Peaks in the size spectrum curve were identified by microscopic examination as due to particular organisms. Large zooplankton organisms were counted manually. Feeding experiments were then carried out on organisms as they occurred naturally in the sea at the time, zooplankton (sometimes partially sorted) feeding on phyto- plankton (as naturally present or in a series of dilutions). Larval and young fish were fed on zooplankton. In studying zooplankton feeding they sometimes differentiated between those species that undertook diurnal vertical migration and those which did not, allowing the first to feed only during the dark hours and the second during the whole 24 hours. The results of the first series of experiments (feeding of zooplankton) showed that even when present in large numbers some phytoplankton might be unavailable to some zooplankton for reasons of size or shape ; intake did not always meet requirements. Thus, on a low density mixture of p-flagellates and Skeletonema, of modal size 8 p and 14 p, Pseudocalanus could obtain only 4% of its body weight daily. When the density of this mixture increased and the modal size was 14 p, a mixture of Pseudocalanus and Oithona ate Skeletonema only and ingested 40% of their weight per day. Calanus (C. plumchrus, copepodid stages 111, I V and V) also fed well, ingesting 15-60% of their weight daily. The result for Oithona is surprising for it has not usually been found to feed well on particles as small as Skeletonema, but the uptake may have been mainly by Pseudocalanus. It is not clear if the uptake of individual species could be assessed. In a bloom of Chaetoceros (C. debilis Cleve and C. socialis Lauder), Calanus paci$cus, Pseudocalanus minutus and euphausiid furcilia were unable to feed, although adult Euphausia pacijica Hansen could ingest 15% of their body weight daily and lay eggs. Larval and young fish showed the same type of result, a 90 mm fish (salmon) for instance being able to get

  • RESPIRATION AND BEEDING IN COPEPODS 105

    enough food from Calanus, but not from Pseudocalanus or euphausiids at the same density, 20 g/m3.

    It is noteworthy that with both zooplankton and fish there was a concentration (varying with both grazers and algae), from 40-190 pg carbon/l below which no feeding took place, and like Adams and Steele (see above) they think this ecologically important. The values seem inconsistent with the fact mentioned above that fat accumulation and egg laying can take place at levels of 100 pg C/1. In laboratory experiments Paffenhrifer (1970) (see above) has found Calanus pacijcus grazing down to a level of 15 or 30 pg C/1.

    Since levels of 50-100 pg C/1 are above what is often found in the ocean it can be deduced either that copepods can adapt their feeding habits to varying food concentrations (for which there is some evidence) or that in the open sea phytoplankton is aggregated rather than evenly distributed. The results of a chlorophyll profile made by fluorometer (Strickland, 1968) from the surface to 75 m indicated that the chloro- phyll is distributed in layers, rich layers of 2 m or more in depth alternating with poor.

    3. SuperJEuous feeding There is another difference of opinion between workers at sea and

    workers in the laboratory, namely, the question of superfluous feed- ing. This occurs if, in an increasing concentration of food, the copepods ingest more, but assimilate less. Harvey et al. (1935), Riley (1947), Beklemishev (1957, 1962) and Petipa (1964a, 1966a) all think that copepods eat 50%-400% of their own weight per day to account for the disappearance of diatoms from the sea and, since they require for maintenance only 1040% (opinions vary), the remainder during a diatom increase must be rejected in the faecal pellets. Gushing (1964, see p. 101) thinks that the loss takes place before ingestion, by diatom spoliation.

    Petipa (1964a) says that superfluous feeding begins at the level at which Calanus can begin to store fat and lay eggs. This level she puts at 200-300 Prorocentrum micans cells/ml or 3 mg biomass/l, presumably as wet weight. With Coscimdiscus or Nitzschia closterium (Ehrenberg), since they are less suitable as food, the figure is higher, 5-12 mg/l. Beklemishev (1962) gives the same biomass figure of 3 mg/l for the start of superfluous feeding and interprets this as 15 000-40 000 cells of Nitzschia closterium or 10-1 000 cells/l. of other species . These figures can be compared with Paffenhrifers estimates of the level at which his Calanus began to lay eggs, namely, 100 pg C/1 corresponding to about 50 Prorocentrum micans cellslml. Petipa also thinks that

  • 106 SHEINA M. MARSHALL

    because copepods in the laboratory cannot carry out vertical migration, their respiration and food requirements are bound to be very much lower than those measured at sea and she supports this by pointing out that in her results the discrepancy is much less in non-migrating stages of Calanus and small non-migrating copepods. Vlymen (1970), however, calculated on theoretical grounds the energy required for swimming and vertical migration in copepods and says that it is a negligible fraction (0.2%) of the total energy used.

    Laboratory experiments have not confirmed the existence of superfluous feeding. Mullin (1963) has found that filtering rate decreases continuously with increasing concentration of food ; Haq (1967) found this also, even when using Artemia nauplii as food. Most workers have found that although filtering rate at first remains constant with increasing concentration of food, it soon drops off (Marshall and Orr, 1955a; Anraku, 1964b; Geen and Hargrave, 1966; Richman, 1964). In experiments with 3zP labelled food, assimilation remained high even when food was passing through the gut at the maximum rate. Conover (1966~) found that assimilation was not affected by temper- ature, age of culture, or the amount of food which had been ingested. In their detailed study of the feeding of Calanus helgolandicus on Biddulphia sinensis, Corner et al. (1972) found that assimilation re- mained unaltered with increased intake up to levels much above anything found in the sea. Experiments with Calanus (C. Jinmarchicus, C. helgolandicus, C. hyperborew) on the efficiency of food utilization and excretion (Conover, 1964, 1966c, Butler et al., 1970) give no support to the idea of superfluous feeding. During the spring diatom increase in the Clyde sea area Calanus jinmarchiczcs increased its intake, but this food was assimilated and the excretion of nitrogen and phosphorus was also greatly increased. Growth efficiencies remained high, as they did with C. hyperborezcs, even in high concentrations of diatoms.

    4. Feeding in laboratory-reared copepods A great advance was made when it became possible to breed

    several generations of copepods in the laboratory. This has long been possible with benthic or tide-pool harpacticids (Provasoli et al., 1969 ; Neunes and Pongolini, 1965; Battaglia, 1970; Nassogne, 1970) and more recently (Jacobs, 1961 ; Zillioux and Wilson, 1966; Heinle, 1966, 1969, 1970; Katona and Moodie, 1969) with neritic and estuarine copepods such as Pseudodiaptomus, Acartia, Pseudocalanus, Temora and Eurytemora. The more pelagic calanids proved difficult and it was not until 1965 (Mullin and Brooks, 1967) that Bhincalanus nasutus and 1970 that Calanus pacijicus (Paffenhfifer, 1970) were reared

  • RESPIRATION AND FEEDING IN COPEPODS 107

    through seven and two generations respectively. The Rhincalanus culture failed from a general decrease in fecundity, growth and survival ; the Calanus culture failed through lack of males or at least of adequate males. Possibly both cultures may have run into the kind of difficulty described by Provasoli et al. (1959), although the Rhincalanus culture was fed on a mixture of different species of phytoplankton and con- tained bacteria (see p. 94).

    The essentials of successful laboratory culture seem to be : large container volume especially large for mating, a frequently changed supply of filtered sea water and the provision of a food (which need not be much greater in quantity than that normally found in the sea, 60-100 pg carbon/l) of suitable quality, i.e. a diatom or dinoflagellate culture of the right cell size and in an early stage of growth. Anti- biotics are not necessary if conditions are carefully controlled. Although the mating of adults in the laboratory and the production of successive generations have not been repeated with pelagic copepods, the methods proved very suitable for rearing them from egg to adult with low mortality and this has made possible a much more detailed study of growth during development. The populations grown from eggs laid and developed in the laboratory must be much more homogeneous than animals caught in the sea. Apart from the traumatic experiences of catching and sorting they are, if reared in large vessels, free from the damaged antennules and broken setae so often found in net-caught specimens. It has always been a question whether the effects of this handling were not one of the main causes of the differences between experimental work in the laboratory and at sea. It should now be possible to find out (see p. 60).

    Whether there are any disadvantages in using laboratory popula- tions it is as yet too early to say. The fact that sex ratios are variable and rarely normal (in Calanuus and other copepods but not in Rhin- calanus) indicates some nutritional inadequacy, and it has been suggested (Lee et al., 1970, 1971) that they may be less adaptable than " wild '' populations. Laboratory reared copepods often do not equal wild copepods in length and weight and Paffenhbfer, who has been successful in obtaining laboratory specimens of weight equal to or greater than those in the sea, suggests that the loss of adaptability, at least in the later stages, may be because by that time copepods in the sea would have begun diurnal vertical migration and so would have encountered a much greater variety of environmental conditions.

    The most detailed work on the energetics of growth has been done by Mullin and Brooks (1967, 1970a and b) on Rhincalanuus nmutus and Calanus pacijcus and by Paffenhofer (1970, 1971a and b) on the

  • 108 SHEINA M. MARSHALL

    second. They have studied the effect of different temperatures and of different species and concentrations of food organisms and have compared their laboratory-reared animals with those taken from the sea. Their figures are all based on carbon content. In Table V they are compared with Petipas (1967) results on C. helgolandicus and Acartia clausi under natural conditions in the Black Sea. Her figures are based on calories. In Table V the figures given are the gross efficiencies (K1 of Russian writers), i.e. the percentage of food ingested which is turned into growth.

    Mullin and Brooks used Thalmsiosira JEuwiatilis and Ditylum brightwellii as foods in concentrations of from 148-352 pg C/1, but only the first could be eaten by Calanus nauplii. Paffenhofer used Lauderia borealis and Gymnodinium splendens in concentrations of about 100 pg C/1. In Mullin and Brooks experiments the growth stages were grouped into three, or four, sections and Paffenhofer has expressed his results both in this way (1971b) and also for individual growth stages from nauplius I V to female (1971a). Although their groups are not quite the same, they can easily be compared. Petipa grouped nauplius 111-VI but studied the copepodid stages individually.

    The efficiencies found by Mullin and Brooks are on the whole higher than those of Paffenhofer and, although there are several exceptionally high percentages, most of them lie between 18% and 40%. Paffenhdfers lie between 17% and 35% and whereas the nauplii in his grouped experiment (nauplius IV to copepodite I) are much the same as the rest, nauplii IV and V when tested individually have much lower efficiencies, 8-10% for nauplius IV and 14-15% for nauplius V. Petipas results agree fairly well over most of the range. She finds the highest efficiency in copepodite I with a gradual decrease in older stages. She says that the nauplius stages swim and feed inefficiently because their limbs are not well developed and they have no movable abdomen nevertheless their overall efficiency is about the same as that of C I1 and C 111. The first copepodid stage, with better developed limbs, with a movable abdomen and living continually near the surface in a rich food supply, is the most efficient stage. The dramatic drop to a 5% efficiency in stage V is accounted for by vertical migration (which, however, begins in stage IV). The possibility of vertical migration is of course one of the main differences between laboratory bred and wild Calanus. Acartia is a less efficient copepod and has less marked vertical migration; the effect of this on the later stages is therefore slighter than in Calanus. Mullin and Brooks found no significant difference between the two foods they used nor between the temperatures of 10C and 15C. Paffenhofer found that efficiencies

  • TABLE V. GROWTH EFFICIENCIES OF Calanw, Rhincalanw AND Acartia ON DIFFERENT FOODS

    Mullin and Brooks, 1970 Paffenhiifer Paffenhiifer, 1971 Petipa, 1967 Source ~~

    Species C. paci$cw Rhincalanus nasutus Calanus paci$cua Calanus pacijkw C. klgolandicua Acartia clausi

    Food Thalassiosira Ditylum Thalassiosira Lauderia Gymnodinium Lauderia Gymnodinium Natural seawater pgC/Zitre 226 177 200 148 352 196 101 95 101 95

    ~ ~~

    T"C Stage NI NII NIII NIV N v NVI CI CI I CII I CIV cv 9 Total NI-

    CVI

    10" 15' 10' 15" 10" 15" 15' 15' 15' 15' Newly moulted body wts Medium body wts

    1 21 18 39 39 22

    21 \ 17.3 20.1 29.6

    34.7

    27.6

    35 34 34 45 30 37

    7.6 9.8 14,7 14.1 29.8 36.7 22.0 22.0 17.6 21.2 22.4 27.2 15.7 25.3 19-6 22.2

    Stage NI N I I NIII m N V I

    14 Nv

    50 17 C I 39 16 CI I 28 23 CI I I 21 16 CIV 5 cv

    8 11

    Petipa also gives figures of 2 % for efficiencies of adult females of Calanus and Acartia.

  • 110 SHEINA M. MARSHALL

    were slightly higher with Cyrnnodinium as food than with Lauderia. The overall efficiency from nauplius I to adult in the results of Mullin and Brooks varies from 30 to 45%, the average being 36%, and in those of Paffenhofer from 19-30%. This may be compared with the figure of 34% from egg to adult (based on nitrogen) found by Corner et al. (1967).

    IV. CONCLUSION In this survey of the respiration and feeding of copepods it will

    have been noted that the results from experimental work are extremely variable. A conclusion drawn from one set of experiments is often directly contradicted by that drawn from another set. Part of this must be due to variability among the individual copepods for in any experiment where individuals have been studied they have been found to vary greatly among themselves. Their behaviour is however affected by so many factors that the main differences are most probably caused by the varying conditions of the experiments. Apart from species, age and sex differences in the copepods used, light, temperature, size of container, crowding, size and quality of food all exert a marked influence and these have differed widely in the experiments of different authors. It must be remembered too that the metabolism of copepods caught at different times of the year may be quite different. The extreme importance of quality of food has only recently been recognized. The results so far obtained must therefore be considered as giving only approximate figures for oxygen consumption and intake of food.

    Problems still outstanding are the effect of vertical migration on the metabolism, the effect of high concentrations of food on the efficiency of assimilation, the extent to which nutrition modifies sex ratios and fecundity, and the differences, if any, between a wild and a laboratory-reared copepod. One of the main needs is for an extension of our knowledge to a wider range of copepods, particularly the carnivorous forms.

    V. ACKNOWLEDGEMENTS

    I am most grateful to the late Dr J. D. H. Strickland for his original invitation and to the Institute of Marine Resources, University of California for giving me facilities and financial support while I was writing this review, also to Professor N. Millott for allowing me to work in the University Marine Station, Millport while finishing it.

    I should like to thank, too, all my colleagues in the University of California, for their generous help, especially Dr M. M. Mullin for

  • RESPIRATION AND FEEDING IN OOPEPODS 111

    reading the typescript and making many useful criticisms and sug- gestions. To Dr H. Barnes and Dr E. D. S. Corner, who read and criticized the typescript, I am much indebted.

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