[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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    f 2:

    m

    f

    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 tempera...

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