The dry weight of a given copepodite stage, sampled at a given time from a homogeneous water mass, .... method of Owens & King (1975), scaled down to.
Hydrobiologia 167/168: 43-59 (1988) G. A. Boxshall and H. K. Schminke (eds), Biology of Copepods © Kluwer Academic Publishers
43
Ecological significance of individual variability in copepod bioenergetics Ulf BAmstedt Institute of Marine Biology, University of Bergen, N-5065 Blomsterdalen, Norway
Key words: bioenergetics, copepods, grazing, lipid, protein, reproduction, respiration Abstract
High interstage variability in body length and mass, reproductive state, and metabolic activity is characteristic of copepod populations from the Barents Sea and coastal waters in Sweden and Norway. The dry weight of a given copepodite stage, sampled at a given time from a homogeneous water mass, may vary by a factor of 4-5 between extreme individuals, protein and particularly lipid content being even more variable. Similarly, high variability in gut fullness and grazing rate within defined copepodite stages typically occurs at all times of the year, both when measured as in situ rate or experimentally determined rate, using homogeneous food suspensions. In accordance with this, maturation state (measured as length of gonads) and spawning (measured as rate of egg production over 24 h) are highly variable factors at the individual level. Since all these factors also influence the metabolic rate of the animals the respiratory rate (measured as ETS activity) of comparable individuals may vary by a factor of 5 or more. The results indicate that high individual variability in size and activity parameters is universal. This can not be explained by existing models of feeding behaviour, growth and development, and calls for new models, in which the nutritional history of the individual may play an important role.
Introduction
By tradition - but certainly also for practical reasons - physiological and behavioral activities of copepods have been interpreted from changes in average values for the population. If the frequencies in such activities are not synchronised among individuals in the population changes in the averages will probably not correspond to the frequency and amplitude in changes for the individuals. Pearre (1979) was concerned about this and showed, through theoretical considerations, that conventional data on vertical distribution over a diel cycle may lead to completely wrong conclusions about diel vertical migration of zooplankton. Hunger and satiation have been considered as main factors motivating the indivi-
dual to migrate up or down (e.g. Pearre, 1974; Mackas & Bohrer, 1976), and these, in turn, are modified by a number of factors, such as recent food intake, nutritive state (e.g. amount of stored energy), age, season, temperature etc. Through studies on the feeding behaviour of herbivorous copepods in recent years (e.g. Koehl & Strickler, 1981; Price et al., 1983; Paffenh6fer & Van Sant, 1985) we have learned that copepods in general are not mechanical filtrators, but can alter their feeding behaviour considerably. This information leads to the suggestion that copepods inhabiting a homogenous environment need not necessarily feed at the same intensity and frequency. Furthermore, the differences in feeding may lead to differences in developmental rate, body size, maturation processes etc, all these factors also being
44 modified by heterogeneities in the habitat. In order to document whether these suggested variations in mass and activity parameters among individual copepods really exist in nature, I present here data on several copepod species, representing populations from boreal and arctic waters. Material and methods Examples of individual variability in body size and chemical composition, and of different activity parameters were taken from various investigations. Individual dry weights, as well as lipid and protein contents of Euchaeta norvegica were investigated in May on a population in Korsfjorden, western Norway, sampled with a 'Beyer Low Speed Midwater Trawl' (see Matthews & Sands, 1973), 1 mm mesh, from c. 500 m to the surface. Individual animals were dried, weighed and analysed for their total lipid and protein content according to the procedures described by BAmstedt (1975). Prosome length, gonad length, and gut fullness were recorded during an annual cycle for Calanusfinmarchicus
and Metridia longa from Kosterfjorden, western Sweden. These populations were sampled regularly around noon and mid night by vertical hauls with a WP2-net, 200 pm mesh, from near the bottom (200-240 m) to 50 m. The animals were preserved immediately with buffered formalin (final concentration in seawater c. 2%) and gut fullness was determined on individuals from a subsample (usually 25 specimens) as length of gut with detectable food, using a Wild M5 stereomicroscope. As neither the diameter of the gut nor the degree of packing through time is constant this measurement can not provide an absolute quantitative assessment of food content but does serve as a relative indication. This value can also serve as a feeding rate index, as it has been shown that the amount of food in the gut is directly related to the feeding rate of the copepod (e.g. Mackas & Bohrer, 1976; Ki0rboe etal., 1982; Tande & Bfmstedt, 1985). Another subsample, usually consisting of25 individuals of each stage analyses,
was stained with borax carmine, dehydrated in an ethanol series, and cleared with cedarwood oil as described by Tande & Hopkins (1981). This procedure enabled the size and maturation state of the gonads to be analysed in a dissection microscope. Although gonad length alone does not give exact information on maturation state, different gonad lengths seem to indicate different maturation states in premature individuals. Copepods were sampled with a submersible pump in Raunefjorden (in March) and in Masfjorden (in April), western Norway. Specimens were used for determination of egg-production rate, feeding activity, body size, lipid and protein content, and measurements of the activity of the electron transport system (ETS activity). Single adult females were incubated in 20-30 ml ambient water from sample depth for c. 24 h for egg production measurements. Other animals were put in chloroform/methanol (2:1 by volume) for total lipid determination (see Btmstedt, 1975). The extracted bodies were dried at room temperature over silica gel and analysed for their protein contents, using the method of Dorsey et al. (1977). Other subsamples were used for determination of gut pigment. A subsample was anesthetized with MS 222 immediately after pumping (5 min after start) and individual copepods transferred to small test tubes with 90% acetone. Total algal pigment (chl. a plus phaeophytin a) was analysed on a Turner mod. 10 filter fluorometer as described by Strickland & Parsons (1972). The extracted bodies were dried over silica gel and analysed for their protein content. ETS activity was analysed on single individuals, using the method of Owens & King (1975), scaled down to a final volume of 2.5 ml and corrected for difference between in situ and incubation temperatures by using the Arrhenius equation (see Bamstedt, 1980). The ETS activity was recorded as the increase in absorbance at 490 nm after an incubation time of 15-20 minutes. Transformation to corresponding rates in oxygen consumption was made by using the fact that one mole of reduced INT (p-iodotetrazolium violet, Sigma Chemical Company, grade I, I 8377) corresponds to one mole of reduced oxygen. An extinction coefficient,
45 norvegica, sampled in May in Korsfjorden, western Norway, deviated from symmetry, espe-
E4 90 , of 19.613 mM-' for 1 cm cuvettes was
recorded for this grade of INT. The same procedures for ETS activity were used on copepods from Kosterfjorden, western Sweden, sampled in August.
cially in adult females and stage 5 copepodites (Fig. 1). Total range in dry weight corresponded to a multiplication factor (ratio between weight of
Calanus finmarchicus and
biggest and smallest individual) ranging from 2.1
C. glacialiswere sampled from 50 m to the surface in the Barents Sea in May, with a Juday net (500 jm mesh), equipped with a large, nonfiltering cod end, and used for experiments on egg-laying rate as described above. The animals were killed by adding a small amount of formalin to the incubation glass, and eggs counted and prosome length measured under a dissection microscope directly after termination of the experiments.
(adult males) to 4.6 (stage 5 copepodites). Individual variability in lipid content was even more
Adult
female
pronounced, with a multiplication factor between c. 2.5 (adult females) and 10 (stage 5 copepodites), the lowest values of stage 4 copepodites being somewhat unreliable (Fig. 2). These differences were to a large extent explained by differences in body weight of the individuals. The same holds true for the individual protein content (Fig. 2), which varied by a factor of 1.2 (adult males) to 5.0 (stage 5 copepodites). Variability in the lipid content of adult female individuals of Calanusfinmarchicus,sampled from Raunefjorden, western Norway in March, showed a total range in lipid content of c. 20 to 100 g with only a poor correlation (r = 0.12) with body length of the individuals (Fig. 3). Pro-
Results Variability in body components
The frequency distribution of individual dry weights of the carnivorous copepod Euchaeta
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3
46 INDIVIDUAL PROTEIN CONTENT
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Fig. 2. Euchaeta norvegica. Scatter diagrams of individual lipid and protein contents (g) versus body dry weight in May 1974, Kosterfjorden, western Norway.
0,7
47 tein and especially protein and lipid combined, were considerably better correlated with the body size, although individuals of a given prosome length could differ by a factor of 4.5 in protein + lipid. These large individual variations within size groups were most evident in the protein/lipid ratio (Fig. 3), although extreme values due to unprecise readings at low levels of any of the components may have overestimated the variability in the ratio estimates. An example of individual variability in body size is given for two copepod populations from Kosterfjorden, western Sweden. The prosome length of Calanusfinmarchicus sampled in the autumn showed a size-range factor between 1.25 (adult females) and 1.37 (stage 5 copepodites) whereas adult females and males of Metridia longa, sampled in the spring, varied by a factor of 1.23 and 1.16, respectively (Fig. 4). If one assumes that body length and body weight are related as a power function with an exponent of 3, then this yields a multiplication factor in wet weight between 1.95 and 2.57 for C.finmarchicus and 1.86 and 1.56 for adult females and males of M. longa.
Variability in feeding activity Gut fullness, as an index of feeding activity, is illustrated for two species from Kosterfjorden, western Sweden in Figs 5a-c. Day and night samples from near-bottom (200-240 m) to 50 m depth indicated that adult females of Metridia longa were actively feeding throughout the year but that individual variability in feeding was very high, with a population usually consisting of both starved and well-fed animals (Fig. 5). Among adult females of Calanusfinmarchicusthere was a higher proportion of non-fed individuals, but again there was considerable individual variability and the feeding individuals dominated at most sampling occasions (Fig. 5). Stage 5 copepodites of C. finmarchicuswere usually heavily dominated by non-fed individuals except in spring and summer, when day samples revealed a considerable proportion of the population to be
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Fig. 3. Calanusfinmarchicus.Scatter diagrams of individual contents of protein, lipid, their ratio and sum in adult females from 3 to 35 m depth in March 1987, Raunefjorden, western Norway.
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50 feeding (Fig. 5). In no single case was the nonfeeding behaviour adopted to by 100% of the population. Single individuals of copepods, sampled in Masfjorden, western Norway in April, were analysed for their gut pigment contents which was correlated to their protein content. A separate determination of the gut evacuation rate for stage 5 copepodites of Calanusfinmarchicus indicated that 1.2% of the gut content was evacuated per minute, and this factor was used for the calculation of grazing rates (see e.g. Tande & BAmstedt, 1985) for all species and stages. This may systematically bias the calculated grazing rates of the different groups, but should not influence the degree of individual variability which is discussed in this paper. Stage 5 copepodites of Calanus finmarchicus showed a weight-specific grazing rate fairly independent of body mass, whereas adult females of Temora longicornis showed a decreasing trend with increasing body mass (Fig. 6). Individual variability was usually moderately high in C. finmarchicus (1-4 ng/100 #ig protein per hour) and Pseudocalanus sp. (3-7 ng/100 g protein per hour), and high in T. longicornis (1-8 ng/100 #g protein per hour) and Centropageshamatus (2-13 ng/100 jig protein per hour). Pump sampling of stage 5 copepodites of C. finmarchicusat descrete depths in Masfjorden, western Norway, in April revealed a vertical profile in grazing rate with high individual variability at all depths, and with a total range from 0.6 to 5.6 ng/100 ,ug protein per hour (Fig. 7). Highest values appeared to occur between 5 and 20 m depth, where the highest in situ fluorescence was also recorded. Grazing rates of all the animals from the vertical profile were plotted against their corresponding individual protein content and this showed a trend of decreasing grazing rate with increasing body mass (Fig. 7) as was also shown earlier for T. longicornis. The high values at 5-20 m depth may then be explained by the occurrence of small-sized individuals there.
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Fig. 6. Scatter diagrams of body-mass (protein) specific grazing rates of various copepod species from 10 m depth, as related to the individual protein content, April 1987, Masfjorden, western Norway.
Variability in reproductionfactors Gonad length, expressed as percentage of prosome length, has been measured on copepods from KosterfJorden, western Sweden over a yearlong cycle (Figs 8A-C). In winter adult females of
51
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53 M. longa showed generally high values with little individual variability. The individual variability increased towards spring and summer and was most pronounced in autumn, when the relative gonad length varied between individuals by a factor of 2.5 (Fig. 8A). With one exception adult females of C. finmarchicus (Fig. 8B) showed high values during winter, although the individual variability appeared to be somewhat higher than for the former species. The individual variability increased in spring and summer, being highest in autumn, when extreme individuals differed by a factor 8. Stage 5 copepodites of C.finmarchicus (Fig. 8C) usually had small gonads in winter but an individual variability corresponding to a factor of 4. Individual variability increased during spring, the population then consisted of a considerable proportion of individuals with relatively well developed gonads. In summer gonads were invariably small, with a considerable part of the population with completely undeveloped gonads.
150 Calanus finmarchicus Cu C) -t
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High individual variability was again evident in autumn. The experimentally determined egg-laying rate of two copepod species from the Barents Sea is illustrated in Fig. 9. For both species, females that did not produce eggs were present, irrespective of the size of the animal. Calanusfinmarchicuspro-
duced up to 130 eggs per day, C. glacialis up to 100, but there was no significant relationship between prosome length and the rate of egg production for either of the two species. However, a positive trend in rate of egg laying versus prosome length was indicated for C.finmarchicus from Raunefjorden, sampled in March, although here also there was a significant contribution in the population from non-producing females of different sizes (Fig. 10). Variability in ETS activity
Copepods from the surface water (17 °C) in Kosterfjorden, western Sweden, sampled in August, showed high individual variability in ETS activity, those sampled from below 50 m depth (8 °C) showed considerably less variability (Fig. 11). An average value for individual dry weight was used for each species when calculating the weight-specific ETS activity, actual variability in body weight thereby adding extra variability to the weight-specific ETS activity. Stage 5 copepodites of C. finmarchicus from Masfjorden, 120
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Calanus alacialis
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Fig. 9. Calanus finmarchicus and C. glacialis. Scatter diagrams of spawning rates as related to prosome length in animals from < 50 m depth in the Barents Sea, May 1987.
a
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Prosome length (m)
Fig. 10. Calanusfinmarchicus.Scatter diagram of spawning rate as related to prosome length in animals from 10 m depth in March 1987, Raunefjorden, western Norway.
54 1 ·
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Fig. 11. ETS activity, expressed as corresponding weightspecific rate of oxygen consumption, of copepod species from < 30 m depth (17 C) and> 50 m depth (8 C) in August 1985, Kosterfjorden, western Sweden.
,ug oxygen/individual per hour 0
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Fig. 13. Calanusfinmarchicus. ETS activity (expressed as above) in stage 5 copepodites from 10 m depth. April 1987, kept in filtered seawater or with excess of Isochrysisgalbana, Masfjorden, western Norway.
.
Depth (m1) 30
1
o
western Norway, sampled at descrete depths in April, showed their highest individual variability below 10 m depth, but with the majority of values occurring in the range 0.2-1.1, g oxygen per individual per hour (Fig. 12). Individual variability within each depth was higher than the variation in average values between sampling depths. Stage 5 copepodites of C. finmarchicus from Masfjorden, sampled in April, showed a decreased ETS activity with starvation, although the individual variability remained high (Fig. 13). Animals kept together with Isochrysis galbanain excess showed an initial decrease but significantly higher values than for the starving animals thereafter, although individual variability was high also in this case.
M
Discussion "'' W. Fig. 12. Calanusfinmarchicus.ETS activity in stage 5 copepodites, expressed as corresponding rate of oxygen consumption per individual, and related to depth of occurence in April 1987, Masfjorden, western Norway.
Body size and mass
The high individual variability in body size and mass as well as in various physiological activities
55
within given developmental stages of copepods seems to be a general phenomenon. Few variables are usually recorded on an individual level, but large differences between replicate samples with several individuals may obviously be explained by an extremely high level of individual variability. Length and body mass of copepods are usually given as average values for the developmental stages, and equations describing the relationship between these variables over the whole life span usually therefore show an unrealistically good fit. Recently Kankaala & Johansson (1986) presented date on individual prosome length and carbon content of two brackish-water copepods. For the development from stage 1 to stage 5 copepodites (no separation of stages) there was a significant relationship between length and body mass whereas neither adult sex (separately tested) indicated a statistically significant correlation.
Most of the results used to exemplify individual variability in body size and body content were derived from net sampling through a water column, and it may therefore be argued that the results only reflect differences in depth of habitat of the individuals. For example, it was shown by Marshall & Orr (1972) that stages 4 and 5 cope-
Adults males of Eurytemora affinis hirundoides
showed that adult females Calanusfinmarchicus
were shown to vary in carbon content by a factor
had a highly variable lipid and protein content (Fig 3). Peterson (1986) found that female
of 5, males of Limnocalanus macrurusby a factor
of 6, and the authors suggested that reproductive status and lipid reserve were the main variable factors which determined the carbon content. Size ranges of defined developmental stages have been documented, especially in some earlier studies on the population dynamics of copepod species. Marshall & Orr (1972) gave some examples for Calanusfinmarchicusfrom the Clyde Sea
area. Stage 5 copepodites sampled below 30 m depth in June varied by a factor of 1.56 in prosome length, and the range in wet weight of these animals would then correspond to a factor of 3.8. High variability in lipid content was reported for stage 5 copepodites of Calanus glacialis by
Bimstedt (1984). Although five individuals were pooled together, total lipid content could vary by a factor of 3 for a given depth. Hakanson (1984) also used groups of five individuals when quantifying the lipid classes in Calanuspacificus. Stage 5 copepodites, sampled off San Diego at different times of the year, showed ranges in wax ester content corresponding to a factor between 3.5 and 15.4. Triglyceride content varied less (2.7-7.8) and polar lipids the least (1.4-2.7). Stage 4 copepodites were considerably less variable.
podites of Calanusfinmarchicusfrom Loch Fyne
were significantly longer in samples from below 30 m depth than in samples from above, although the frequency distributions usually overlapped considerably. Since the diel vertical migration should ensure that individuals are subject to a variable depth, one would expect that the most actively migrating stages were most homogeneous. There is no such indication of less variability in the late copepodite stages, which are supposed to be the most active migrators. Furthermore, pump-sampling from 10 m depths
Calanus marshallae raised to adult stage under
controlled conditions in the laboratory were very variable in size, and suggested that variation in terminal size was due entirely to genetic effects. However, a test wherein the body length of the daughters was related to the body length of their mothers did not give any significant correlation, and the daughters' size was extremely variable. Because fecundity of this species is unrelated to the body size of the adult female, there would not be any obvious selective advantage to evolving hereditary dominance of large size (Peterson, 1986), however, the opposite may be true for other species. Pseudocalanussp. shows a positive relationship between body size of mother and offspring and fecundity is positively correlated with the size of the female (McLaren & Corkett, 1978). Feeding
Analyses of gut fullness and grazing rates of copepods collected both by nets towed through a water parcel (Fig. 5) and by pumps from discrete depths (Figs. 6, 7) indicate a very high variability
56 between individuals. Earlier functional models of the feeding dynamics of copepods focused on the food abundance and the size of individual food particles (e.g. Frost, 1972, 1977; Boyd, 1976). In recent years more attention has been paid to the quality of the food and the behaviour of the grazer (e.g. Poulet & Marsot, 1978; Alcaraz et al., 1980; Strickler, 1982; Paffenhofer & Van Sant, 1985; Van Alstyne, 1986; Price & Paffenhofer, 1986), and this has greatly increased the understanding of the mechanisms regulating the feeding rate of copepods. Nevertheless, results from these studies can not fully explain such a great variability as is shown in Figs. 5-7 and by BAmstedt (1984) and Bnimstedt & Ervik (1984), where a considerable part of the populations did not feed at all. BAmstedt (1984) suggested that individuals of Calanus glacialiswere intermittently feeding in arctic waters in summertime, but discontinuous feeding in a homogenous food environment has hitherto not been described for copepods. Price & PaffenhOfer (1986) suggested that changes of the time spent resting the feeding appendages is an important factor in regulating the food intake of copepods. However, for Eucalanus elongatus this
only varies by a factor of four over a wide range in food concentration, and resting is on the time scale of one second or less (Price & Paffenhofer, 1986). Even when newly captured copepods are held in a homogeneous suspension of a suitable food, individual grazing rate varies a lot (unpublished results). One factor therefore to which more attention should be given is the nutritional history of the animals. Reproduction events
Peterson (1986) observed that the variability in median developmental time to adulthood between individuals from different egg clutches of Calanus marshallae,held in an uniform food environment, was rather variable, ranging from 52 to 70 days. Since the individual variability in developmental rate may vary by a factor of two (Fig. 4 in Peterson, 1986) and durations of the two last developmental stages and of the egg-laying period
may be very prolonged in Calanus (Marshall & Orr, 1972) the age of adult females, developed from a single generation, may be very variable. Such age differences may certainly explain part of the great variability in gonad length shown by Calanusfinmarchicus and Metridia longa (Fig. 8).
The large and less variable size of gonads, shown by adult females in winter (Fig. 8) is consistent with the idea of gonad development being more or less independent of present food regimes in the overwintering generation (Tande & Hopkins, 1981; Runge, 1984). At other times food regimes greately influence the maturation processes and starvation causes the gonads to revert to an undeveloped reproductive state (Runge, 1984). Different copepod species have different time schedules for their egg production. The extreme forms, species that carry egg sacs (e.g. Pseudocalanus minutus, studied by Corkett &
McLaren, 1969) and those that produce eggs continuously (e.g. Acartia tonsa, studied by Parrish & Wilson, 1978) are both influenced by environmental factors such as food supply and temperature. However, these factors act on Pseudocalanus by only modifying the time interval between production of consecutive egg sacs (Corkett & McLaren, 1969; Corkett & Zilloux, 1975), whereas A. tonsa almost instantaneously regulates its production rate (Kiorboe et al., 1985). However, most species studied develop a clutch of oocytes to maturity synchronously, and spawn them within a relatively short period (Runge, 1984). If food and temperature regimes are sufficient, then spawning may occur in an endogenously controlled diel rhythm entrained by light (Marcus, 1985). Short-term experiments (
