ICES Journal of Marine Science: Journal du Conseil Advance Access originally published online on January 13, 2008
ICES Journal of Marine Science: Journal du Conseil 2008 65(3):332-338; doi:10.1093/icesjms/fsm180
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This article appears in the following ICES Journal of Marine Science issue: 4th International Zooplankton Production Symposium: Human and Climate Forcing of Zooplankton Populations [View the issue table of contents]
Copepod growth in detail: pattern similarity to decapod larvae
College of Oceanic and Atmospheric Sciences, Oregon State University, Corvallis, OR 97331-5503, USA
tel: +1 541 7374524; fax: +1 541 7372064; e-mail: cmiller{at}coas.oregonstate.edu
Miller, C. B. 2008. Copepod growth in detail: pattern similarity to decapod larvae. – ICES Journal of Marine Science, 65: 332–338.It is proposed that copepods grow between one moult and the next in much the same fashion as established by Klaus Anger and others for decapod crustacean larvae. The analogy is justified by commonality of (i) approximately isochronal development patterns, (ii) potential for continuously exponential growth at stage-to-stage resolution, and (iii) demonstrated points of reserve saturation. Thus, as for crab zoeae, the copepod pattern should be very fast initial growth, then slowing as activity shifts to preparation of the new exoskeleton prior to moult. As much as 80% of growth may occur in the first half of the moult cycle, with no growth at all in the last third. Establishing the exact patterns for copepods faces difficulties not presented by decapod larvae, and some solutions to these problems are suggested. Obtaining precise data will help to predict and interpret (model correctly) the effects of food limitation in the field.
Keywords: biomass determination, copepod, growth pattern, point of no return, point of reserve saturation
Received 5 July 2007; accepted 5 September 2007; advance access publication 13 January 2008.
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Likely copepod growth patterns |
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In order to appreciate the role of zooplankton in material flow and transformation in the sea, it is essential that their rates of growth and production can be determined and the factors of control understood.Planktologists have taken particular interest in copepod growth patterns, stimulated in part by the search for a shortcut to secondary production estimation for this crustacean group (Huntley and Lopez, 1992; Hirst and Sheader, 1997; Hirst and Lampitt, 1998; Hirst and Bunker, 2003; Hirst et al., 2003, 2005). That is because copepods are consistently a dominant proportion of the mesozooplankton in oceans and lakes, and mesozooplankton are important in the foodwebs leading to harvestable, large animals (primarily fish and squid). Despite this interest, available approximations of growth rates for copepods in the field remain crude and unreliable. I propose that good dividends could derive from learning the growth patterns of copepods with more precision than has been applied to date, particularly for the copepodite stages responsible for a major share of mesozooplankton tissue production. Initially at least, the work must be done on laboratory stocks, with transfer of implications to field results. The basic notion, proposed earlier by Carlotti and Nival (1991, 1992), and Crain and Miller (2001), is that copepods add biomass at rates strongly varying through their moult cycles in patterns similar to those demonstrated for crab larvae by Klaus Anger and others (Anger and Dawirs, 1981; Anger and Spindler, 1987; Anger and Ismael, 1997; reviews in Anger, 1998, 2001).
Crab larvae offer strong advantages for determining within-stage growth patterns compared with copepods. Many female crabs carry their eggs attached to their abdomen or abdominal legs until they hatch as zoeae, at a stage of development comparable to the copepodite stages of copepods. These larvae begin to feed, gain weight, and moult. Hatching in many or most species occurs in near synchrony that is sustained through several moults. Thus, a clutch can be progressively sacrificed to determine the time course of biomass increase. Individual variability can be modest because the eggs in a clutch are full siblings, so biomass determinations can be made for counted groups. A graph (Figure 1) from Anger (1998, 2001) gives the pattern for Zoea I of the spider crab Hyas araneus. Growth is very rapid at first, with 82% of the total stage dry-weight increment laid up in the first half of the moult cycle. Then growth slows, presumably because morphogenetic preparation for the next moult takes up more of the ingested nutrition. In the final 30% of the moult-to-moult interval, there is no growth at all in the sense of biomass increase. Ingestion and assimilation also decrease markedly after about half of the interval.
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Specific points in this larval-crab growth pattern are associated with aspects of the moult cycle (reviewed in Anger, 2001). Completion of an initial fraction of moult-cycle growth, usually an increase of 60–70% over biomass at moult that is accomplished in only 20–30% of the moult cycle, is associated with initiation of the premoult sequence of epidermal events. This transition is often designated D0 in a scheme of epidermal stages A to E: A, initial post-moult during body expansion by drinking; B, exoskeletal thickening by secretion of additional chitin; C, intermoult; D, premoult divided into substages of formation of new exoskeleton; E, ecdysis. The first localized separation of epidermis from the exoskeleton (apolysis), usually around the tips of limbs bearing long setae, occurs in D0. There is tight, hormonally controlled correlation among these stages to the division phases (M, G1, S, G2) of cells multiplying for epidermal expansion and presumably for increasing segmentation and other complexity (Freeman, 1993).
Significantly for the comparison with copepods, D0 in crabs is associated with a "point of reserve saturation" (PRS), after which moulting will proceed to the next instar even if food is entirely withdrawn at any subsequent time. Transition from C to D0 is hormonally controlled, an event likely enabled by passing a rather definite tissue-mass to body-volume ratio, a triggering condition factor. The existence of PRS is an important feature of decapod larval development (Anger and Dawirs, 1981; Anger et al., 1981; Dawirs, 1984, 1986; Anger and Spindler, 1987; Staton and Sulkin, 1991; Abrunhosa and Kittaka, 1997; Anger, 2001). The exact timing varies among species, but for many, withdrawal of all food at only 
30% of the moult-to-moult interval will not inhibit moulting to the next stage. By PRS, the larva has been hormonally triggered to complete exoskeleton development and to moult. If the larva is fed immediately after such a moult during starvation, some extra time will be required for it to recover and complete the next stage, and mortality rates are typically somewhat enhanced (Anger and Dawirs, 1981).
Decapod crustacean larvae also have a point of no return (PNR; Anger and Dawirs, 1981; Anger et al., 1981; Dawirs, 1984, 1986; Staton and Sulkin, 1991; review in Anger, 2001; Paschke et al., 2004). If not fed for a sufficiently long interval after a moult, they will not be able to resume growth even when given copious food, and they die. The character of a possible PNR in copepod development remains to be established, as discussed at the end of this paper.
An analogy between within-stage growth patterns in copepods and those of decapod larvae is supported by three strong similarities already established. First, both have roughly constant stage durations, so called isochronal development (Miller et al., 1977). There has been much debate about this in regard to copepods (e.g. Landry, 1983), and there are deviations. For example, when N3 is the first-feeding naupliar stage, which is typical of broadcast spawning forms like Calanus, it is longer than the other naupliar stages, particularly longer than N1 and N2. There is usually also definite extension of intermoult intervals at the last copepodite stages in Calanus and many other species, particularly extension of C5. However, data for Calanus agulhensis and Calanoides carinatus (Peterson and Painting, 1990) and for Calanus finmarchicus (Campbell et al., 2001) demonstrate that the main sequence of development, even in Calanidae, has nearly constant intervals. A good demonstration of the isochronality of decapod larvae is shown by Anger (1998, Figure 2 here), based on data from a thesis by Schultze (1993) for Pandalus montagui. That shrimp moults at remarkably equal intervals as it passes through eight larval stages.
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Second, looked at on a stage-to-stage basis (as opposed to durations within the moult cycle), both decapod larvae and copepods add biomass approximately exponentially, when provided with replete nutrition. A good example for decapods is the larval growth pattern of the saltmarsh crab Chasmagnathus granulata, which, at Zoea I, II, III, IV, Megalopa, and Crab I, has dry weights of, respectively, 190, 356, 757, 1661, 3211, and 5468 µg, increasing about twofold per stage (Anger and Ismael, 1997). Many pelagic, calanoid copepods can add biomass at nearly constant, exponential rates through all or most of their development, if they are fed a replete and qualitatively suitable diet. Again, there are deviations: (i) non-feeding, early naupliar stages lose weight rather than grow; (ii) possibly growth is slower during the metamorphosis between the sixth naupliar and first copepodite stages (e.g. Acartia, Miller et al., 1977); and (iii) it is likely that storage lipid added in late stages increases body mass at a rate different from early body growth. However, the literature provides many examples of (or approximately of) exponential growth. As a small sample, Acartia hudsonica (Landry, 1978), Acartia californiensis (Miller et al., 1977), Pseudodiaptomus marinus (Uye et al., 1983), and Pseudocalanus newmani (Lee et al., 2003) add weight in roughly constant ratios between stages. The excellent data of Vidal (1980a, b) and Campbell et al. (2001) for two different species of Calanus show closely exponential initial growth, then slowing in the last stages, C4 and C5.
There are some datasets that seem to show copepod growth that is even more extreme than continuously exponential. Consider the growth pattern of Pseudodiaptomus hessi found by Jerling and Wooldridge (1991; Figure 3). Their dataset has the advantage that the animals were actually weighed, rather than including weights based on a general weight-to-length ratio (Rey-Rassat et al., 2004, stress the importance of this). However, weights were determined after quite long preservation, and age was determined by me for the figure by summing stage durations provided by Jerling and Wooldridge (1991) as B
lehrádek functions determined in the laboratory. Therefore, some uncertainty remains about actual weight-at-age. The food regime, however, was just the particulate contents in water from the Sundays River estuary, South Africa, where the P. hessi were collected.
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Third, both decapod larvae and copepodites have a PRS early in each moult cycle. For crabs and lobsters, PRS has been explicitly demonstrated (citations above). The demonstration in copepods is less refined. Copepodites of a given stage collected at sea and placed in filtered seawater (starved) will continue to moult until remarkably large percentages have reached the next stage. In experiments with Calanus pacificus C4 collected close to the California coast (Miller et al., 1984, their Figures 3, 4, 6, 8, 9), the fractions moulting rose progressively over 2 days to typically 50–70% of the numbers initially sorted. Clearly, copepodites have exactly the same capacity as crab zoeae to establish a PRS very early in the moult cycle.
Based on these similarities, decapod larvae are a good model for the detailed growth pattern of copepodites.
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Obtaining copepod growth patterns at within-stage detail |
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We lack the datasets necessary to examine copepodite biomass increase at within-stage resolution. Almost inevitably, such data must be developed by laboratory rearing. For just one copepodite stage (e.g. C3), the data would be a table, for a statistically adequate number of individuals distributed throughout the age range of the stage, of (i) exact age-within-stage (time since the prior moult), (ii) biomass as dry weight or carbon content, and (iii) body volume or at least body length. We lack such data because, on the whole, it has not been possible to raise groups in sufficient moulting synchrony for a stage to have narrow variance in age added since the last moult (e.g. Sciandra, 1986; Peterson and Painting, 1990; discussed by Lopez, 1991). However, Campbell et al. (2001) nearly obtained developmental synchrony with cohorts of Calanus finmarchicus reared on a diet apparently close to ideal. They did not determine within-stage biomass increments, but another rearing with equal synchrony might allow it.
In addition, individuals are too small in many species and stages for biomass determination on single specimens. Readily available measurement techniques (dry weights by electro-balance, carbon analysis, etc.) are not sensitive enough for specimens of any but the largest stages of large species. The biomass measures need to be precise to within a few per cent. Length is needed because overall body size varies in a given stage by substantial ratios; for example, length of Calanus finmarchicus C5 varies by a factor of 1.7 and body volume by a factor of 4 (Miller et al., 2000).
Despite these difficulties, there are ways forward to define the copepod growth pattern with higher resolution than is currently available (4-h resolution by Carlotti and Nival, 1991). A system has been developed at Oregon State University to take digital pictures every six minutes of each of 24 female copepods in dishes (Miller et al., in litt.). The pictures have allowed us to determine to within 6 min (0.1 h) when clutches of eggs are produced. The 24 dishes, mounted on plexiglas sleeves hanging from a motor-driven carousel, are pulled around an annular plexiglas trough filled with precisely temperature-regulated water once every 6 min. As each dish passes the camera that is focused on its bottom, the camera takes a picture and transfers it to a computer server. Modern digital storage capacity allows thousands of pictures to be accumulated at reasonable cost, and they can be scanned at suitable intervals to determine the timing of the events they record. In place of spawning dishes, beakers containing one copepodite with a replete diet can be hung from the carousel. New moults sink and are visible in the photographs of the beaker bottoms. Time marks on the photos (or times recorded with the computer files) will show when new moults first appear and thus determine the time at zero age within the new stage. Once the moulting times of a set of copepodites are known, suitable ages after the moult can be assigned for determining biomass. More than one camera arrangement can be imagined, perhaps a system with the camera moving rather than the dishes that could take recurring pictures of many more than 24 specimens.
Then, because of the effect of body size (body volume = f[body length]) on biomass, weights must be determined for each single specimen. Biomass could be dry weight determined with a balance, or it could be carbon content. Dry weight determinations of single individuals will only be feasible for larger copepods. For example, the C3 of Acartia will grow from 0.8 to 1.8 µg, considerably less than the weights of the tared metallic foils needed for drying and weighing them. Very good practice with an electrobalance will provide weights to ± 0.2 µg, at best, considering the error propagation of the tare weighing and tare–animal weighing. For purposes of determining small increments of growth through the moult cycle, these errors of 10–25% are far too large. Suitably precise results can probably be obtained for the copepodite stages of larger species. The C3 of Calanus will grow from 25 to 45 µg, for which the precision of weighing is sufficient to provide a very good within-stage growth sequence.
An appealing alternative is direct carbon analysis. Salonen (1979) reported the development of a high-temperature carbon analyser that, he claimed, could be calibrated to estimate minuscule amounts of carbon, down to 0.01 µg without sample weighing. The analytical device was a catalytic furnace, comparable with that in any CHN analyser, burning samples with high-purity oxygen. Water was condensed from the resulting mixture of gases, and carbon was determined by non-dispersive infrared (NDIR) detection of the CO2 content. Consequently, NDIR analysis of carbon at the necessary sensitivity is certainly possible, and the current generation of Schimadzu machines (e.g. their TOC-VCS/TOC-VCP model) applying oxidation and NDIR can determine as little as 4 ng of carbon in small water (or seawater) samples (100 µl). However, Schimadzu's furnace attachment for solid samples requires 100 µg of carbon, which is too much, about equivalent to the content of an adult Calanus. The combustion gases from the furnace of a standard CHN analyser could be redirected to a suitable NDIR detector, and suitable detectors are available. A machine of the necessary combined capability is not currently on the market, although one could be built to determine the growth pattern of copepods.
If the basic weight-at-age for a suitable stage can be obtained, combining the suggestions above, then a way must be found to account for the effect on biomass of variation in body volume or linear dimensions. After that standardization, a sort of standardized "Anger graph" (like Figure 1) could be developed for copepods. For example, something like the approximate formula for body volume as a function of length in C. finmarchicus C5, which was developed by Miller et al. (2000) from optically determined dimensional data, could be applied. That is,
Body Volume = 0.0292 (Prosome Length)3.67.
The exponent larger than 3.0 implies that shape is not constant with size, that longer bodies are relatively wider. Weights at specific ages-within-stage could be compared as ratios with volumes estimated by such a function from simple length measures. Species- and stage-specific volume = f(length) models would be needed and probably can be developed directly from the age–length–mass tables for the copepodite stage under study. The resulting data can be expected to follow a curve like that in Figure 4, which is just a representation of the analogy to decapod larvae.
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The observations can readily be extended to determine the PRS for copepodites. After different intervals with replete nutrition, the animals would be transferred to filtered seawater and their subsequent moulting (or failure to moult) monitored. PRS would likely be reached at
30% of the moult-to-moult interval, or when the animal had reached approximately three-quarters of its fully fed final weight. It should also be possible to examine the interaction of varying nutrition levels with the growth pattern and to define PRS in terms of weight or condition factor, rather than in terms of the required duration of initial feeding on a replete diet to establish reserve saturation. The latter has consistently been the form of data for identifying PRS in decapod larvae. A growth-limiting diet might well allow an animal to reach PRS, but only after an extended period. |
Discussion |
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If someone is persuaded by this argument to obtain the data for determining the growth dynamics of pelagic copepods at high within-stage resolution, what will we gain? Clearly, it can be done, but the necessary miniaturization of the measurements means that it will be difficult. What would the field gain by having this information? Why is the analogy to decapod larvae not sufficient to inform our studies on the role of copepods in pelagic ecology?
Copepods are the archetypal mesozooplankton, so they represent that whole trophic complex in many ecosystem models (e.g. Landry, 1975; Steele, 1998; Steele and Clarke, 1998; Peña, 2003; Lancelot et al., 2005). Moreover, copepod developmental timing is important in many models of their population dynamics (e.g. van den Bosch and Gabriel, 1994; Miller et al., 1998; Carlotti and Wolf, 1998; Speirs et al., 2006). However, both classes of model generally apply imprecise growth mechanics (or none). The partial uncoupling of biomass growth from stage-to-stage development implied by the PRS phenomenon means that fully representative models, especially those invoking food limitation, should include detailed representation of the timing and nutritional responses of growth.
Food limitation commonly affects mesozooplankton, and among copepods it almost certainly affects older stages preferentially (Hirst et al., 2003). Because of the PRS phenomenon, it can be seen in the field in the proportions of individuals in different tooth-formation stages (Crain and Miller, 2001). After the onset of near-starvation, individuals accumulate in the post-moult phases of successive stages, whereas later moult-cycle stages disappear. Initiation of tooth development in copepodites apparently occurs at the same stage in development as PRS, much as PRS is closely coupled to the D0 stage (initial integument apolysis) of the decapod moult cycle (Anger and Spindler, 1987). Much effort has gone into understanding food limitation effects on copepods, particularly work by Vidal (1980a, b) and Klein Breteler et al. (2004 and references therein), but that work lacked a refined, underlying model of growth and development mechanics. We could draw a suitable model from the analogy to decapods, but it would be better to have real, copepod-specific data.
As stated in the initial paragraphs, if a decapod larva is subjected to a period of starvation soon after moult and if that persists long enough, the larva will not recover its capacity to eat and grow when food reappears. It dies. It has passed the PNR. Certainly, copepods also exhibit such limits on their ability to recover from starvation, limits with the potential to remove important trophic components from pelagic ecosystems. Sometimes such removal will be in process while the animals are still alive to be captured in plankton samples, misleading observers about the effective and future trophic relations in the ecosystem. Techniques for experimentation with copepodites of accurately known age-within-stage will allow more precise study of starvation and malnutrition effects on copepod growth, including probabilities for recovery and the extent of developmental delays. We know from work on starvation in adults and C5 (e.g. Dagg, 1977; Koski and Klein Breteler, 2003) that different species differ strongly in their ability to persist through and recover from starvation; those with substantial storage lipids survive longer. There are also studies of adult females in which recovery of egg production after starvation events was the issue of concern (e.g. Niehoff, 2000).
It is likely that starvation has different effects on naupliar and copepodite stages. Tsuda (1994), for example, showed that copepodites of Pseudocalanus newmani survive longer without food than nauplii, but, short of dying, their capacity to recover once food is again available (i.e. the existence of a PNR) remains unknown. Lopez (1996) has performed an approximate determination of PNR in naupliar stages of Calanus pacificus that were fed, or not fed, with a culture of Procentrum minimum. She states "... survivorship and development rate during the remaining naupliar stages were reduced when initial feeding was delayed for 10 h after moulting to N3. In otherwise well fed stages N3–N6, development and survival were reduced after starvation periods >6 h and >14 h, respectively...".
There are effects of starvation on copepods comparable with the decapod PNR, and Lopez cites Anger et al. (1981) in making that association. Starvation effects similar to PNR have been modelled for copepods by Batchelder et al. (2002), replacing the notion of a tolerable duration of starvation with a minimum survival weight approached by modelled catabolism. Probably a minimum weight (or condition factor) is a better form of data than has usually been provided for decapod larvae (or for Calanus nauplii by Lopez), where PNR has only been characterized as the fatal duration of complete absence of food before a standard replete diet is provided. It is likely that minimum survival weights or condition factors could be discovered by experiments with animals of known age-within-stage. Determinations of PNR by Paschke et al. (2004) for early larvae of Crangon show that starvation resistance varies seasonally, with larvae from larger winter eggs better able to recover from longer starvation than those from smaller summer eggs. Thus, time to PNR is certainly more complex than has been demonstrated for either meroplankton or holoplankton, varying with every aspect of nutrition: food quantity, quality, timing of availability (e.g. Gimenez and Anger, 2005), and parental investment in eggs. PNR is certain to exist in copepods, for copepodite stages as well as nauplii. Both its timing and the low food levels inducing it should be determined. Doing that in light of high-resolution growth patterns will show us the details of the interaction of copepods with the nutrition available in their habitat.
From the decapod analogy, we know that copepodite growth rate almost certainly varies through the moult cycle, even with replete nutrition. Less certainly but very likely, rates of feeding and metabolism will also vary with moult phase. Therefore, correct interpretation of copepod physiological data requires attention to the moult-cycle phase of observed copepodites. In many cases, copepods develop in temporally focused cohorts; for high-latitude populations, these are annual or biennial cohorts. If we collect, say, C4 of a species of interest for measurements of rates, the age-within-stage composition will very likely advance with the progress of the seasons, i.e. with the developmental advance of the population cohort. Therefore, measured rates will also vary. Possibly, the age-within-stage composition of a population at the moment it is studied could be approximated from proportions of tooth-development stages (Crain and Miller, 2001). For example, the decapod analogy (Figure 1) suggests that a stock of copepodites all at older ages within their stage (all with new teeth forming on the epidermis of the gnathobases) is likely to have lower feeding rates than stocks at younger ages. Because late-phase animals would not be adding weight, they would be feeding very slowly.
In sum, knowing the detailed growth dynamics of copepods will lead to better understanding of pelagic ecology. The analogy with decapod crustaceans suggests that growth in each instar will be rapid initially, then slow and later stop well before the moult from the stage. Exoskeletal morphogenesis takes place during the final phase. The requirements for such studies of copepods are more difficult than for studies of crab or shrimp larvae, but collecting suitable data is possible. Application of the decapod larval analogy does not, unfortunately, suggest that demonstrating the within-stage growth patterns of copepods will return us to a simple, reliable method for estimating the secondary production attributable to a given species or stage of planktonic copepods. That Holy Grail of mesozooplankton ecology will likely remain hidden awhile. However, understanding within-stage growth processes will help us to explain why copepod development is less food-sensitive than growth and to predict the effects of that on size distributions. It will provide tools to demonstrate starvation when it occurs in the field and for assessing the effects of nutrition on mortality patterns. It will help to explain the outcomes of moulting-rate determinations and other field-based evaluations that are affected by cohort structure. The insights will branch out in many directions.
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