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Rapp. P.-v. R éun. Cons. int. Explor. M er, 191: 330-338. 1989 Nekton and plankton: some comparative aspects of larval ecology and recruitment processes Hein Rune Skjoldal and W ebjørn Melle Skjoldal, Hein R une, and Melle, W ebjørn. 1989. Nekton and plankton: some comparative aspects of larval ecology and recruitment processes. - Rapp. P. v. Réun. Cons. int. Explor. M er, 191: 330-338. The larval ecology of fish and zooplankton differs in many respects. The fecundity of fish is 3-4 orders of magnitude higher than for zooplankton. Despite this, zooplank ton eggs and larvae are in general much smaller than fish larvae. Zooplankton larvae are predominantly herbivores whereas fish larvae feed on larger particles and are predominantly carnivores. Egg production in zooplankton is closely coupled with feeding conditions of the females, whereas that of fish is more distantly related both temporally and spatially. The ability to endure starvation is roughly equal for larvae of fish and zooplankton despite the smaller size of the latter. A m ajor difference in terms of predation is that fish eggs and larvae are large enough to be preyed upon by plankton-feeding fish, whereas eggs and larvae of zooplankton are not. Loss of individuals during larval drift is much more likely for fish with spawning migration as part of the life cycle than for zooplankton. Fish larvae seem therefore more prone to suffer losses due to food limitation, predation, and variable currents than do larvae of zooplankton. This is in accordance with higher mortality rates of fish larvae than of zooplankton larvae. The relative contributions by the three m ajor factors (food limitation, predation, and vagrancy) causing this high mortality are difficult to separate because they are interrelated and variable. In the fish recruitment variability problem we are probably looking for relatively small differences in mortality rate to explain large variations in num ber of recruits. Hein Rune Skjoldal and Webjørn Melle: Institute o f Marine Research, P.O. B ox 1870, Nordnes, N-5024 Bergen, Norway Introduction By definition plankton and nekton are differentiated by their respective abilities to determine their horizontal distribution. Fish are a m ajor group of nekton which use their ability to swim for purposes such as feeding and reproduction. Many species migrate to restricted spawning areas which are located in relation to the water circulation pattern so as to ensure transport of recruits back into m ajor feeding areas (Harden-Jones, 1968; Sherman et al. , 1984; Dragesund and Gjøsæter, 1988). Z ooplankton, in contrast, spawn over a much wider part of their distribution area than do fish, and there is little evidence for behaviourally localized spawning areas. The large variability in recruitment of commercial fish stocks has received long-lasting scientific attention. Despite this, the mechanism involved in recruitment processes have not yet been properly resolved. Current research activities are guided by three m ajor groups of hypothesis: that the recruitment variability is due to (1) food limitation, (2) predation, or (3) physical oceanic variability (Sissenwine, 1984). 330 Nekton and zooplankton have one thing in common, both groups being part of the plankton in the larval stage of their life cycles. They are therefore subject in part to the same ecological recruitment processes. Here we com pare their reproductive and larval ecology, emphasizing similarities and differences in basic eco logical properties of nekton and zooplankton. We have done this in a very general way, using fish and crus taceans (with a bias towards copepods) as typical rep resentatives for the two groups. Where possible we have chosen our examples from the Barents Sea ecosystem. Spawning behaviour Many marine fish populations have more or less welldefined spawning areas where the adults aggregate after a spawning migration to mate and spawn. The location of spawning areas is the result of adaptation to the physical regime which disperses and transports the lar vae and juveniles into areas which are favourable for growth, survival, and further reproduction (HardenJones, 1968; Sherman et al., 1984; Sinclair, 1988). The dominant commercial fish stocks in the Barents Sea provide many clear examples of this (Dragesund and Gjøsæter, 1988). The limited swimming capacity of zooplankton prevents them from performing extensive horizontal spawning migrations to well-defined spawning areas like fish. Instead they spawn over most or all of their area of distribution. It is likely, however, that specific repro ductive behaviour has evolved as a mechanism for aggregation to improve the chances of encounter between the sexes. Swimming speed is related to body size, and this sets upper limits to the distance and size of aggregations. The physical dispersive forces in the ocean are generally much stronger in the horizontal than in the vertical direction. Aggregation in the vertical would therefore seem to be a mechanism whereby zooplankton could meet for reproductive purposes. Many zooplank ton species living in spatially restricted environments such as estuaries or coral reefs have evolved behavioural patterns which contribute to their retention (Sinclair, 1988). A seasonal vertical migration upwards in spring from overwintering in deeper water is a common phenom enon for many open water zooplankton species (e.g. Østvedt, 1955). Aggregation in the surface layer is a possible mechanism for concentrating the population, thus enhancing the probability that males and females meet. This probability would decrease with decreasing abundance per area. Reproduction would therefore be less intense in the border areas of distribution than in the central areas. Swarming behaviour could play a more important role in reproduction of zooplankton than has generally been recognized. Several species of copepods have been observed to form dense local monospecific swarms con sisting mainly of adults (U eda et al., 1983). Calanus finmarchicus can form dense red patches in the surface layer (Wiborg, 1976). Krill occur regularly in schools or swarms of different sizes and probably for several different purposes (H am ner et al., 1983). Swarming in relation to reproduction was indicated for Meganyctiphanes norvegica by Nicol (1984). In fishes mating and spawning usually occur simul taneously. For most crustacean zooplankton, on the other hand, mating involves transfer of a spermatophore that is used to fertilize the eggs when subsequently spawned. Egg size and fecundity The fecundity of fish can be very high, and, as a conse quence, the size of the eggs is small relative to the size of the adult fish. The mean ratio of egg to adult volume is about 10-7 for fish species from the Barents Sea as shown in Figure 1. The difference in size between egg and adult is considerably less for zooplankton, with a Species.C alanus g- < o gla c ia lis . C. hyperboreus. M etrid ia ,__________ . , longa. P s eu d o calan u s E u chaeta = -* .____________ . f i n m ar ch ic us . C. .___________. sp. . norvegica. .-------------------- . T h y s a n o e s s a r a sc h ii. T. ^ ----------------------- . i n er m is . , T. l o n g i c a u d a t a . w < ?v----------------- . , M allotus v illo s u s . .-------------------------------- . C lu p e a h a r e n g u s . ._______________________ . Boreogadus saida. Pollachius ------------ - viren s. , Melanogram m us a e glefinus. . Gadus m orhua. .____________________________. i i i 1 i 1--------1------- 1--------1--------1------- 1 1Ö6 1Ö5 1o‘ 10"3 1Ô2 101 10° 101 102 103 10‘ V o l u m e (ml ) Figure 1. Egg volume (left point) related to body volume of mature females (right point) of zooplankton and fishes, pv = volume including perivitelline space. Based on data from Bogorov (1959), Zelikman (1961), Pertsova (1966), H em pel and Blaxter (1967), Blacker (197i), Schopka (1971), G jøsæter and Monstad (1973), Williams and Lindley (1982), Bergstad et al. (1987), Kjesbu (1988), P. D alpadado, H. Gjøsæter, T. Jakobsen, T. Jørgensen, W. Meile, and K. F. Wiborg (unpubl. data from scientific cruises and commercial catches, Institute of Marine Research, Bergen). mean ratio of egg to adult volume of 10-3 for copepods and 2 • 10" 4 for krill (Fig. 1). Despite being small relative to the adult, fish eggs are still almost 2-3 orders of magnitude larger in volume than eggs of krill and cope pods (Fig. 1). On a logarithmic scale, the variation within each of the 3 groups, copepods, krill, and fish, is relatively limited. There is, however, a fairly strict relationship of increasing egg size with increasing size of species for copepods and krill as well as other crustacean taxa (Mauchline, 1988). D ata on fecundity of zooplankton compiled by Paffenhöfer and Harris (1979) show a variation from <10 to 1 .4 -104 eggs per female. For fish the fecundity can be as high as 3 - 107 (Blaxter, 1969). The ratio between gonad weight and body weight for fishes ranges from 0.04 to 0.65 (Gunderson and Dygert, 1988). A similar range of 0.02 to 0.50 has been reported for the ratio between brood volume and body volume of copepods (Mauchline, 1988). Thus the reproductive effort is roughly similar in fishes and zooplankton. Given the difference in size between eggs and adults, the fecundity is therefore 3 -4 orders of magnitude higher for fish than for zooplankton. Since fish in general spawn repeatedly over several years whereas most zooplankters spawn in only one season, the difference in total fecundity over the life cycle is even greater. 331 Feeding ecology The feeding ecology of fish larvae has been the subject of numerous studies (reviewed by H unter, 1981 ; Turner, 1984). Zooplankton is the predom inant food for most species of fish larvae, with copepod and barnacle nauplii, tintinnids, copepodites, cladocerans, gastropod lar vae, pteropods, and appendicularians as common food items (Turner, 1984). Phytoplankton can also constitute an im portant part of the diet of young larvae, par ticularly of clupeoid species (Govoni et a l., 1983). There is evidence that phytoplankton also may play a role in the first feeding of cod larvae (Klungsøyr et a l., 1989). Much less has been done concerning the feeding ecology of larval stages of zooplankton. Nauplii of the few copepod species that have been investigated have been found to feed primarily on phytoplankton (Turner, 1984). A common feature has been that phytoplankton in the smallest size range have been grazed with low efficiency, grazing being predominantly on algae of medium or large size (e.g. Berggren et a l., 1988). The larval stages of krill are also assumed to feed primarily on phytoplankton (Mauchline and Fisher, 1969). T he size-efficiency hypothesis (Brooks and Dodson, 1965) postulated that large size produced a competitive advantage in that a large consumer would be able to utilize both small and large prey items. It has been shown that the total size range of prey increases with increasing size of fish larvae (H unter, 1981; Govoni et al., 1983). Pearre (1986) found, however, that more realistic ratio-based indices for trophic niche breadth were in general constant as the fish grew and showed no consistent trend with size of fish species. He further concluded that, combined with a constant or declining prey biomass in increasing geometric size classes (Shel don et a l , 1972; Platt and D enm an, 1977), a constant trophic niche breadth would imply a constant or declin ing prey biomass as predators become larger. Extensive studies of Canadian freshwater lakes have revealed a consistent pattern in size distribution with two pronounced peaks in the phytoplankton and mesozooplankton size ranges respectively (Sprules et al., 1983). In marine benthic communities there appears to be a similar consistent biomass distribution with peaks corresponding to bacteria, meiofauna, and macrofauna respectively (Schwinghamer, 1983). Sprules et al. (1983) suggested that a peaked size spectrum similar to that of lakes may also be the case for marine waters with large seasonal variations in climate and productivity. Peaky size distributions may be characteristic for young organ ism assemblages, whereas the flat spectrum may be a feature of old and m ature communities (McCave, 1984). The limited num ber of size spectra for tem perate and high latitude marine environments tend to support a general p attern with peaks in the phytoplankton and mesozooplankton size ranges (Schwinghamer, 1983; Hargrave et al., 1985; Witek and Krajewska-Soltys, 332 1987). The trough between these peaks is in the region of about 50-200 urn. This coincides with the size region of prey for most first-feeding fish larvae (H unter, 1981). The general nature of the minimum in particle con centration around 100 urn needs further confirmation. It is possible, however, that fish larvae, due to their size, feed in a minimum region of the particle size spectrum. Superimposed on any such general size spectrum, there will no doubt be large temporal variation. The spring phytoplankton bloom is a dramatic wave in pri mary production. Overwintering zooplankton spawn, and the resulting new generations develop as distinct cohorts (e.g., Krause an d T rahm s, 1982). The dynamics of these events lead to marked changes in the size distributions, as exemplified by data from St Georges Bay, Nova Scotia (Hargrave et al., 1985). The timing of occurrence of suitable prey is therefore of great im portance in addition to average abundance levels. There is a marked difference between plankton and fish in the dependence of egg production on the feeding regime. Egg production of many herbivorous zooplankters such as copepods and krill is closely related to the current feeding conditions and food intake (Kiørboe et a l., 1985; Ross and Q uentin, 1986). This acts to increase the chances that zooplankton larvae, which feed roughly on the same food as the adults (Berggren et al., 1988), will hatch at a time and place when and where the phytoplankton concentration is high. The egg pro duction of fish, on the other hand, is much more distantly related to the present feeding conditions both temporally, spatially, and qualitatively. This produces a much looser coupling between the occurrence of larvae and their food for fish than for zooplankton. M etabolism and starvation The length of time an animal can endure starvation is a function of metabolic rate and am ount of available body reserves. The am ount of reserves possessed by larvae at hatching varies among groups and species. Nauplii of the larger calanoid copepods do not feed during the first naupliar stages. Calanus finmarchicus and C. helgolandicus start to feed in stage III (Marshall and Orr, 1966) and the larger species C. hyperboreus in stage V (Conover, 1962). Several carnivorous copepods such as e.g. Euchaeta norvegica do not feed in the naupliar stages at all (Matthews, 1964). The duration of the non feeding naupliar period is, at 5°C, about 1.5 weeks for C. finmarchicus and about 3 weeks for C. hyperboreus (Tande, 1988). Naupliar stages III and IV of C. pacificus experienced 50% mortality after 4-5 d of starvation at 15°C (Fernandez, 1979). For smaller nauplii the time they can endure starvation can be even shorter (Dagg, 1977). The nauplii and metanauplius larvae of krill have non-functional mouthparts and feeding starts in the first calyptopis stage (Mauchline, 1980). In Antarctic krill Euphausia superba, the development of the non-feeding stages lasts about 20 d at 0°C, whereas the first feeding stage (calyptopis I) survives about 6 d without food (Ikeda, 1984). Z oea larvae of several benthic crus taceans have 50% survival after 3-15 d of starvation (Lang and Marcy, 1982). The survival time of fish larvae under starvation shows considerable variation among species. McGurk (1984) summarized information on larvae of 25 species of mar ine fishes. The time from fertilization to the age of irreversible starvation was strictly correlated with the time from fertilization to absorption of the yolk (r = 0.98) and inversely correlated with tem perature (r = -0 .9 1 ). The time from hatching to absorption of the yolk ranged from 1.5 to l i d . whereas the time from absorption of the yolk to the age of irreversible star vation ranged from 0.5 to 15 d (McGurk, 1984). For northern species these times at am bient tem perature were about 6 and 5 d for cod and haddock and 9-10 d for herring. It appears from the data reviewed that the capacity of starvation for fish larvae is roughly similar to that of zooplankton larvae. Weight-specific metabolic rate generally shows a clear inverse relationship with body size (e.g., Ikeda, 1985). Using such a relationship and assuming that half the body mass could be metabolized prior to death, Threlkeld (1976) developed a simple model to predict survival time during starvation. According to this model, at 20°C, a copepod nauplius of 1 u.g dry weight would survive for 3 d without food whereas a fish larvae of 100 |j,g would survive for about 9 d. Fishes have annual production/biomass (P/B ) ratios that are on average 4 5 times higher than those of invertebrates of the same size, reflecting a generally higher metabolic activity (Banse and M osher, 1980). This difference in metabolic activity, if shown also by the larval stages, would counteract the larger size of fish larvae, resulting in the fairly equal starvation potential for larvae of the two groups. Predation In recent years there has been increasing attention to predation as a possible cause of recruitment variability in fish stocks (H unter, 1981; Sissenwine, 1984; Bartey and H oude, 1987). The predation impact on fish eggs and larvae has been assessed for one or a few potentially important predators (e.g., Möller, 1980; D aan et al., 1985), but data on total mortality due to predation are lacking. For zooplankton eggs and larvae our knowledge on predation mortality is even more limited. The difference in size of eggs and larvae between zooplankton and fish makes them vulnerable to pre dation from different parts of the predator size spec trum. Cyclopoid copepods could be important as predators on copepod eggs and nauplii. They are widely distributed and occur often in high abundance. Species of Oithona are generally considered to be omnivores or carnivores (Turner, 1984). Oithona similis and O. nana have been found to prey on copepod nauplii (Marshall and O rr, 1966; Lampitt and Gamble, 1982). The vertical distribution of Oithona copepodites in the Barents Sea is often similar to that of copepod nauplii (Ellertsen et al., 1981). O ther forms among the smaller plankton, such as the dinoflagellate Noctiluca (Daan, 1987), may also predate on zooplankton eggs and larvae. Eggs and larvae of zooplankton are an important com ponent of the diet offish larvae (Turner, 1984). The abundance of fish larvae is considered to be generally too low to affect the density of their prey (Cushing, 1983), and they have therefore limited effect on the mortality of zooplankton eggs and larvae. Predators on fish eggs and larvae belong to a variety of animal groups, such as ctenophores, medusae, chaetognaths, polychaetes, crustaceans, squids, fish, and birds (Hunter, 1981; Bailey and H oude, 1987). A major difference between plankton and fish is that the eggs and larvae of the former are generally too small to be preyed upon with any efficiency by planktivorous fishes (Hardy, 1924; D aan, in press). Fish eggs and larvae, in contrast, are big enough to come into the predation realm of pelagic fish. This may give rise to significant differences in the predation pressure exerted on eggs and larvae of fish and zooplankton respectively. Fuiman and Gamble (1988) considered predation by fish to be more im portant than predation by invertebrates as a source of mortality of fish eggs and larvae. The schooling and migratory behaviour of planktivorous fishes allows them to search through extensive areas and concentrate in areas with abundant food. This probably enables them to exploit their food resource more efficiently, resulting in relatively high predation pressure on their prey. Aggregation of pelagic fish in areas with high abundance of fish eggs and larvae could be a direct response, but it could also be indirectly cued as a response to high abundance of zooplankton in the same area. The vulnerability of eggs and larvae to predators are affected by a wide range of factors, both intrinsic and external (H unter, 1981; Bailey and H oude, 1987) of which patchiness in distribution and anti-predatory behaviour are most im portant. McGurk (1986) showed that the rate of mortality of fish eggs and larvae was positively correlated with the degree of patchiness in distribution. This is contrary to what has been anti cipated from theoretical consideration of spatial distri bution, search time, and satiation (Gulland, 1987), and could be due to the behaviour of predators and prey (McGurk, 1987). It is possible that, for instance, plank tivorous fish concentrate their foraging effort in areas with high and patchy distributed prey abundance. 333 Populations of fish in the Barents Sea can be used to Patchiness occurs at various spatial scales. On a large illustrate this point. Capelin (Mailotus villosus) is a scale it seems clear that the restricted spawning areas dominant planktivorous fish which has a large scale of fish result in higher patchiness for fish than is the case for zooplankton. Within a spawning area there is seasonal migration northwards following, with a time lag, the receding ice edge. This behaviour allows capelin probably also finer scale patchiness due to behaviourally to exploit the secondary production of a considerable determ ined aggregations of spawning fish. For part of the Barents Sea and to maintain a large stock zooplankton where mating and spawning are temporally under favourable conditions (Sakshaug and Skjoldal, separated, patchiness induced by swarming is probably 1989; Skjoldal and Rey, 1989). Capelin matures at an reduced at the time of spawning. It is therefore a reason age of about 4 yr and migrates to the coasts of northern able assumption that patchiness of eggs and larvae is Norway and Kola to spawn (Tjelm eland, 1987). Spawn greater for fish than for zooplankton, both on a fine and ing areas along a wide stretch of coast of the southern large scale. Barents Sea and widely distributed feeding areas may Mortality rates of fish eggs and larvae are high, typi represent a situation where the range is short and the cally in the range 0.1—1.0 d 1, which are 5 to 10 times higher than predicted from their dry weight by the target wide. This may explain the relatively low fec undity of capelin, which, on the other hand, makes general model of Peterson and Wroblewski (1984) (M cGurk, 1986, 1987). There is a general decrease in this species more vulnerable to predation. Increased predation from the strong 1983 year classes of herring mortality with increasing development from egg through and cod probably played a m ajor role in the recruitment larval stages that corresponds to a decrease in the degree of patchiness (M cG urk, 1986, 1987). D ata on mortality failure and collapse of capelin stock from 1984 to 1986 (Mehl, 1987; Skjoldal and Rey, 1989). of pelagic crustaceans tend, on the other hand, to fall Cod is predominantly a piscivorous fish (Mehl, 1987) below the prediction of Peterson and Wroblewski’s (1984) model (M cGurk, 1987). Reported mortality rates which requires an abundant pelagic fish resource such of copepod nauplii tend to fall in the range 0.1-0.7 d “ 1 as capelin in order to sustain a large population. The (Heinle, 1966; Mullin and Brooks, 1970; Kimmerer feeding areas of cod will therefore be determined to a and McKinnon, 1987). M cGurk's (1987) regression for large extent by the patchy and variable distribution of pelagic crustaceans predicts a mortality rate of 0.12 d ‘ 1 capelin. The m ajor spawning area of cod is located in for a nauplius of 2 ^ig dry weight (e.g. Calanus). With Lofoten, and larvae are transported over a long distance a fecundity of 250-2000 eggs per female (Paffenhöfer, in a rather complex circulation system into the optimal 1970; Marshall and O rr, 1972) and a duration of egg feeding areas in the Barents Sea (Bjørke and Sundby, and naupliar stages of 30-60 d at 0-5°C for Calanus 1987; Dragesund and Gjøsæter, 1988). The probability (Marshall and O rr, 1972; Tande, 1988), a minimum of vagrancy is high due to variations in the current surviving num ber of two individuals corresponds to pattern which may transport larvae out over deep water mortality rates of 0.08-0.23 d ' 1. Increased mortality in the Norwegian Sea or into cold waters of the Svalbard rate for adult copepods has been ascribed to size selec region. This may be one reason for the high fecundity of cod. tive grazing by fish (Landry, 1978). Zooplankton species and populations need also to The available information suggests that eggs and lar vae of zooplankton tend in general to have lower m or maintain themselves within geographical areas where tality rates than those of fish. The size difference which the living conditions are favourable. However, the situa brings fish eggs and larvae into the size range preyed tion for zooplankton is different since they spawn over upon by visual plankton-feeding fish, could be a major a wide area. Their abundance and distribution will therefore be governed by their population dynamics and factor responsible for this difference. the circulation pattern. Individuals, either larvae or adults, which drift into areas unfavourable to repro Larval transport and distribution duction and growth, are expatriated vagrants that are The difference between fish and plankton in having and lost to the population. The expatriates are likely to not having restricted spawning areas, has important originate from outskirts of the area of distribution implications in terms of larval drift and distribution. where the living conditions are suboptimal. We consider The drift of fish larvae from spawning to nursery areas it unlikely that the fecundity of zooplankton would be is the reversal in the life cycle of the spawning migration increased to counteract the effect of such expatriation. by adult fish. Sinclair (1988) has stressed the importance of spatial losses of recruits from a population in his G eneral discussion “m em ber/vagrant” hypothesis. The spatial extent of the nursery areas may be an im portant aspect determining The foregoing analysis of reproduction and larval eco the likelihood that larvae transported by currents will logy has revealed several differences between fish and strike home and be “m em bers” or whether they miss zooplankton when these are considered as general groups (Table 1). Zooplankton larvae appear to be in a more their target areas and become “vagrants” . 334 Table 1. General characteristics of reproduction and larval ecology of fish and zooplankton. (It should be noted that there are many exceptions to these generalities.) Fish Zooplankton Horizontal to restricted spawning areas Vertical aggregation and swarming Mating and spawning In one act Temporally separated Patchiness in distribution of eggs and larvae High Lower i ( r 7- i o - 5 10 4-10 3 Egg size (diameter: mm) 1.0-2.0 0.1-0.5 Fecundity (eggs per female) 104-1 07 10:-103 Spawning behaviour Migration Egg size and fecundity Egg to adult volume ratio Larval feeding ecology Trophic type Carnivores Herbivores Size of food particles 30-200 fim 5-50 vim General food abundance Lower Higher Food of larvae and adults Different Same Egg production and feeding conditions of females Distantly related both temporally and spatially Closely coupled Food predictability Low Higher due to the synchronizing effect of the above coupling 2-30 d Roughly comparable to fish larvae Higher Lower Relatively large predators, including planktivorous fish Small predators (cyclopoid copepods, etc.) Susceptibility to predation loss High Lower Total mortality rate High Lower High. Loss of recruits by vagrancy is likely Less. Expatriation of both juveniles and adults from outskirts of distributional area Starvation and metabolism Larval starvation capacity Metabolic activity Predation Predator field Larval drift and transport Spatial constraints on life cycle closure favourable situation than are fish larvae in many respects. They have a more predictable and abundant food source, are relatively resistant to starvation, are less prone to be preyed upon, and are at less risk of not hitting home to nursery areas. This provides at least a partial explanation for the lower mortality of zooplank ton larvae com pared to fish larvae. A central question in the fish recruitment variability problem is which factors cause the high mortality in the early stages of fish. To allocate the responsibility by 335 each of the main factors, starvation, predation, or trans port loss, is difficult due to the fact that they are inter related and their relative im portance probably variable. The high fecundity of fish can be viewed as an adap tation to counter high mortality of the early stages of development. O n the other hand, an increase in fecundity for a fish of a given size represents less ener getic investment in each egg, and larvae that are more susceptible to starvation or food limitation (Ware, 1975). Thus high fecundity can also be viewed as causing high mortality. Prolongation of the larval period, either inherently or due to food limitation and poor growth, can result in higher mortality due to predation. In the context of spatial life cycle closure there could be inter relationships between the duration of the planktonic stages, total mortality and fecundity. Much attention has been given to mortality in the very earliest stages in the life history of fish since the critical period concept was introduced by H jort (1914). There is little evidence, however, in support of an exceptionally high and variable mortality at this period. There are in contrast many examples of rather constant or declining rate of mortality with development during the egg and larval stages (McGurk 1986, 1987; Fossum 1987). Large variability in year-class strength need not imply large variation in rate of mortality. If the mortality rate is high over a long period, a relatively small variation in mortality rate will produce a large variation in the number of survivors. Recruitm ent studies on cod in the Lofoten area have revealed a relatively constant mortality rate of about 0.15 d _1 for eggs and larvae during a period of 40 d after spawning (Fossum, 1987). This mortality rate would result in 120 surviving larvae out of 1 million eggs after 2 months. Varying the m or tality rate to 0.10 and 0.20 d _1 would leave 2500 and 6 survivors, respectively (Fig. 2). Thus, a difference in mortality rate by a factor of 2 results in more than two orders of magnitude difference in the number of surviving larvae 1 month after resorption of the yolk sac. A m oderate variation in growth rate due to feeding conditions or tem perature can have an equally drastic effect. Increasing and decreasing the growth rate by 50% and 33% , respectively, results in changes of devel opm ent time from 60 d to 40 and 90 d respectively. With a constant mortality rate of 0.15 d ^ 1 this produces m ore than three orders of magnitude difference in num ber of survivors (Fig. 2). The logarithmic nature of the exponential relationship is also evident if one considers zooplankton. With a generation time of 3 0 d, the fec undity must be 40 and 800 eggs per female to sustain mortality rates of 0.1 and 0.2 d ' 1 (Fig. 2). The high rate of mortality at the egg and larval stages of fish seems well docum ented. If the high mortality rate applies to a relatively long period during the egg and larval stages, as it appears to do, we are indeed 336 to N 0.2 Time ( days ) Figure 2. Effects of mortality rate on exponential survivorship curves in three hypothetical cases: 1) Survivors out of 1 million eggs after 60 d at mortality rates of 0.1, 0.15 and 0.2 d " 1. 2) Survivors after 40 and 90 d (representing a 2.2-fold change in growth rate) at a mortality rate of 0.15 d “ 1. 3) Required egg numbers to produce 2 survivors after 30 d at m ortality rates of 0.1 and 0.2 d ' 1. looking for relatively small differences in mortality rate to explain the large variability in recruitment. We sug gest that predation plays an overriding role for the high mortality rates (Fig. 3). The feeding conditions are considered to influence mortality mainly through the exposure time for predation. The same is probably the case for at least some of the spatial aspects which influence recruitment. Resolving the recruitment prob lem will require high accuracy and precision in carefully designed field sampling programs. The interrelations between the causes of mortality (Fig. 3) and their varia bility put emphasis on the need for a more broad system ecological approach in future recruitment variability PREDA TION T o ta l R e c ru its no. o f eggs ' g ro w th r FOOD L IM IT A TION d is t r i b ution SPA TIAL ASPECTS Figure 3. A schematic representation of interrelationships between predation, food limitation, and spatial aspects as causes of mortality in fish eggs and larvae. Food limitation is thought to act mainly through reduced growth rate and increased time of predation. 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