AN OVERVIEW OF
THE CRITICAL PERIOD CONCEPT OF
LARVAL FISH MORTALITY prepared by: William S. Snyder
The Ohio State University
01 March 1982
Understanding the population dynamics of larval fish cohorts is important in the accurate prediction of year-class strength and in growth and mortality models. One of the most important factors is the critical period: the extreme mortality that may occur between the time of yolk-sac absorption and the initiation of feeding. The critical period concept is based upon the aspects of larval starvation relative to prey density and abundance, larval growth and development as it relates to sensory and locomotory abilities, and feeding efficiencies, competition, predation, and susceptibility to physicochemical variability in the environment. It was concluded that the sum of all the interacting factors which influence the early life of fish can be generalized into two "environments": a hostile environment, in which available food resources are inadequate and catastrophic mortality occurs (classical critical period concept); or a benign environment in which available food resources are adequate enough to reduce or eliminate the "critical period".
In the past several decades increasing emphasis has been placed on understanding the population dynamics of larval fishes such that accurate models can be derived that will relate precisely year-class strength to ichthyoplankter growth and mortality (Hunter 1976). In the past, estimations of year-class strength have been based on gross projections from fecundity or on population estimates of juveniles or adults (Cushing 1975, Parrish 1973). To understand larval dynamics, attention must be focused upon the factors and mechanisms that influence the high mortality inherent in larval fish (Cushing 1974, May 1974, Hunter 1976). One fact that seems most important to larval survival is the presumed exponential rate of mortality that occurs between the time of yolk-sac absorption and the initiation of feeding, termed "critical period" (May 1974). This paper will investigate the factors that influence larval survival during this time, as well as assess the concept of "critical period."
The term "critical period" was first employed by the French fish culturists Fabre-domerque and Bietrix (1897; summarized in May 1974). They coined the term la periode critique to describe their observation of the high mortality in larval fish, which seemed coincident with the complete absorption of the yolk sac. This conception was strictly an observed correlation.
Hjort (1914; summarized in May 1974) developed a more generally understood definition of critical period through studies of cod (Gadus sp.) and herring (Clupea harengus) stocks by theorizing that year class strength was determined early in the life of the fish. He advanced his theory by stating that larval survival during this time would be influenced largely by a lack of food which would result in catastrophic mortality, or by larval transport on currents to unfavorable nursery areas (this latter aspect was cited as being the determining factor of year-class strength in Pacific herring, Clupea h. pallasi, by Stevenson 1962). In either case, the underlying assumption is that first-feeding larvae are extremely sensitive to food deprivation (Laurence 1974, May 1974).
"Critical period" has had broad usage throughout technical text, often in vague and indefinite context. Gulland (1965) used the conceptually similar term "critical period phase," which he defined as being "the phase during which the strength of the year-class is determined." Because of the vagueness, these definitions give no indication as to what stage of development the fish were in, or as to what sort of mortality had occurred.
In an effort to delineate a working definition of critical period, May (1974) defined it as the "critical period concept" or "the proposal that most larval mortality is concentrated during a relatively short period in early development". Thus, the term has been delineated to the massive mortality occurring at a fairly specific point during larval development.
The issue remains, however, as to the causality of, and the mechanisms through which, the critical period occurs. In other words, what makes the critical period critical?
WHAT MAKES THE CRITICAL PERIOD CRITICAL
Only in recent years have the mechanisms which relate critical period to year-class strength begun to be understood and much controversy still exists over causality. The general consensus which arises from the results of numerous larval mortality studies (Braum 1967, Cushing 1974, 1975, Houde 1978, Hunter 1972, 1976, Hunter and Thomas 1974, Laurence 1977, May, 1974, Stevenson 1962, Theilacker and Lasker 1974), is that the critical period concept is ultimately based in the interrelationships of various factors leading to increased vulnerability due to starvation and predation.
The aspect of larval starvation is often the most considered. At the time of first feeding, larvae are least efficient at capturing prey (Braum 1967, Houde 1978, Houde and Schekter 1980, Hunter 1972, Laurence 1977, May 1974). In laboratory experiments with the northern anchovy (Engraulis mordax), Hunter (1972) determined that the required food density for first feeding larvae was as much as 37 times greater than that for larvae several days older. A later study (Houde 1978) agreed, inasmuch as stating that the initial food concentration during the first 5 days of exogenous feeding is the most important factor affecting survival. Likewise, the low gross growth efficiencies and low feeding success rates achieved by first feeding winter flounder (Pseudopleuronectes americanus) larvae were cited (Laurence 1977) as being the cause of the fact that the highest critical prey densities (minima) were required at first feeding.
In a generalized, yet quantitative statement by Houde and Schekter (1980), the conclusion was drawn that only a small percentage of first feeding larvae of any species can capture enough prey to meet the minimal requirements for growth and survival. Though the evidence suggests that the mortality of first feeding larvae may influence year-class strength, a summary of 10 years of catch curve data on larval Engraulis indicated no significant increase in mortality during the "critical period" (Hunter 1972). Hunter counters this observation though, by pointing out that the mortality at all stages is so high that the increased vulnerability is not detectable, and that food may not be the limiting factor. This latter concept is supported in a study of larval fishes in the Black Sea (Dekhnik et al. 1970, as cited in May 1974), which revealed that mortality was highest in the yolk-sac stage, that few larvae had not fed successfully, and that only a fraction of the available food had been consumed. Preferential feeding was also determined via the observation that similar prey had been selected by different species of larvae under different conditions of plankton density and composition.
Thus, direct starvation is not the only mortality factor. When considering the critical period, the indirect effects of starvation may be of more importance than the direct effects (Braum 1967, Laurence 1977).
Larval starvation is complicated indirectly by decreasing swimming abilities and hence, feeding efficiencies (Braum 1967, Houde and Schekter 1980, Hunter 1972, Laurence 1977, May 1974). Laboratory demonstration has shown that starvation increases larval fish's susceptibility to various physicochemical influences such as toxins, salinity, pH, and low dissolved oxygen, and to biological influences such as infection and predation (Ivlev 1961).
The term starvation has too many contributing and resultant factors to be used singularly in identifying the basis of the critical period. More insight can be gained only by looking at the separate factors that influence the survival of larval fish.
FACTORS INFLUENCING LARVAL SURVIVAL
Prey Density and Abundance
Because starvation, traditionally, has been the basic theme in the critical period concept (Braum 1967, Hunter 1976, May 1974), the abundance of larval fish prey and the preferred prey species have been major topics of investigation. These data suggest that the quantity of prey consumed is positively correlated with the density and size of prey organisms, and hence, a prey density minima for larval survival exists (Houde and Schekter 1980, Hunter 1972, Hunter and Thomas 1974, Ivlev 1961, Lasker 1975, Lasker et al. 1970, Scura and Jerde 1977, Werner and Blaxter 1980). One such investigation (Houde 1978) found survival, standard length and weight per survivor, and food concentration all to be positively correlated. From the first-feeding requirements derived, in combination with field estimates, the investigator concluded that average prey density in the sea was substantial enough to ensure significant survival. Other investigators disagree (Houde and Schekter 1980, Hunter and Thomas 1974, Werner and Blaxter 1980).
These investigators claim the opposite to be true: average prey densities are not sufficient enough to allow successful exploitation by first-feeding larval fish. This claim, though, is allowable under the generally known concept that organisms are not randomly dispersed through the sea, but are aggregated. Thus, planktonic aggregations or patches provide nursery areas in which adequate prey concentrations are likely to occur.
Working under such a premise, Hunter (1972) determined that it is not the absolute number of prey organisms that are available to the larvae that correlate with survival, it is the density. This concept was agreed with by the determination that extensive larval feeding occurs in the chlorophyll maximum layers (highest phytoplankter density) off the California coast (Lasker 1975). Such prey patches also hold the possibility of significantly reducing or eliminating the effects of the critical period by allowing the feeding of larval fish that still have a yolk-sac (Hunter and Thomas 1974). A study on herring (Clupea harengus) (Werner and Blaxter 1980) achieved results which suggested that the herring was dependent upon the plankton patches. Peter (1974) closely correlated larval fish nursery areas in the Arabian Sea to upwellings and areas of current divergences (areas of naturally high productivity). A more recent study (Iles and Sinclair 1982) correlated herring spawning areas to hydrographic features such as gyres or estuaries which display retention mechanisms. These results are similar to other studies which correlate larval activities to characteristic spatial and temporal prey organism aggregations (Cushing 1975, Ware 1975, 1977).
Prey species composition is equally as important as density. Marine fish larvae feed primarily on zooplankton rather than phytoplankton (Houde and Schekter 1980). In a survey of 26 species of teleosts in the Mediterranean and the adjacent Atlantic (Duka and Gordina 1973), it was found that copepod nauplii comprised 90% of the prey consumed by small larvae. Another study (Kjelson et al. 1975) on the feeding habits of three Atlantic species determined that copepods and copepodites made up 99-100% (both by number and weight) of the organisms consumed. Many other studies suggest that the naupliar and copepoditic life stages of copepods form a significant portion of many larval fishes' diet (see Appendix for a literature review summary of larval prey preference). Phytoplankton, however, may form an important initial or alternate food source.
Lasker et al. (1970) found that for the first week of exogenous feeding northern anchovy larvae could subsist on the dinoflagellate Gymnodinium splendens with survival and growth rates comparable to anchovy larvae fed nauplii. In a subsequent study, Lasker (1975) determined that the anchovy larvae were transient feeders on the dinoflagellate, shifting from the phytoplankter to nauplii as their size increased. This alternate foraging strategy was agreed upon in another study on northern anchovy (Hunter and Thomas 1974). This investigation concluded that the denser phytoplankton represented a transitional food source for larvae until larval feeding efficiencies were such that the less dense zooplankton could be exploited (see Appendix).
Selectivity for phytoplankter species was demonstrated by Scura and Jerde (1977), who found that unarmored dinoflagellates such as Gymnodinium were selected for over armored dinoflagellates such as Gonyaulax polypedia. Though both dinoflagellates were of a ingestible size, the Gonyaulax proved inadequate as a food source unless supplemented by microzooplankton (these results closely agree with a similar study by Lasker et al 1970).
Food resources other than phytoplankton and copepods are also consumed. Houde and Schekter (1980) found larvae which had preyed significantly on cilliates and occasionally on protozoans, but these alternative or "suboptimal" resources were only utilized at low nauplii concentrations (re Appendix).
Larval Growth and Development
Closely integrated with the aspects of abundance and distribution of food resources are the more direct aspects of larval growth and development. Newly-hatched larvae have the temporary food resource of the yolk-sac; when it is exhausted they lack the tissue and lipid reserves of adult fish, hence the larvae must either successfully feed or die (Cushing 1974, 1975, Jones 1973 as cited by Ware 1975). The mortality process in larval fishes was described by Ware (1975) as being "a size and density-dependent function of available food supply and predation," however, in the context of feeding success versus mortality, larval feeding success has been positively correlated to larval size, hence, growth (Braum 1967, Houde 1978, Ivlev 1961, May 1974, Rosenthal and Hempel 1969).
The mechanism underlying the feeding-success/larval-growth correlation is that the larval fish's predatory efficiency is initially low, but increases rapidly with growth (age, size) (Blaxter and Staines 1971 as cited by May 1974, Houde and Schekter 1980, Hunter 1972, Laurence 1977). The primary key to the larvae's predatory efficiency is its locomotory abilities. Braum (1967) state that locomotion is the most significant factor influencing survival. In a similar vein, one study reported that the feeding success among clupeid larvae is limited by their lack of maneuverability (Rosenthal and Hempel 1969). Larval locomotion and maneuverability, though is keyed to feeding success through the larvae's development in general.
Beyer (1980) defines feeding success as "the probability of capturing the prey organism assuming attack; derived from basic principles as a function of the predator's mouth size, the prey width, and the precision of the strike." The aspect of the feeding strike, along with the predator mouth size, relates directly to the development of the larvae--its maneuverability and its perception of the prey. As the larvae grow, they become more efficient predators. Hunter (1972) observed the increased swimming abilities in herring larvae with age, and when considering this in terms of the increased volume searched per unit time, it correlates with the decreased density of prey organisms that is required by older larvae (Braum 1967, Houde 1978, Houde and Schekter 1980, Hunter 1972, Hunter and Thomas 1974, Laurence 1977, May 1974, Rosenthal and Hempel, 1969, Werner and Blaxter 1980).
Sensory development is a significant aspect of feeding success. At hatching,
most larval fish have developed olfactory organs and naked neuromasts, but lack sufficient pigmentation in the eyes to make them operable (Hunter and Thomas 1974). This fact adds significance to the concept of the alternate foraging strategy of feeding on phytoplankters, which could be contacted and consumed using the chemical stimuli of olfaction. The aspect of olfactory-based predation is supported by the observation that larval anchovy can feed on Gymnodinium in the dark (Hunter and Thomas 1974).
After the eyes develop, vision is the primary sense employed in the larval fish's foraging strategy. This is supported by the positive phototaxic nature of the larvae's attack (Braum 1967, Hunter 1972) and simply by the fact that most larvae feed during the day in illuminated waters (Hunter and Thomas 1974, Kjelson et al. 1975, Laurence 1977, Seliverstov 1974). Marak (1974), however, observed larval redfish (Sebastes marinus) with full stomachs day and night, and hence, concluded that this species fed continuously.
Braum (1967) through laboratory observation has determined that larval whitefish (Corregonus wartmanii) use both light and gravity for orientation. When preparing to strike, the larval whitefish position themselves at a 50-degree angle from the water surface. By doing this, Braum theorized, the whitefish could highlight its prey against the light surface.
Observations on the winter flounder (Laurence 1977) suggested that starvation via low prey densities was not due to food availability, but instead was due to having a day "too short" to consume the daily food requirement or growth. This observation, though, is based on a correlation between estimations of the required feeding-day length for survival and the photoperiod of the study situation: a strong correlation, but doubtful cause and effect.
A study of diurnal vertical migrations in larval herring (Seliverstov 1974) suggested that positive phototaxis developed through evolution in illuminated waters. The point made here is that the basis of this adaptation is the requisite trophic relationship of the predators being where the prey are located. Phytoplankters, naturally, exist in the euphotic zone, thus zooplankters, and hence, larval fish are also found there. In a photic setting, vision is the most efficient sense that can be utilized for predation, thus the larval fish's adaptation to a vision-based predation strategy.
This concept leads one to consider what sort of limits or changes might occur in feeding efficiency or foraging strategy in turbid water or under otherwise optically-limited conditions.
Another aspect of larval development is the development of the digestive system. In most first-feeding larvae, digestion is grossly inefficient (Braum 1967, Hunter 1972, Laurence 1977). In a laboratory feeding study with herring (Werner and Blaxter 1980), it was observed that in experiments with Artemia as the prey, the Artemia would occasionally be defecated alive. The results reveal that the rate of assimilation is not directly related to the rate of ingestion. Increased rates of ingestion leads to increased rates of egestion (shorter evacuation time), thus digestion and potential assimilation are reduced.
Laurence (1977) in the development of a bioenergetic model for winter flounder, remarks on the observation of a sharp, initial reduction in the time required to capture and consume a daily ration of prey that occurs shortly after first feeding. He attributes this reduction to the larvae's increased predatory abilities (learned responses), and to the increased digestive efficiency as the digestive system develops (re Hunter 1972). Feeding time, however, increased quickly as the larvae's increased metabolic requirements (via growth) increased the daily ration requirement.
As mentioned in the preceding paragraph, the learned response forms yet another aspect of larval development. Braum (1967) reports of a pursuit response in whitefish larvae which develops and becomes very acute after several failed attacks on nauplii. He theorized that this "tracing instinct" is the direct result of the prey's evasion.
Another study (Hunter and Thomas 1974) reports of non-random search patterns and the ability to stay with prey aggregations, both of which increase after several days. This suggests that they are learned responses.
Observations on the feeding of anchovy concluded that feeding largely depends on the maturation of sensory and locomotor systems, but went on to suggest that feeding sequences were learned behavior and transferable experiences (Hunter 1972).
Very little work has been done on investigating possible correlation between critical period and the effects of competition. From what can be drawn from existing studies, little or no correlation exists. The spatial and/or temporal resource partitioning that would have occurred as a result of competition among adult, juvenile or older larvae stocks would probably reduce the chance of interspecific competition between first-feeding larvae. Hunter (1976) however, points out that interspecific interactions may occur between larvae competing for common planktonic resource, whereas the adults utilize different resources, and thus, do not compete.
Spatial and temporal resource partitioning is common among similar species. An example would be the herring spawning cycles studied by Cushing (1975). In this instance both geographical location and seasonal variation occur in which the spawning of different biological stocks of Clupea were related to specific planktonic production cycles. Stocks were identified as autumn, winter, or spring spawners, and were related to North Sea, Coastal Atlantic, or Oceanic production cycles, respectively. Each stock's reproductive strategy, in terms of fecundity, the size of eggs produced, and their spawning schedule, is closely related to their characteristic spawning areas in terms of the time of peak planktonic production and the mean size of the organisms constituting the plankton.
Cushing's (1975) results are very similar to the results of a study on the spawning of Atlantic mackerel (Scomber scombrus) (Ware 1977). In this work, Scomber were found to have two basic spawning periods, spring and summer. The spring spawn was dominated primarily by older fish which produced larger eggs, and the summer spawn was mostly younger fish producing smaller eggs (re Ware 1975: inverse relationship between egg diameter and water temperature; and that larger eggs produce larger larvae). The resultant spring population of large Scomber larvae were suited to prey on the overwintered adult copepods then present, while the smaller summer spawned larvae were best suited to feed on the nauplii and copepodites produced that season.
An example of temporal partitioning can be seen in a small eutrophic lake in Ontario (Keast 1980). In this instance, a succession of spawning takes place each spring by yellow perch (Perca flavescens), troutperch (Percopsis omiscomaycus), black crappie (Pomoxis nigromaculatus), rock bass (Ambloplites rupestris), and sunfish (Lepomis sp.). The larvae of each species utilize precisely the same naupliar and copepoditic cyclopoids. The larval stages, however, are very size selective in their feeding. The result is a progressive temporal partitioning of the zooplanktonic resource through the spawning season, which reduces interspecific competition, while maximizing the temporal carrying capacity of the nursery area.
Intraspecific competition could possibly influence the effects of the critical period. Two main mechanisms exist that might influence starvation (Hunter 1976). One mechanism would occur in pelagic stocks, wherein an increase in the spawning stock results in the occurrence of larvae in areas of low prey organism production. The other mechanism would occur in demersal stocks, wherein an increase in the spawning stock results in an increased density of larvae in the optimal nursery area. Both mechanisms would, in effect, result in increased intraspecific competition.
No literature was reviewed which reported on either of these phenomena.
Predation does not affect the critical period as much as it affects the entire larval population (Hunter 1972). Many researchers feel that it is the leading cause of mortality of larval fish (Houde 1978, May 1974, Theilacker and Lasker 1974, Ware 1975). Hunter (1976) cites 5 mechanisms through which predation could influence a larval fish population. They are:
1) cannibalism by adults;
2) reproductive response of predator population to the production of eggs and larvae;
3) attraction of predators as a function of the size or density of patches of eggs or larvae;
4) selection of prey by the predator as a result of experience;
5) survival of the predator as a function of the abundance of eggs or larvae.
As mentioned previously, these would tend to influence the larval population as a whole, with little or no affect on the critical period.
Predation, though usually thought of as being nektonic in origin, can be planktonic. Davis (1959) reports of having observed larval rock bass being attacked by Mesocyclops edax (copepod). Numerous copepods swarmed the larvae, biting at fins and persistently attacking, until the larvae succumbed from fatigue.
Similarly, brine shrimp (Euphasia pacifica) have been observed to be a
significant predator of larval Engraulis in the California Current (Theilacker and Lasker 1974). Arrow worms (Chaetognatha) and medusae (Coelenterata) also have been observed as predators of ichthyoplankton (Fraser 1969). One study (Lillelund and Lasker 1971) observed that although the copepod Labidocera trispinosa would prey on Engraulis larvae, predation was reduced by the presence of Artemia (a preferred prey). Overall, there is no certainty of the role of ichthyoplankton in the feeding strategy of planktonic predators.
Another aspect of predation that has received little attention is cannibalism by other larvae. Literature is extremely limited on this matter, and it is difficult to make any statements as to the correlation of cannibalism to critical period. My primary research with larval freshwater drum (Aplodinotus grunniens), however, has produced several examples. Drum larvae were observed at yolk-sac absorption stage ranging from 3.5 - 4.0 mm (TL). First-feedings were observed, commonly, from 4.5 - 5.0 mm (TL) which had 3/4 swallowed a 4.0 mm (TL) larva. No conclusions have been drawn from these data concerning larval cannibalism.
Cannibalism often exists as a portion of alternate foraging strategies. An investigation of predator-prey interactions in Oneida Lake, New York (Forney 1974), revealed that with older walleye (Stizostedion vitreum) (juveniles and adults), feeding switched to white perch (Morone americana) and smaller walleye when the typical prey (yellow perch) densities were down. This concept can possibly be extended to larval populations to suggest cannibalism as an alternate-foraging mechanism.
Cannibalism of larvae or juveniles by adults, however, may regulate year-class strength. Alm (1952 as cited by Chevalier 1973) observed the feeding of adult Eurasian perch (Perca fluviatilis) on their young, and reported that year-class strength significantly increased following the removal of adult perch.
Overall, the abiotic variables (i.e. turbulence, shear, storm surge) tend to affect the larval fish population as a whole. The major influencing factor, temperature, however, may have significant effects on critical period. Temperature effects not only the number of eggs spawned and the length of incubation period (Hunter 1976, Ware 1975), but also the size or amount of yolk stored at hatching (Braum 1967). It has been observed that at lower temperatures, fish tend to produce large eggs, which in turn, have larger yolks and produce larger larvae (Ware 1975). By having a larger yolk, a larva has an increased survival time until exogenous feeding is necessary. In addition, the larger larva is more able to feed upon the given prey (Laurence 1977, Ware 1975, 1977). It has also been observed that yolk absorption occurs faster at higher temperatures (Lasker et al. 1975). Thus, unseasonably high temperatures may produce larvae less fit to prey successfully on the given food resource, and hence, survive the critical period.
Turbulence tends to have deleterious effects upon the system. It can take the form of wave-induced turbulence, wind-induced shear, tidal currents and eddies, or upwellings (Hunter 1976, Ivlev 1961, Peter 1974). The effects of critical period could be increased by the current transport of larvae or eggs into less productive waters (Cushing 1974, May 1974), or it could disrupt the prey patches or aggregations which may form vital first-feeding concentrations for larvae (Lasker 1975) (see Prey Density and Abundance).
SUMMARY: CONSIDERATION OF THE CRITICAL PERIOD CONCEPT
When considering the critical period concept, attention must be given to all of the factors that influence the survival of first-feeding larvae. This discussion of the various factors is neither exhaustive nor complete--it merely highlights a few of the more prominent considerations. The quantity of literature that can contribute relevant information to the study of the critical period is vast.
The classical definition of critical period is based on the assumption that exponential mortality occurs between the time of total yolk-sac absorption and the initiation of first-feeding (May 1974). If catastrophic mortality is a requirement, then Hunter's (1972) 10 years of catch curve data negates the critical period concept. The point to be made is that the critical period exists as a concept--an abstract definition of a time of great potential vulnerability in the early life history of fish. Thus, instead of viewing catastrophic mortality as being a requirement for the existence of the critical period, it should be taken as the ultimate consequence. Hence, the critical period would be viewed as a time of potential vulnerability and the degree of criticality depends upon the factors influencing the nature of period between yolk absorption and first feeding.
Assuming that larval fish are highly sensitive to food deprivation (Laurence 1977, May 1974), it follows that if prey densities and species are such that exogenous feeding can begin about the time of yolk-sac absorption, then no exceptional mortality will occur via starvation (May 1974). Such would be the case when larval fish could utilize phytoplanktonic resources (Hunter and Thomas 1974, Lasker et al 1970, Lasker 1975) in dense aggregations (Houde and Schekter 1980, Hunter 1972, Scura and Jerde 1974), thereby not requiring highly developed locomotor and sensory abilities (Braum 1967, Houde and Schekter 1980, Hunter 1972, Hunter and Thomas 1974, Laurence 1977, Rosenthal and Hempel 1969).
However, when first feeding is inhibited, the indirect effects of starvation interact to complex the situation. The interaction is so intricate that there is no proven cause and effect, just correlations. Basically, larvae must feed soon after yolk-sac absorption or they will die (Cushing 1974, 1975, Jones 1973, as cited by Ware 1975). Feeding success, though, is limited largely by lack of maneuverability (Rosenthal and Hempel 1969, Beyer 1980), hence the close positive correlation between feeding success (predatory efficiency) and larval growth and development (Braum 1967, Houde 1978, Houde and Schekter (1980), the successful feeding larva is enhanced by developing faster, thereby increasing its predatory efficiency, and thus escaping from the period of greatest vulnerability (critical period) faster. On the other hand, the unsuccessful larva experiences decreased development, hence, decreased feeding efficiency, thus increasing its vulnerability to predation, infection, and deleterious physicochemical influences (Ivlev 1961).
To conclude, the underlying hypothesis of the critical period concept is that it is the time period in which year-class strength (stock size) is regulated (Braum 1967, Cushing 1974, Houde and Schekter 1980, Hunter 1976, May 1974, Scura and Jerde 1977). Assuming the feeding/starvation concept of critical period, the sum of all the interacting factors which influence the early life of fish can be generalized into two "environments": a hostile environment, in which available food resources are inadequate and catastrophic mortality occurs (classical critical period concept); or a benign environment in which available food resources are adequate enough to reduce or eliminate the "critical period". Thus, in the case of the hostile environment, year-class strength determination could probably be delineated to the catastrophic reduction in numbers proceeding first feeding. While in the case of the benign environment, year-class strength determination probably could not be delineated to any specific point in the fish's life history, but rather occurs as a continual adjustment of numbers over time (re Cushing 1974)
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Appendix: Preferred and alternate prey for various species of ichthyoplankton.
Species Prey: Species, Preference, Utilization* Source
Clupea harengus Pseudocalanus sp. (86% of diet) [P] Hardy 1924 (in Wyatt 1974)
Engraulis mordax Gymnodinium splendens [F] Lasker et al. 1970
(dinoflagellate) Lasker 1975
26 sp. of teleosts in copepod nauplii (90% of diet) [P] Duka and Gordina 1973
Mediterranean and adjacent
Clupea harengus eggs, nauplii, and early copepoditic Bainbridge et al. 1974
Scomber scombrus stages of copepods [P]
Engraulis ringens de Mendiola 1974
larvae <11.0 mm Calanus sp. - eggs and larvae [P]
ciliates and protozoans [S]
larvae >11.0 mm Calanus sp. (exclusively) [P]
Engaulis mordax Gymnodinium spendens [F,S] Hunter and Thomas 1974
copepod nauplii [P]
Clupea harengus Calanus sp. (all stages) [F,P] Jones and Hall 1974
Sebastes marinus Copepods (all stages): [P] Marak 1974
Euphasiids, fish eggs, invert. eggs [S]
Clupeonella d. delicatala copepodites [P] Pinus 1974
Mauralicus muelleri nauplii and copepodites: [P] Williams and Hart 1974
Pleuronectes platess Oikopleura sp. (almost exclusively) [P] Wyatt 1974
Brevoortia tyrannus 4 taxa of copepod [P] Kjelson et al. 1975
Lagodon rhomboides - 76-99% of gut contents
Leiostomus xanthurus - 99-100% of identifiable gut contents
Engraulis mordax nauplii and copepodites [F,P] Arthur 1977
Pseudopleuronectes americanus naupliar, copepoditic, and adult copepods [P] Laurence 1977
Engraulis mordax Gymnodinium splendens [F,S] Scura and Jerde 1977
nauplii and copepodites [P]
Scomber scombrus calanoid copepods and barnacle cypris [N] Ware 1977
Achirus lineatus nauplii and copepodites [P] Houde 1978
Anchoa mitchilli cilliates and protozoans [S] Houde and Schekter 1980
Ambloplites rupestris nauplii and small cyclopoids [F,P] Keast 1980
* Bracketed letters indicated observed prey utilization: F = first-feeding staple
N = no statement on observed prey utilization
P = primary staple
S = supplemental or alternate staple
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