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A framework for further study of recruitment processes in flatfishes
231
Netherlands Joumal of Sea Research 32 (2): 231-233 (1994)
A FRAMEWORK FOR FURTHER STUDY OF RECRUITMENT PROCESSES IN FLATFISHES DAVID O. CONOVER Marine Sciences Research Center, State University of New York, Stony Brook, New York 11794-5000, USA
ABSTRACT Can the 'recruitment problem' (Le., what controls the mean and variance of year class success?) ever be solved even for a single group of fishes? Fishery biologists from around the world focused intensely on the issue with regard to the flatfishes. Although a consensus was not attained, and few of the competing hypotheses were eliminated, several promising new ideas on how to proceed won support.
1. INTRODUCTION The 'holy grail' of fishery oceanography is to know what determines the mean and variance of recruitment to a given stock and to translate this understanding into a predictive model with accuracy on a time scale of one year. The history of this endeavour reveals success so far in identifying a variety of factors that do, or could potentially, affect recruitment. The most prominent factors are food, predation, advection, and the quantity and quality of the parental stock. The organizers of the second international flatfish symposium, however, realized correctly that if 'the recruitment problem' is to be solved, we must do more than simply 'round up the usual suspects'. They argued that it's time to synthesize our knowledge in the form of a series of testable alternative hypotheses and then to begin the task of rejecting as many such hypotheses as possible. Although few of the participants left the meeting convinced that even one of the major hypotheses could be eliminated, the gathering did generate much discussion on the nature of the problem and how to proceed. What follows is a summary motivated largely by comments of the participants. 2. A FRAMEWORK FOR FURTHER STUDY First, appreciate the sheer enormity of the problem being faced. The fishes have probably the most diverse array of reproductive strategies of any group of animals. Extant species clearly have solved the recruitment problem successfully in a rich variety of ways. This diversity informs us that there is no single solution to recruitment. Second, recognize that one year is an extremely fine time scale over which to pre-
dict or understand recruitment. The recruitment strategies of extant stocks or species evolved from successes and failures averaged over many individuals on time scales of generations. Each success and failure is recorded in the memory possessed by a population: Le., its genetic structure. The rarity of fishes that spawn only once in their lifetime ought to suggest to us that predicting recruitment at any single point in time is very difficult. Reproductive strategies of flatfishes at first glance appear fairly homogeneous. Virtually all flatfishes are marine, oviparous, have external fertilization, have separate sexes, and lack territoriality and nesting, brooding or other forms of parental care. Yet other features of the early life history, such as length of larval life, differ dramatically. A useful start in organizing our thinking about flatfish recruitment might be to attempt formal classification of their recruitment tactics. A variety of multivariate analyses might be employed to identify functional groups based on similarities in traits (see Winemiller & Rose, 1992). Variables might include egg size, egg buoyancy, spawning temperature, spawning season duration, length of embryonic, larval, and juvenile stages, drift distance (spawn site to nursery), growth rate, fecundity, age at maturity, maximum size, level of recruitment variability, and others. Statistically defined functional groupings could then be compared with a phylogeny to determine if similar suites of traits have evolved independently or are a function largely of common ancestry. Assuming that the diversity of recruitment patterns in flatfishes can be organized objectively into a small number of groups, one or two species within each might be chosen as a biological model of the group as a whole. Criteria for selecting such species ought to
232
D.O. CONOVER
include the existence of a reliable and lengthy recruitment time series, high variability in recruitment, strong environmental forcing factors, ability to describe completely the physics of the environment over appropriate temporal and spatial scales, existence of multiple stocks across some clearly defined environmental gradient (e.g., latitude), knowledge of main interactions with other species, feasibility of laboratory study, and existence of hatcheries to provide adults and progeny for experimental manipulations and introductions. Next, hypotheses concerning the likely abiotic and biotic determinants of year class variability for our model species need to be assembled into a conceptual model (e.g. Fargo, 1994). These presumed factors could then be combined in a simulation model that would allow relative effects on recruitment of various perturbations to be measured. An individualbased modelling scheme such as that presented by Chambers et aL (1994) for winter flounder is one way of accomplishing this. Major influences on recruitment predicted from the model can be tested in a number of ways. First, comparative analyses of local stocks distributed across a clearly defined habitat gradient might be very instructive. Latitude is one such gradient that received much attention in this meeting and the east coast of North America or Japan where thermal differences with latitude are especially steep would be good places to look. Comparisons among local stocks from areas that vary greatly in productivity or in abundance of predators might also prove fruitful. Henderson & Seaby (1994) showed how data accumulated by electric power plant operations might represent a rich source of information for conducting geographic comparisons. Second, controlled perturbations of a small subset of the stock might be employed. These could include transplants across habitats, direct habitat manipulation, manipulations of density in enclosures, or massive introduction of marked progeny supplied by hatcheries. Finally, much can be learned from careful observation of the effects of natural anomalous events. When interpreting geographic variation it may be very important to distinguish between environmental (phenotypically plastic) and genetic (local adaptation) sources of variation. The reasons go beyond simply needing to know the spatial organization of stocks in nature. The adult members of any stock are survivors of a successful recruitment process. Given that most species are highly fecund and that the greatest mortality occurs in the early life history stage, there is much potential for differential survival of phenotypes and hence natural selection on early life history traits. To the extent that they are heritable, we would expect early life history traits of any particular stock to be uniquely tuned to the features of the environment that consistently affect recruitment probability (if any). The nature of genetic variation in early life history traits
among local stocks can therefore teach us much about recruitment strategies under different environmental conditions. 'Common garden' experiments (Le., where the environment experienced by progeny is held constant thereby allowing stock-specific differences to be expressed) are needed to explore this problem. With both a model in one hand, and a scheme for data collection to test it in the other, the likelihood of moving ahead in our understanding of recruitment is greatly enhanced. Yet the task is far from easy and it will almost certainly be a gradual process that may never truly be complete. Probably the most important advice that can be offered is to be knowledgeable of and communicate with practicers of the numerous other disciplines that bear on marine science. Chief among these is physical oceanography. Incomplete knowledge of the physics of the systems we study is a major impediment. Yet new technology for remote sensing of the environment and for data processing is being engineered at a rapid pace and schemes for providing nearly continuous monitoring of a wide variety of variables are being organized. Ultimately, some day it may be possible to mount a variety of miniaturized sensors directly on the fish themselves. The pace of technological development over the last two decades suggests that this dream may soon not be unrealistic. Molecular genetics has much to offer. The DNA of the mitochondrial genome is highly variable and genetic markers or fingerprints specific to local flatfish stocks of interest may some day be available. Genetic marking of progeny arising from hatchery operations is already feasible. Imagine the improvement in our understanding of advective processes if progeny at different life stages could be identified by the spawning aggregation from which they came. It is my conviction that we still lack sufficient understanding of the bioenergetics of growth and degrowth in the early life history of fishes. For example, lack of knowledge concerning the problems (if any) faced by young-of-the-year flatfish in surviving winter was evident. Although there was much debate over whether young plaice experience food limitation during the summer when concentrated in the Wadden Sea, there was little attention focused on the potential consequences. Do flatfish rely on lipid reserves as an energy source in winter? If so, do they experience size-dependent starvation stress during the winter (as do some other fishes)? Does summer density affect winter survival? An additional physiological problem that bears upon the issue of density-dependence is the bioenergetics of cohort consumptive demand. Fish cohorts begin life with very high weight specific energy requirements but very low biomass density. As cohort biomass increases weight specific energy demand goes down, but the maximum consumptive demand of a cohort will generally be maximized in the juvenile
A FRAMEWORK FOR FURTHER STUDY OF RECRUITMENT IN FLATFISHES stage (see Yanez-Arancibia et aL, 1993). As Beverton (pers. comm.) discussed, the juvenile stage of many flatfishes is also often a period of habitat concentration. Bioenergetic modelling would be a useful way of pinpointing more precisely the habitat, temperature, and life stage where cohort energy demand is greatest. That is the life history period most likely to display density-dependent influences on growth and perhaps recruitment. Plaice would be a good choice for such an analysis, not only because sufficient data on growth, mortality, and weight specific food consumption appear to be available, but because habitat concentration in the juvenile stage is well documented. Behavioural ecologists need to play a bigger role in our understanding of recruitment, particularly in relation to predator prey interactions. Just one example is the recent debate over the 'bigger is better' concept: Le., the idea that larvae should grow as fast as possible in order to reduce the duration of the predationvulnerable larval stage. Leggett & DeBIois (1994) argued that this paradigm has been over-sold. They suggest that larger larvae are actually more susceptible to predation because of greater visibility and because their faster swimming speeds lead to a higher encounter rate with predators. They may be correct. But the missing piece of this puzzle is knowledge of the relation between size, age, and the behavioural capabilities of growing larvae and juveniles. For example, attainment of an age or size that permits schooling ought to alter dramatically the relative vulnerability to predation mortality. Average swimming speeds may not be as relevant to predatorprey dynamics as is the ability to modify speed in relation to perception of predation risk. Are flatfish larvae/juveniles capable of aggregating prior to, or after, settlement and does this affect predation vulnerability?
233
The above is only a sample of the questions that drew attention during this meeting. Doubtlessly these reflect my own interests and biases. Although we did not come close to solving the recruitment problem in flatfish, I think each of the participants came away with new ideas about how to think about recruitment. Few were convinced we should give up. In fact, the success of the meeting was in creating renewed vigour to forge ahead. Acknowledgements.--I thank the National Science Foundation and the organizers for supporting my participation in this meeting. 3. REFERENCES Chambers, R.C., K.A. Rose & J.A. Tyler, 1994. Effects of prey abundance, mortality and temperature on youngof-year populations of winter flounder, Pleuronectes americanu~, an individual-based numerical experiment.~eth. J. Sea Res. (submitted). Fargo, J., 1994. Examining recruitment relationships for Hecate Strait English sole (Pleuronectes vetulus).-Neth. J. See Res. 32: (in press). Henderson, P.A. & R.M.H. Seeby, 1994. Factors influencing juvenile flatfish abundance in the lower Severn Estuary, England.~eth. J. Sea Res. 32: (in press). Leggett, W.C. & E. DeBIois, 1994. Recruitment in marine fishes: is it regulated by starvation and predation in the egg and larval stages?---Neth. J. Sea Res. 32:119134. Winemiller, K.O. & K.A. Rose, 1992. Patterns of life-history diversification in North American fishes: implications for population regulation.~an. J. Fish. Aquat. Sci. 49: 2196-2218. Y&i~ez-Arancibia, A., A.L.L. Domfnguez & D. Pauly 1993. Coastal lagoons as fish habitats. In: B. Kjerfve. Coastal lagoon processes. Elsevier Oceanography Series 60. Elsevier Science Publishers: 339-351.
Netherlands Joumal of Sea Research 32 (2): 231-233 (1994)
A FRAMEWORK FOR FURTHER STUDY OF RECRUITMENT PROCESSES IN FLATFISHES DAVID O. CONOVER Marine Sciences Research Center, State University of New York, Stony Brook, New York 11794-5000, USA
ABSTRACT Can the 'recruitment problem' (Le., what controls the mean and variance of year class success?) ever be solved even for a single group of fishes? Fishery biologists from around the world focused intensely on the issue with regard to the flatfishes. Although a consensus was not attained, and few of the competing hypotheses were eliminated, several promising new ideas on how to proceed won support.
1. INTRODUCTION The 'holy grail' of fishery oceanography is to know what determines the mean and variance of recruitment to a given stock and to translate this understanding into a predictive model with accuracy on a time scale of one year. The history of this endeavour reveals success so far in identifying a variety of factors that do, or could potentially, affect recruitment. The most prominent factors are food, predation, advection, and the quantity and quality of the parental stock. The organizers of the second international flatfish symposium, however, realized correctly that if 'the recruitment problem' is to be solved, we must do more than simply 'round up the usual suspects'. They argued that it's time to synthesize our knowledge in the form of a series of testable alternative hypotheses and then to begin the task of rejecting as many such hypotheses as possible. Although few of the participants left the meeting convinced that even one of the major hypotheses could be eliminated, the gathering did generate much discussion on the nature of the problem and how to proceed. What follows is a summary motivated largely by comments of the participants. 2. A FRAMEWORK FOR FURTHER STUDY First, appreciate the sheer enormity of the problem being faced. The fishes have probably the most diverse array of reproductive strategies of any group of animals. Extant species clearly have solved the recruitment problem successfully in a rich variety of ways. This diversity informs us that there is no single solution to recruitment. Second, recognize that one year is an extremely fine time scale over which to pre-
dict or understand recruitment. The recruitment strategies of extant stocks or species evolved from successes and failures averaged over many individuals on time scales of generations. Each success and failure is recorded in the memory possessed by a population: Le., its genetic structure. The rarity of fishes that spawn only once in their lifetime ought to suggest to us that predicting recruitment at any single point in time is very difficult. Reproductive strategies of flatfishes at first glance appear fairly homogeneous. Virtually all flatfishes are marine, oviparous, have external fertilization, have separate sexes, and lack territoriality and nesting, brooding or other forms of parental care. Yet other features of the early life history, such as length of larval life, differ dramatically. A useful start in organizing our thinking about flatfish recruitment might be to attempt formal classification of their recruitment tactics. A variety of multivariate analyses might be employed to identify functional groups based on similarities in traits (see Winemiller & Rose, 1992). Variables might include egg size, egg buoyancy, spawning temperature, spawning season duration, length of embryonic, larval, and juvenile stages, drift distance (spawn site to nursery), growth rate, fecundity, age at maturity, maximum size, level of recruitment variability, and others. Statistically defined functional groupings could then be compared with a phylogeny to determine if similar suites of traits have evolved independently or are a function largely of common ancestry. Assuming that the diversity of recruitment patterns in flatfishes can be organized objectively into a small number of groups, one or two species within each might be chosen as a biological model of the group as a whole. Criteria for selecting such species ought to
232
D.O. CONOVER
include the existence of a reliable and lengthy recruitment time series, high variability in recruitment, strong environmental forcing factors, ability to describe completely the physics of the environment over appropriate temporal and spatial scales, existence of multiple stocks across some clearly defined environmental gradient (e.g., latitude), knowledge of main interactions with other species, feasibility of laboratory study, and existence of hatcheries to provide adults and progeny for experimental manipulations and introductions. Next, hypotheses concerning the likely abiotic and biotic determinants of year class variability for our model species need to be assembled into a conceptual model (e.g. Fargo, 1994). These presumed factors could then be combined in a simulation model that would allow relative effects on recruitment of various perturbations to be measured. An individualbased modelling scheme such as that presented by Chambers et aL (1994) for winter flounder is one way of accomplishing this. Major influences on recruitment predicted from the model can be tested in a number of ways. First, comparative analyses of local stocks distributed across a clearly defined habitat gradient might be very instructive. Latitude is one such gradient that received much attention in this meeting and the east coast of North America or Japan where thermal differences with latitude are especially steep would be good places to look. Comparisons among local stocks from areas that vary greatly in productivity or in abundance of predators might also prove fruitful. Henderson & Seaby (1994) showed how data accumulated by electric power plant operations might represent a rich source of information for conducting geographic comparisons. Second, controlled perturbations of a small subset of the stock might be employed. These could include transplants across habitats, direct habitat manipulation, manipulations of density in enclosures, or massive introduction of marked progeny supplied by hatcheries. Finally, much can be learned from careful observation of the effects of natural anomalous events. When interpreting geographic variation it may be very important to distinguish between environmental (phenotypically plastic) and genetic (local adaptation) sources of variation. The reasons go beyond simply needing to know the spatial organization of stocks in nature. The adult members of any stock are survivors of a successful recruitment process. Given that most species are highly fecund and that the greatest mortality occurs in the early life history stage, there is much potential for differential survival of phenotypes and hence natural selection on early life history traits. To the extent that they are heritable, we would expect early life history traits of any particular stock to be uniquely tuned to the features of the environment that consistently affect recruitment probability (if any). The nature of genetic variation in early life history traits
among local stocks can therefore teach us much about recruitment strategies under different environmental conditions. 'Common garden' experiments (Le., where the environment experienced by progeny is held constant thereby allowing stock-specific differences to be expressed) are needed to explore this problem. With both a model in one hand, and a scheme for data collection to test it in the other, the likelihood of moving ahead in our understanding of recruitment is greatly enhanced. Yet the task is far from easy and it will almost certainly be a gradual process that may never truly be complete. Probably the most important advice that can be offered is to be knowledgeable of and communicate with practicers of the numerous other disciplines that bear on marine science. Chief among these is physical oceanography. Incomplete knowledge of the physics of the systems we study is a major impediment. Yet new technology for remote sensing of the environment and for data processing is being engineered at a rapid pace and schemes for providing nearly continuous monitoring of a wide variety of variables are being organized. Ultimately, some day it may be possible to mount a variety of miniaturized sensors directly on the fish themselves. The pace of technological development over the last two decades suggests that this dream may soon not be unrealistic. Molecular genetics has much to offer. The DNA of the mitochondrial genome is highly variable and genetic markers or fingerprints specific to local flatfish stocks of interest may some day be available. Genetic marking of progeny arising from hatchery operations is already feasible. Imagine the improvement in our understanding of advective processes if progeny at different life stages could be identified by the spawning aggregation from which they came. It is my conviction that we still lack sufficient understanding of the bioenergetics of growth and degrowth in the early life history of fishes. For example, lack of knowledge concerning the problems (if any) faced by young-of-the-year flatfish in surviving winter was evident. Although there was much debate over whether young plaice experience food limitation during the summer when concentrated in the Wadden Sea, there was little attention focused on the potential consequences. Do flatfish rely on lipid reserves as an energy source in winter? If so, do they experience size-dependent starvation stress during the winter (as do some other fishes)? Does summer density affect winter survival? An additional physiological problem that bears upon the issue of density-dependence is the bioenergetics of cohort consumptive demand. Fish cohorts begin life with very high weight specific energy requirements but very low biomass density. As cohort biomass increases weight specific energy demand goes down, but the maximum consumptive demand of a cohort will generally be maximized in the juvenile
A FRAMEWORK FOR FURTHER STUDY OF RECRUITMENT IN FLATFISHES stage (see Yanez-Arancibia et aL, 1993). As Beverton (pers. comm.) discussed, the juvenile stage of many flatfishes is also often a period of habitat concentration. Bioenergetic modelling would be a useful way of pinpointing more precisely the habitat, temperature, and life stage where cohort energy demand is greatest. That is the life history period most likely to display density-dependent influences on growth and perhaps recruitment. Plaice would be a good choice for such an analysis, not only because sufficient data on growth, mortality, and weight specific food consumption appear to be available, but because habitat concentration in the juvenile stage is well documented. Behavioural ecologists need to play a bigger role in our understanding of recruitment, particularly in relation to predator prey interactions. Just one example is the recent debate over the 'bigger is better' concept: Le., the idea that larvae should grow as fast as possible in order to reduce the duration of the predationvulnerable larval stage. Leggett & DeBIois (1994) argued that this paradigm has been over-sold. They suggest that larger larvae are actually more susceptible to predation because of greater visibility and because their faster swimming speeds lead to a higher encounter rate with predators. They may be correct. But the missing piece of this puzzle is knowledge of the relation between size, age, and the behavioural capabilities of growing larvae and juveniles. For example, attainment of an age or size that permits schooling ought to alter dramatically the relative vulnerability to predation mortality. Average swimming speeds may not be as relevant to predatorprey dynamics as is the ability to modify speed in relation to perception of predation risk. Are flatfish larvae/juveniles capable of aggregating prior to, or after, settlement and does this affect predation vulnerability?
233
The above is only a sample of the questions that drew attention during this meeting. Doubtlessly these reflect my own interests and biases. Although we did not come close to solving the recruitment problem in flatfish, I think each of the participants came away with new ideas about how to think about recruitment. Few were convinced we should give up. In fact, the success of the meeting was in creating renewed vigour to forge ahead. Acknowledgements.--I thank the National Science Foundation and the organizers for supporting my participation in this meeting. 3. REFERENCES Chambers, R.C., K.A. Rose & J.A. Tyler, 1994. Effects of prey abundance, mortality and temperature on youngof-year populations of winter flounder, Pleuronectes americanu~, an individual-based numerical experiment.~eth. J. Sea Res. (submitted). Fargo, J., 1994. Examining recruitment relationships for Hecate Strait English sole (Pleuronectes vetulus).-Neth. J. See Res. 32: (in press). Henderson, P.A. & R.M.H. Seeby, 1994. Factors influencing juvenile flatfish abundance in the lower Severn Estuary, England.~eth. J. Sea Res. 32: (in press). Leggett, W.C. & E. DeBIois, 1994. Recruitment in marine fishes: is it regulated by starvation and predation in the egg and larval stages?---Neth. J. Sea Res. 32:119134. Winemiller, K.O. & K.A. Rose, 1992. Patterns of life-history diversification in North American fishes: implications for population regulation.~an. J. Fish. Aquat. Sci. 49: 2196-2218. Y&i~ez-Arancibia, A., A.L.L. Domfnguez & D. Pauly 1993. Coastal lagoons as fish habitats. In: B. Kjerfve. Coastal lagoon processes. Elsevier Oceanography Series 60. Elsevier Science Publishers: 339-351.