Reviews in Fish Biology and Fisheries 10: 61–89, 2000. © 2000 Kluwer Academic Publishers. Printed in the Netherlands.
61
Is density-dependent growth in young-of-the-year fishes a question of critical weight? J.H. Cowan, Jr.1 , K.A. Rose2 & D.R. DeVries3 1 Department
of Marine Sciences, University of South Alabama, Mobile, AL 36688, USA (Phone: (334) 4607136; Fax: (334) 460-7357; E-mail:
[email protected]); 2 Coastal Fisheries Institute and Department of Oceanography and Coastal Sciences, Louisiana State University, Baton Rouge, LA 70803-7503, USA; 3 Department of Fisheries and Allied Aquacultures, Auburn University, Auburn, AL 36849-5419, USA Received 5 January 2000; accepted 3 April 2000
Contents Abstract Introduction Conceptual arguments and exposition of premise Evidence from selected individual-based models Summary and chronology of the literature Empirical evidence from freshwater systems Empirical evidence from marine systems Discussion Acknowledgements Appendix References
page 61 61 62 68 74 74 76 77 80 81 82
Abstract We develop a conceptual argument that density-dependent growth via reductions in prey resources are most likely to occur in the late-larval or juvenile stage in both marine and freshwater fishes. We use results from a suite of individual-based models and literature examples of a variety of marine, estuarine and freshwater species to provide evidence of the effects of age-0 fish on their prey. We conclude that larval-stage survival related to foodlimited growth contributes significantly to recruitment variability. However, density-dependent regulation of cohort biomass via feedbacks derived from reductions in prey resources is most likely to occur at a “critical-weight” during the late-larval or juvenile stage. This occurs when fish densities remain relatively high, and population consumption is highest relative to prey density and replenishment rate. We compare our critical weight concept to Houde’s (1997) critical size hypothesis.
Introduction High fecundities of fishes ensure high early life stage abundances that are subject to both densityindependent controls responsible for variability in recruitment, and density-dependent regulation that stabilizes recruitment (Cushing, 1974; Rothschild, 1986; Houde, 1994). Information on growth ratemediated effects of food limitation on mortality and
recruitment variability is pervasive in the marine fish literature (see Heath, 1992; Leggett and DeBlois, 1994; and Table 1 for review). These effects have been the cornerstone of many “recruitment hypotheses” including Hjort’s (1914) critical period, Cushing’s (1975) match/mismatch, Lasker’s (1978) stable ocean, and Houde’s (1989) stage duration hypotheses (see Leggett and DeBlois, 1994 for review). Densitydependent growth due to competition for food can
62 result in density-dependent mortality. Slower growth leads to prolonged stage duration and mortality often decreases with size. Density-dependent mortality also is implicit in long-term population stability via decreased recruitment variability (Ricker and Foerster, 1948; Shepherd and Cushing, 1980; Houde, 1989). Density-dependent growth, however, is not simply food limitation of growth rate. Rather, it refers to a situation where the feeding rate of an individual is reduced by the presence of other members of the same population, cohort or year-class, i.e. intracohort competition for food increases with the density of individuals (Heath, 1992). It has been suggested that processes that determine survival of fish eggs and larvae are similar in both lakes and oceans and occur over similar spatial scales in both waterscapes (Rice et al., 1987; Magnuson, 1988). Similarity in processes affecting survival is remarkable given the fundamental differences in the degree of spatial “connectivity” of marine and freshwater ecosystems. If similar processes operate, and if food availability is important during the first year of life, the effects of food limitation and densitydependent trophic linkages may be similar for both marine and freshwater fishes. Toward this end, Houde (1994) predicted that juvenile-stage dynamics will be relatively important in determining recruitment levels and variability of freshwater fishes, while larval-stage dynamics will be more important in marine species. He compared the dynamics (instantaneous daily growth (G) and mortality rates (Z)) and energetics properties of marine and freshwater fish larvae. Marine larval fish cohorts typically begin as dense patches but lose biomass rapidly (G/Z < 1.0) during a relatively long larval stage. Typical cohorts of freshwater fish larvae are initially less dense, but accumulate biomass relatively rapidly (G/Z > 1.0) during a short larval stage duration. This suggests that the potential for small, density-dependent changes in food concentration to affect recruitment variability is high during the larval stage of marine fishes relative to freshwater fishes. However, smaller initial cohort sizes, short stage durations and lower mortalities of freshwater larvae result in relatively high numbers entering the juvenile stage, increasing the potential for density-dependent regulation in the juvenile stage in freshwaters. In partial contradiction to Houde’s (1994) prediction, we develop a conceptual argument that densitydependent regulation is more likely to occur in the late-larval or juvenile stage for both marine and fresh-
water fishes. We focus on the potential for larval and juvenile marine and freshwater fishes to effect recruitment levels through density-dependent feedbacks on their prey resources. We use predictions from a suite of selected individual-based models (IBM) and literature examples of a variety of marine and freshwater species to provide specific, “semi-quantitative” examples of age-0 fish effects on their prey. Finally, we conclude with a discussion and integration of the lines of evidence in support of our argument. Admittedly, this first-step analysis employs a semiquantitative or weight-of-evidence approach, and we recognize that this type of synthesis has both advantages and disadvantages. Advantages include the formulation of a general and testable hypothesis beyond a single species or location. Such analysis and generation of paradigm is often lacking in the important, but historically intractable, field of fisheries recruitment theory. One obvious disadvantage is the use of data from a variety of studies on different time and space scales not designed to be used for our purpose. Thus, we recognize that while our conceptual argument and inferred process-level interactions between fishes and their prey resources are sufficient to explain the patterns summarized herein, other density-dependent feedbacks resulting in similar final outcomes are possible (see Cowan et al., 1999). It is our hope that this review functions to stimulate subsequent research to challenge contentions presented here and replace them with well-supported tests of hypotheses.
Conceptual arguments and exposition of premise Pelagic ecosystems generally show a declining biomass distribution of organisms (in logarithmic size categories) with increasing weight (Sheldon and Parsons, 1967; Sheldon et al., 1972; Platt and Denman, 1977, 1978; Silvert and Platt, 1978). Small organisms are in general much more abundant than large organisms. One explanation consistent with this pattern infers that losses among size classes are attributable to predation, and that predation is highly size-selective with larger organisms eating smaller ones of a fixed proportional size (Sheldon et al., 1972; Heath, 1995; Houde, 1997). If the relationship between predator and prey size or biomass is known, it follows that growth and productivity of both prey and predator also are predictable from established, weight-dependent metabolic rules (Peters,
63 1983; Houde, 1997). Growth and mortality of pelagic organisms must be closely correlated. Taxa or life stages with rapid growth rates are predicted to have high mortality and, thus, high turnover rates (Houde, 1997). This argument has been used by several authors to explore the sized-based and correlative nature of growth and mortality of teleost life history stages (Ware, 1975; Peterson and Wroblewski, 1984; McGurk, 1986, 1987; Bailey and Houde, 1989; Houde, 1989; Pepin, 1991, 1993; Paradis et al., 1996; Houde, 1997). Results suggest that rates usually conform to those predicted by theory (i.e. number and density decline in relationship to weight), although fish eggs and larvae apparently die at rates somewhat faster than expected (Peterson and Wroblewski, 1984; McGurk, 1986, 1987). Consequently, Pepin (1993) cautioned that research on teleost early life stages based upon simple size-spectrum theory may not have practical applications, given limitations of sampling patchy eggs and larvae to estimate abundance. However, despite obvious limitations, we agree with Houde’s (1997) admonition that it is highly probable that body size and stage-specific productivity are factors related to teleost recruitment, although the exact form of these relationships remain largely unknown and may be species specific. Thus, following Bollens (1988), we have redirected these arguments to include age-0 fishes and their prey resources, focusing on the potential for density-dependent feedbacks. We note in advance that our conceptual model is based only upon first moments (i.e., means) of relationships. We recognize the importance of changes in variance with size, but suggest that the use of means is valid for making qualitative arguments. Speciesspecific predictions, however, would require incorporation of second and perhaps higher order moments of relationships. Our conceptual model begins with the apperception that the smallest size classes of age-0 fish consume particles from a relatively narrow size range that broadens as they grow, and that mean weight and variance in weight of prey individuals eaten by an age-0 fish predator increases with predator weight (Figure 1). We assume that the effect of age0 fish predators on their prey depends on the balance among prey density, prey replenishment (productivity and turnover) rate, and predator consumption rate (Figure 2; see also Bollens, 1988). Theory predicts (Peters, 1983) that prey density and replenishment rate will decrease with increasing prey weight (Figure 2b and d). Because prey weight eaten increases with
predator weight (Figures 1 and 2a), prey density and replenishment rate also will decrease with predator weight (Figure 2c and e). Consumption rate of an age-0 fish predator (grams individual−1; Figure 2f), multiplied by decreasing predator density with weight (Figure 2g), should lead to a dome-shaped relationship between population consumption rate (grams m−3 ) and age-0 fish weight (Figure 2h). Population consumption rate (grams m−3 ) can be expressed in terms of prey density (number of prey eaten m−3 ; Figure 2i) by dividing the grams consumed by the predator population by the average weight of prey individuals eaten by a predator. The relationship between population consumption and predator weight at low predator weights is uncertain because a small value of population consumption (grams m−3 ) is divided by a small value of prey weight eaten. Population consumption likely decreases at high predator weight because population consumption is decreasing, while being divided by prey weight eaten which is increasing. Using relationships derived in Figure 2, we can further derive a relationship between the ratio (K) of population consumption to the sum of prey density and replenishment rate [K = C/(D + R)] and predator weight (Figure 3). K is the fraction of tomorrow’s prey density that was consumed by the age-0 fish today. Based on our experience, we argue that the greatest effect would most likely be at some intermediate or maximum predator weight (e.g. Regions II and III in Figure 3). A large effect at low predator weight (Region I in Figure 3) is unlikely because prey densities and replenishment rates (D + R) are likely to be high at small predator weights. Prey density and replenishment decline rapidly with predator weight (e.g. as fish shift from feeding on small zooplankton to benthos and to fish). As population consumption increases and prey density and replenishment rate decrease with predator weight, K could either continue to increase with predator weight or show a maximum value at some intermediate level of predator weight. If the age-0 predators eventually become piscivorous, then their effect may be maximal at higher predator weight because of the very low prey densities and replenishment rates of fish prey. If the age-0 predators continue to feed on zooplankton or benthos, then their effect would likely be maximal at some intermediate level of predator weight where population consumption is maximum. Decreasing water temperatures in the fall, and the concomitant decrease in consumption rates, also favor the maximum value of
64 Table 1. Literature providing evidence of food limitation and/or, more specifically, the potential for marine fish larvae and juveniles to impact prey resources. Strong = direct evidence; statistically significant community reductions in prey biomass or numbers; consumption rates similar to prey replenishment rates. Some = weak or inferential evidence; statistically significant reductions in biomass or numbers of only one or a few prey types from among a diverse prey community. None = no evidence or negligible effects. Studies where predation effects were measurable (strong or some) also were assumed to provide evidence of potential for food limitation Species
Location of study
Field observations, larval stage Clupea harengus Georges Bank NW North Sea fronts Noregian coastal current Clupea harengus pallasi Strait of Georgia, British Columbia, Canada Bamfield Inlet, British Columbia, Canada Kulleet Bay, British Columbia, Canada Clupea pallasi Auk Bay, AK, USA Sardinops sagax California Current, USA Sprattus sprattus Western English Channel, UK Callionymus lyra Microchirus variegatus Phrynorhombus novegicus Sprattus sprattus Dogger Bank frontal region, North Sea Ammodytes lancea Pomatoschistus minutus Merlangus merlangus Myoxocephalus scorpius Arnoglossus latrena Anchoa mitchilli Biscayne Bay, FL, USA Engraulis mordax California Current, USA California Current, USA Anchoa mitchilli Biscayne Bay, FL, USA Callionymus pauciradiatus Gobiidae Opisthonema oglinum Orthopristas chrysoptera Gadus morhua Norwegian coastal waters Theragra chalcogramma Southeastern Bering Sea Western Gulf of Alaska Gadus morhua Georges Bank Melanogrammus aeglefinus Melanogrammus aeglefinus Georges Bank Pleuronectes platessa Other abundant species Melanogrammus aeglefinus Northern North Sea Trisopterus esmarkii Merlangius merlangus Gadus morhua Pollachius viren Cynoscion regalis Delaware Bay, DE, USA Ammodytes americanus Long Island Sound, NY, USA Scomber scombrus Long Island Sound, NY, USA Thunnus maccoyii East Indian Ocean East Indian Ocean Thunnus maccoyii East Indian Ocean T. alaunga Katsuwonus pelamis Rhombsolea tapirina Port Phillip Bay, Australia Ammotretis rostratus Rhombsolea tapirina Port Phillip Bay, Australia Ammotretis rostratus Pleuronectes platessa Dutch Wadden Sea Southern Bight, North Sea Parophrys vetulus Oregon shelf waters, USA Isopsetta isolepis Enclosure/exclosure experiments, larval stage Anchoa mitchilli Chesapeake Bay, USA Mallotus villosus Bryant Cove, Newfoundland Cynoscion regalis Delaware Bay, USA
Length Food Density dependent range limitation or potential based on reductions in prey
Prey type
Source
Calanoid copepods Copepod nauplii
Strong Strong Strong Some None None None None None
None Strong None None None None None None None
Microzooplankton Copepod nauplii Copepods Copepods
Cohen and Lough, 1983 Kiorboe et al., 1988 Fossum and Moksness, 1993 Robinson and Ware, 1988 McGurk, 1989 Purcell and Grover, 1990 McGurk et al., 1993 Murphy, 1961 Fortier and Harris, 1989
Strong
Strong
Copepods
Munk and Nielsen, 1994
Some Strong None None
None None None None
Copepod nauplii
Leak and Houde, 1987 Smith, 1985 Owen et al., 1989 Houde and Lovdal, 1985
Some None Strong Strong
None None None None
None
None
None
None
Some None None Some Strong Strong
None None None None Strong Strong
None
Calanus finmarchicus Copepod nauplii Copepod nauplii
Ellertsen et al., 1989 Dagg et al., 1984 Bailey et al., 1995 Buckley and Lough, 1987 Cushing, 1983
Zooplankton Mostly copepods
Economou, 1987
Zooplankton Cyclopoid copepods
Goshorn and Epifanio, 1991 Monteleone and Peterson, 1986 Peterson and Ausubel, 1984 Jenkins and Davis, 1990 Jenkins et al., 1991 Young and Davis, 1990
None
Microplankton
Jenkins, 1987
None
None
Microplankton
Jenkins, 1988
Some Some Some
None None None
Zooplankton Zooplankton Zooplankton
Hovenkamp, 1989 Hovenkamp, 1990 Gadomski and Boehlert, 1984
Some Some None
None None None
Copepod nauplii Cowan and Houde, 1990 40–50 µm Zooplankton Frank and Leggett, 1986 Copepods Duffy and Epifanio, 1994
Copepod nauplii Copepod nauplii
65 Table 1. Continued Species
Location of study
Length range
Food Density dependent limitation or potential based on reductions in prey
Prey type
Source
Strong
Strong
Zooplankton
Arrhenius and Hansson, 1993
None
None
Copepods
Thompson and Harrop, 1991
Some
Some
Pseudocalanus sp. Calanus pacificus
Bollens, 1988
Some None
None None
Zooplankton Zooplankton
Bollens et al., 1992 McKenzie et al., 1990
(30–50 mm) Some
Some
Harpacticoid copepods Harpacticoid copepods Harpacticoid copepods
Feller and Kaczynski, 1975
Modeling studies, larval stage Clupea harengus Baltic Sea Sprattus sprattus Gadus morhua Western Irish Sea Limanda limanda Sprattus sprattus Callionymus spp. Hypothetical plus Dabob Bay, WA, USA Merluccius productus Clupea harengus pallasi Ichthyoplankton Temperate fjord Mulitiple (review) Field observations, post-larval to juvenile stage Oncorhynchus keta Puget Sound, WA, USA Oncorhynchus keta Oncorhynchus keta Oncorhynchus gorbuscha Sardinops sagax caeruleus
Nanaimo River, British Columbia, Fry Canada Nanaimo River, British Columbia, Fry Canada Departure Bay & Hammond Bay, Fry British Columbia, Canada Gulf of California
Atherina breviceps Bot estuary, South Africa Gilchristella aestuaria Caffrogobius multifaciatus Clinus spatulatus Psammogobius knysnaensis Synganthus acus Haemulon aurolineatum Harrington Sound, Bermuda H. flavolineatum H. sciurus Orthopristas chrysoptera Gerres cinereus Diplodus bermudensis Multiple but mostly Bougue Sound, NC, USA Lagodon rhomboides Orthopristats chrysoptera Leiostomus xanthurus North Inlet, SC, USA
None
None
Strong
Strong
Strong
None
Some
Some
None
Sibert et al., 1977 Sibert, 1979 Godin, 1981 Hammann et al., 1988
None
Crustacean zooplankton Invertebrates
(20–80 mm) None
None
Meiobenthos
Alheit and Scheilbel, 1982
None
None
Invertebrates
Adams, 1976
Some
Some
Bennett and Branch, 1990
Clinus superciliosus Callionymus pauciradiatus
Cape Peninsula, South Africa Biscayne Bay, FL, USA
None None
None None
Pomatoschistus microps
Wadden Sea, FRG
None
None
Pomatoschistus microps P. minutus Pomatoschistus microps P. minutus Pleuronectes platessa Various crustaceans Pomatoschistus microps P. minutus Pleuronectes platessa Various crustaceans Valenciennea longipinnis
Schlei fjord, Baltic Sea
Some
Some
Swedish west coast
Some
Some
Harpacticoid Coull et al., 1989 copepods, meiofauna Meiofauna Gibbons, 1988 Harpacticoid Sogard, 1984 copepods, meiofauna Infauna Berge and Hesthagen, 1981 in Evans, 1983 Harpacticoid Schmidt-Moser and Westphal, copepods 1981 in Hicks, 1984 Infauna Moller et al., 1985
Swedish west coast
Some
Some
Infauna
Pihl, 1985
One Tree Reef, Great Barrier Reef Banyuls Bay, western Mediterranean Sea
None
None
Meiofauna
St. John et al., 1989
Some
Some
Harpacticoid copepods
Tito de Marais and Bodiou, 1984
Strong
None
Epifauna
Shaw and Jenkins, 1992
Buglossidium luteum Arnoglossus thori A. laterna Rhombosolea tapirina
Swan Bay & Port Phillip Bay, Australia
(
