Condition and growth of reef fish at settlement: Is it important?

Transcription

1 Australian Journal of Ecology (1998) 13, Condition and growth of reef fish at settlement: Is it important? MARK I. McCORMICK Department of Marine Biology, James Cook University, 1bwnsville, Qld 4811, Australia Abstract The incorporation of information on the phenotypic attributes and performance offish into models of population dynamics may greatly enhance our ability to predict population chan,ge. To date, reef-fish research has concentrated on numerical aspects of the recruitment process, with little attention to the quality of recruits. Information reviewed here suggests that the attributes of individual fish, be they related to fish size, performance or condition at the end of the larval phase, may markedly influence the dynamics of the demersal life stages. This review briefly explores the levels of variability in some aspects of fish condition at settlement, the mechanisms by which this ',ariability is enhanced or affected by density-dependent processes, and the ramifications of this phenotypic variability for the persistence of cohorts. Key words: growth compensation, individual quality, mt:tamorphosis, recruitment, reef fish, selective predation, settlement. INTRODUCTION Reef-fish settlement and recruitment has been extensively studied during the past two decades. Emphasis has been placed on quantifying the numerical variation in new individuals entering a local reef population, and its correlation with environmental events or features (e.g. Milicich 1994; Milicich & Doherty 1994). Recently, a number of reef-fish researchers, enthused by decades of temperate fisheries research (e.g. Ferron & Leggett 1994), have focused on the qualitative aspects of individual fishes at settlement. This research has been motivated by the desire to identify attributes of individual fish that survive to a particular life stage (in this case settlement) and to determine whether these attributes are predictive of a fish's subsequent fimess. Until recently researchers have typically ignored the strong link between events in the plankton and those on the reef (Boero et at. 1996). This is due in part to the pelagic-to-demersal nature of the generalized reeffish life cycle, for which sampling logistics, and processes that influence the life stages, are largely dissimilar. The sparse literature available suggests that these two life stages cannot be viewed as separate entities; events and conditions during the pelagic stage may bias events in the demersal life stages following settlement. Measures of individual quality (whether measured Accepted for publication October as growth, performance capabilities, or biochemical, developmental or behavioural components of fitness) demonstrate that individuals within a population differ, particularly in their response to environmental variation. It is upon this variation in an individual's traits that selective proces~:es act, and this may determine which individuals reproduce and the quality of their offspring. Chambers and Leggett (1987) noted that quantifying the phenotyp4:s of fish at metamorphosis and settlement has doubl,~ utility for our understanding of fish population dynan.1ics. First, we can look backwards in ontogeny, as the phenotype of an individual at metamorphosis represents the integration of an individual's larval growth and development. Second, we can look forward into the juvf:nile period, as the phenotype of a fish at this transition may be predictive of success in its new habitat. Despite an extensive temperate-water fisheries literature showing the importance of condition to the outcome of predator--prey interactions (e.g. Fuiman & Higgs 1997), the importance of variable larval condition at metamorp hosis and settlement has been largely ignored in studies of reef-fish population dynamics. Evidence :;uggests that predation within the first 7 days after settll:ment may remove 30-78% of the newly settled fishes to a coral reef (Doherty & Sale 1985; Victor 1986a; Booth 1991; Carr & Hixon 1995) and between 73 ami 85% of newly settled flatfishes from temperate se diment flats (Van der Veer & Bergman 1987; Tanaka et ai. 1989). Such high mortality is a strong ar~;ument for the importance of an

2 ( 260 M. I. McCORMICK (e.g. size-selective mortality) may have little influence on the levels of variability in other traits (e.g. lipid content, important for growth). Size-related traits will be accentuated by growth rates that vary greatly among individuals within cohorts and samples (McCormick & Molony 1993). A wide variety of morphological, histological and biochemical methods of quantifying condition (reviewed by Ferron & Leggett 1994) have been used by temperate fisheries workers to predict survival probabilities of larvae under particular food regimes. To date, only relatively gross measures of condiltion have been used to assess the quality of reef fish. l.aboratory and field experiments are required to determine how limited food influences growth and devel\;>pment in targeted reef-fish species. A comparison of measures of condition (e.g. Theilacker 1978) will reveal measures that are sensitive to feeding levels and may allow researchers to assess the feeding history of individual newly settled fish, or pro-rate the success of these fish. MAINTENANCE OF CONDIllON AND GROWTH An evaluation of the importance of the quality of an individual at settlement requires detailed information on the fate of individuals of known condition. Due to our present inability to assess any but the simplest measures of condition non-destructively, info"rmation on the ensuing effects of variable condition air settlement is only available in relation to fish size. Con2 (8%) :] CARBOHYDRATE :Y~~~~~t:;:=i==;- 2 ~. 2 ~,~~ PROTEIN NoV.G).1-4-' WATER G)JM. 3 \ :...J I.I.I ' I Can (84 %) Fig. 1. Comparison of length (SL), weight (WT) and biochemical composition (protein, lipid, carbc)hydrate, water) of the damselfish Pomacentrus amboinensis from five settlement pulses collected monthly over 3 years of settlement (1-3). Means (95% confidence circles) are plotted on canonical variate axes with respect to vectors that represent trends in the analysed variables. The strength of the trends in each variable measured on individual settlers is displayed by vector length. Note that settlers in the second year had significantly more protein and carbohydrate than fish from the other 2 years (modified from Kerrigan 1996). SL Variability in growth of individuals of a cohort is well known to be density-dependent when densities are forced well above natural mean levels, such as in aquacultural situations (De Silva & Anderson 1995). The limited research on growtll of juveniles in reef systems suggests that social interactions and density dependence are also important in field situations (e.g. Jones 1987a; Tupper & Boutilier 1995a). This may be particularly important where densities of conspecifics or competitors are high and reproductive systems are based on size-dependent hermaphroditism (e.g.labroid fishes). Evidence that size advantages are maintained after settlement in demersal fish is limited, coming from two sources: repeated measurf:s of individuals, and inferences from otolith microstructure. The latter is yet to be used for studies of the correspondence between larval and post-settlement growth rates in reef fishes. Forrester (1990) repeatedly measured tagged individuals of the tropical damselfish, Dascyllus aruanus, from settlement to 10 months after settlement. He found that size differences among individuals within a social group were maintained for the duration of the study. Only the largest fish at settlement were reproductively mature at the end of the study. A similar pattern of size-dependent growth has been found in the large temperate wrasse, Tautogolabrus adspersus (Tupper 1994), and the Atlantic cod, Gadus morhua (Tupper & Boutilier 1995b). In fish populations that have multiple recruitment events within a season, thf' maintenance of size differences among individuals will be complicated by the prior settlement of conspecifics or competitors. Studies of tropical damselfish, whi(:h generally have strong sizehierarchies, indicate that the maintenance of growth differences among a cohort after settlement depends upon whether larger conspecifics or competing species are present (Ochi 1986; Jones 1987a,b; Forrester 1990). COMPENSATORY GROWTH MECHANISMS Growth compensation is the term applied to describe a reduction in size differences among individuals due to changes in individual growth patterns (e.g. when an individual that grows slow'~r than the population average begins to grow faster than average). To my knowledge, there are few demonstrations of compensatory growth for reef-fish populations. This may be a function of the lack of studies 'that have examined individual growth, especially during the pelagic to demersal transition. Intuitively, there is a strong likelihood that growth compensation is an important component of an individual's success after settlement for demersal fish. The pelagic and demersal environments impose radically different ecological and physiological constraints on

3 IMPORTANCE OF FISH CONDITION AT SETTLEMENT 259 individual's capabilities at the time of settlement. If predation is selective with respect to some aspects ofindividual quality, then this high predation pressure shortly after settlement may have important: and long-lasting implications for the juvenile population. Key questions in an examination of the link between the early pelagic life history and demersal life stages, as reflected by the condition of newly settled fishes, include the following. To what extent do fish within a population vary in condition at settlement? Is this variability maintained in the juvenile population, and if so how? Is high quality at settlement linked to persistence on the reef or other measures of individual success? This paper briefly addresses these issues and, in doing so, highlights the valuable insight into the population dynamics of reef fishes that cain be obtained by assessing the phenotypic variability of individuals at settlement. VARIABILITY IN PHENOTYPES AT METAMORPHOSIS AND SETTLEMENT While it is no surprise that fish vary in their growth and condition at settlement, quantifying and contrasting the levels of variability in phenotypes is the first step in evaluating the consequences of varying environments on these characters. Larval duration has been estimated for more than 300 species of reef fish. Reliable estimates of size at settlement exist for fewer species (Victor 1991). Most estimates are based on small sample sizes «10 fish) and there is a paucity of information on levels ofvariability in size or age at settlement. However, when large samples are examined (e.g. Victor.l986b), or when fishes from multiple sites or times are compared (e.g. Wellington & Victor 1992; McCormick 1994; Sponaugle & Cowen 1994), high levels of variability are commonly found (see Cowen & S,ponaugle 1997). Levels of variability are species specific with overlying familial trends (e.g. labrids and acanthurids tend to have greater larval durations relative to mullids and pomacentrids). Regardless of the magnitude of the larval duration or size at settlement, both have been found to vary significantly among locations and across time within a species. McCormick (1994) partitioned the variation in larval duration and size at settlement for eight samples of settling goatfish (Upeneus tragula) at one sampling station on the Great Barrier Reef (GBR), collected over a 2 month period. Sampling month accounted for 20% of the variation in size at settlement whereas differences among samples within a month explained 49% of the variability in larval duration. Much of the remaining variability in these attributes (51 % for duration, 75% for size) was explained by differences among individuals within a sample. On a broader time scale, Kerrigan (1996) found that differences among three consecutive recruitment seasons explained 18% of the variability in size and only 8% of the variability in larval duration for the common tropical damselfish Pomacentrus amboinensis. Differences in lunar pulses of settlers within a season accounted for 20 and 15% of the variation in size and larval duration, respectively. Once again, differences among individual fish within a pulse accounted for most of the variation in size and age at settlement (60 and 77%, respectively). In both studies, differences among samples (or pulses in settled1ent frequency) and years were attributed to pelagic processes such as the availability of food, or water tempt:rature influencing growth and developmental rates. Most of the growth c:stimates for reef fish are only rough approximations of average growth during the larval period, calculated from size and age at settlement for individuals (e.g. Mc<:;ormick 1994; Kerrigan 1996), or averages for a cohort from a restricted size distribution (e.g. Thorrold & Milicich 1990). Growth trajectories have seldorn been examined in detail for individuals (such as when properly validated backcalculation of growth histories are used). Variability in growth during the larval stage is typically high and has been attributed to three causes: variable water temperature during the larval life stages (e.g. Francis 1994; McCormick & Molony 1995), food availability (McCormick & Molony 1992) and delays in settlement once a stage of physiological competence has been reached (Cowen 1991). Other factors, such as genetic and non-genetic parental influences, water quality and salinity, which have been found to affect growth in temperate fisheries species, are also likely to influence the growth of reef fishes. Substantial levels of variability have also been found in the nutritional condition of reef fish at settlement, quantified by the total lipid, protein and carbohydrate composition of individual fish (McCormick & Molony 1993; Kerrigan 1996). Kerrigan (1996) found that for two species of tropical damselfish, nutritional composition varied significantly both among lunar pulses of recruits and between y~ars. Trends in lipid and protein composition between years and among pulses were similar for the two spe(:ies, suggesting that they were influenced by similar processes in the pelagic environment (Fig. 1). The two studies that have examined the interrelationships among various measures of condition at settlement (McCormick & Molony 1993; Kerrigan 1996) have found correlation~ among measures to be weak. In particular, fish lengtll was weakly correlated to concentrations of energy storage products. These weak correlations also suggest that no single measure of condition comprehensively describes a fish's potential to survive or compete; a conclusion also reached by a number of temperate studies (Theilacker 1978; Neilson et al. 1986). Selective pressures directed at one trait

4 262 M. I. McCORMICK predation on juvenile fish have used otoliths to backcalculate sizes of cohorts of known initial size distributions. Properly validated (Campana & Jones 1992), this method has proven to be a powerful method of examining the action of accumulated past predation events on the juvenile stages of freshwater and marine fishes (e.g. Post & Prankevicius 1987; Yamashita et at. 1994). This technique has yet to be used to examine the influence of selective predation on reef-fish populations or the influence of larval growth history on post-settlement growth dynamics. CONDITION AT SETTLEMENT AND PERSISTENCE Information on the ensuing effects of differential condition of recruits is central to an understanding of the importance of fish condition to reef-fish population dynamics. To date, only one field study has addressed the relationship between fish condition at settlement and subsequent persistence of individuals. Preliminary evidence for the tropical reef fish Pomacentrus moluccensis suggests that biochemical condition at the time of settlement does influence post-settlement persistence (D. J. Booth pers. comm. 1996). Six locations at Bowden Reef, central GBR, were monitored for larval supply and recruitment during the summer of , using light traps and visual censuses. Light trap collections of fish from each recruitmenlt pulse were assayed for total lipid composition. The survival of each pulse of fish was determined using visual.. censuses and back-calculated recruitment dates from s81mples of juveniles collected in the July following recruitment. The proportion of recruits that arrived in Nc)vember 1992 and which persisted until the July 1993 collection was positively correlated to the total lipid content of the recruits across the six study sites. The addition of information on the lipid content of recruits enhanced the ability of recruitment information to predict persistence by 30%. Mechanisms for this relationship are unclear, but it is hypothesized that recruits with higher lipid levels may be able to avoid predation or exploit food resources more efficiently. SYNTHESIS Evidence presented here highlights the potential for research on the consequences of phenotypic variation at settlement to provide novel insights into the processes influencing fish population dynamics. This brief review emphasizes the embryonic nature of these types of studies for reef-fish systems and points to the need for further research into all aspects of how phenotypic attributes of individuals relate to past life-history events, future survival and success. The ability to rear reef fish from eggs of known parentage through to the juvenile stage will greatly advance our understanding of the link between larval life history and subsequent success or failure of individuals once settled. The pressing requirement for detailed laboratory experiments is joined by the need for field experiments thai: complement and extend laboratory results. Further studies of the consequences of phenotypic variability may support the incorporation offish attributes into individual-based models of population dynamics (e.g. Chambers 1993). Although prey condition has not yet been an '~xplicit component of individual-based models, prey size and type, pollutants and other characteristics have be:en included (e.g. references in Van Winkle et at. 1993). Using such models, measures of individual performance and condition can be incorporated to predict population responses to simulated changes in environm(:ntal conditions. ACKNOWLEDGEMENTS Formulation of this work benefited greatly from discussions with Brigid Kerrigan, Howard Choat, Chris Chambers, Dave Booth and lain Suthers. I am especially grateful to Dave Booth for allowing me access to unpublished data. Comments from Chris Chambers and Bob Cowen greatly improved an earlier version of the paper. Many thanks to Creoff]ones and Mark Hixon who, together with a myriad of other helpers, organized the workshop. REFERENCES Bailey K. M. & Houde E. D. (1989) Predation on eggs and larvae of marine fishes and the recruitment problem. Adv. Mar. BioI. 26, Bertram D. F., Chambers R. C. & Leggett W. C. (1993) Negative correlations between larval and juvenile growth rates in winter flounder: implications of compensatory growth for variation in sizt:-and-age. Mar. Ecol. Prog. Ser. 96, Bertram D. F. & Leggett W. C. (1994) Predation risk during the early life history periods of fishes: separating the effects of size and age. Mar. Ecol. Prcg. Ser. 109, Boero F., Belmonte G., Fanelli G., Piraino S. & Rubino F. (1996) The continuity of living matter and the discontinuities of its constituents: do plankton and benthos really exist? Trends Ecol. Eval. 11, Booth D. J. (1991) The effects of sampling frequency on estimates of recruinnent of the domino damselfish Dascyllus albisella Gill. J. Exp. Mar. Bioi. EcoL 145, Booth D. J. (1995) Juvenile groups in a coral-reef damselfish: density-dependent effects on individuals fitness and population demography. Ecology 76, Campana S. E. & Jones C. M. (1992) Analysis of otolith microstructure data. In: Otolith Microstructure Examination and Analysis (eds D. K. Stevenson & S. E. Campana). Can. Spec. PubL Fish. Aquat. Sci 117,

5 IMPORTANCE OF FISH CONDITION AT SETTLEMENT 261 fish. This is illustrated by the fact that many fishes undergo major morphological changes around the time of settlement (e.g. Randall 1961; Makey & McCormick, unpubl. data). Given the variability in body and performance attributes of fish at settlement, and the poor correlation among them (disc:ussed previously), fish that performed best in the pelagic phase may not necessarily be those that perform best once settled. To date, the only study to document compensatory growth over the transition from larvae to juvenile was Bertram et al. (1993). In an aquarium study using winter flounder, Pleuronectes americanus, they demonstrated that size advantages gained during the larval stage could be lost in the early juvenile stage, rather than being accentuated as conventional theory would suggest. They suggested that such compensatory growth may be the result of differences in the timing of developmental events during the ontogeny of individuals. Late-metamorphosing fish (with slower larval growth) have longer developmental intervals and may have organ systems that function better than faster growing, early metamorphosing individuals. Despite the fact that compensatory growth has not been conclusively demonstrated in me field for reef fish, these taxa have been shown to possess the ability to respond rapidly to favourable conditions by increased growth rates. McCormick and Molony (1992) experimentally manipulated the feeding re'gime of late-larval stage goatfish. They found that fish that had been starved close to the point-of-no-ret.:urn could rapidly recover so that at settlement they hlad similar muscle development, biochemical composition and morphology to fish that were fed continuou$ly. Cowen (1991) used otolith increments to infer that larvae of the temperate wrasse, Semicossyphus pulcher, that had been swept offshore by currents had a period of greatly reduced growth rates. However, once settlement occurred these slower growing fish displayed similar growth rates to those that did not have an extended period of reduced growth in their larval stage. If the assumption of a strong positive relationship between otolith growth and somatic growth is correct then this finding may represent one of the only field examples of compensatory growth yet found for reef fish. The expression of an individual's potential for compensatory growth will depend on whether the fish's social interactions combine to suppress or accentuate growth. Priority of settlement may be important in species that have multiple recruitm!ent episodes in a single season, especially when size~based hierarchies exist after settlement. PHENOTYPIC SELECTION B1i PREDATORS The interaction of predation with the size and nutritional status of larval fish is believed to be an important influence on cohort strength in many temperate fishes (Miller et al. 1988; Rice et al. 1993). Predation on young larvae is often size- or agedependent (Bailey & Houde 1989), although it does not necessarily favour those fishes that are larger, older or in better condition :e.g. Methot 1983; Neilson et al. 1986; Rice et al. 1987; Utvak & Leggett 1992; Pepin et al. 1992; Mesa et al. 1994). There is considerably less informatio~ on the size or condition-related selel;tivity of predation on juveniles. In general, the existing evidence is derived from experiments conducted under laboratory conditions with relatively simple test!icenarios of predation (Mesa et al. 1994), with few ;lttempts to verify results with field experiments. Demonstrations of size/conditionselective predation have largely involved freshwater piscivore species as prey, such as salmonids or perch (see references in Mella et al. 1994). Generally, juveniles that were smaller or in poor condition showed higher levels of mortality (Post & Prankevicius 1987; Tsukamoto et al. 1989; Mesa et al. 1994; Ellis & Gibson 1995). The few reef-fish studies that have been undertaken have typically been conducted in the field and have suffered from small sample sizes due to tagging and monitoring limitations (e.g. Booth 1995; Carr & Hixon 1995). Evidence to da1:e from tropical studies suggests the results of predation are species- and situationdependent. In a field study of the small Hawaiian damselfish, Dascyllus albisel12, Booth (1995) found that large juveniles had higher survival during one year of a 2 year study. Similarly, Groll (1984; cited in Booth 1995) used laboratory experiments and field observations to examine predation by the cornetfish (Fistularia sp.) and stomatopods (Crustacea) on D. albisella recruits. He found that smaller recruits were consumed disproportionately to larger recruits in the laboratory, and the size of prey in the guts of both predators from the reef confirmed this apparent size selection. Other field studies have also suggested That predators differentially consume smaller juveniles (e.g. Carr & Hixon 1995). In contrast, McCormick and Kerrigan (1996) found that predation by lizardfish (Synodus sp.) on newly settled goatfish (Upeneus traguia) in the laboratory was nonselective with respect 10 fish size or total fat content. These results support those of Bertram and Leggett (1994) who found neither age nor size of newly metamorphosed winter flo\mder (Pleuronectes americanus) influenced the vulnerability of individual fish to predation by a species of shrimp. Differences in results among these studies may be due to the field-based studies not accounting for variable developmental state with juvenile size, while the laboratory-based studies examined the risk of predation at a constant developmental stage (metamorphosis). Clearly, further studies on the selectivity of predation at settlement are required. Large-scale field examinations of the selectivity of

6 IMPORTANCE OF FISH CONDITION AT SETTLEMENT 263 Carr M. H. & Hixon M. A. (1995) Predation effects on early post-settlement survivorship of coral-reef fishes. Mar. Ecol. Prog. Ser. 124, Chambers R. C. (1993) Phenotypic variability in fish populations and its representation in individual-based models. Trans. Am. Fish. Soc. 122, Chambers R. C. & Leggett W. C. (1987) Size and age at metamorphosis in marine fishes: an analysis of laboratory-reared winter flounder (Pseudopleuronectes americanus) with a review of variation in other species. Can. J. Fish. Aquat. Sci. 44, Cowen R. K. (1991) Variation in the planktonic larval duration of the temperate wrasse Semicossyphus pulcher. Mar. Ecol. Prog. Ser. 69,9-15. Cowen R. K. & Sponaugle S. (1997) Relationship between early life history traits and recruitment among coral reef fishes. In: Early Life History and Recruitment in Fish Populations (ed. R. C. Chambers & E. A. Trippel) pp Chapman & Hall, New York. De Silva S. S. & Anderson T. A. (1995) Fish Nutrition in Aquaculture. Aquaculture Series 1, Chapman & Hall, London. Doherty P. J. & Sale P. F. (1985) Predation on juvenile coral reef fishes: an exclusion experiment. Coral Reefs 4, Ellis T. & Gibson R. N. (1995) Size-selective predation of O-group flatfishes on a Scottish coastal nursery ground. Mar. Ecol. Prog. Ser. 127, Ferron A. & Leggett W. C. (1994) An appraisal of condition measures for marine fish larvae. Adv. Mar. Bioi. 30, Forrester G. E. (1990) Factors influenc~ the juvenile demography ofa coral reef fish. Ecology 71, Francis M. P. (1994) Duration of larval and spawning periods in Pagrus auratus (Sparidae) determined from otolith daily increments. Environ. Bioi. Fish. 39, 13Q-52. Fuiman L. A. & Higgs D. M. (1997) Ontogeny, growth and the recruitment process. In: Early Life History and Recruitment in Fish Populations (eds R. C. Chambers & E. A. Trippel) pp Chapman & Hall, London. Jones G. P. (1987a) Competitive interactio\!ls among adults and juveniles in a coral reef fish. Ecology 68, Jones G. P. (1987b) Some interactions between residents and recruits in two coral reef fishes. J. Exp. Mar. Bioi. Ecol. 114, Kerrigan B. A. (1996) Temporal patterns in size and condition at settlement in two tropical reef fishes (Pomacentridae: Pomacentrus amboinensis and R nagasakiensis). Mar. Ecol. Prog. Ser. 135, Utvak M. K. & Leggett W. C. (1992) Age and size-selective predation on larval fishes-the bigger.is-better hypothesis revisited. Mar. Ecol. Prog. Ser. 81, 13-'24. McCormick M. I. (1994) Variability in age and size at settlement of the tropical goatfish Upeneus traguia (Mullidae) in the Great Barrier Reef lagoon. Mar. Ecol. Prog. Ser. 103, McCormick M. I. & Kerrigan B. A. (1996) Predation and its influence on the condition of a newly settled tropical demersal fish. Mar. Freshwater Res. 47, McCormick M. I. & Molony B. W. (1992) Effects of feeding history on the growth characteristics of a reef fish at settlement. Mar. Bioi. 114, McCormick M. I. & Molony B. W. (1993) Quality of the reef fish Upeneus traguia (Mullidae) at settlement: is size a good indicator of condition? Mar. Ecol. Prog. Ser. 98, McCormick M. I. & Mol,my B. W. (1995) Influence of water temperature during tile larval stage on size, age and body condition of a tropiclil reef fish at settlement. Mar. Bcol. Prog. Ser. 118, Mesa M. G., Poe T. P., Gadomski D. M. & Petersen J. H. (1994) Are all prey created equal-a review and synmesis of differential predation on prey in substandard condition. J. Fish. Bioi. 45, Memot R. D. (1983) Seasonal variation in survival of larval BlIgraulis mordax estimated from me age distribution of juveniles. Fish. Bull. 81, Milicich M. J. (1994) Dyrtamic coupling of reef fish replenishment and oceanographic processes. Mar. Bcol. Prog. Ser. 110, Milicich M. J. & Doherty P. J. (1994) Larval supply of coral reef fish populations: magnitude and synchrony of replenishment to Lizard Island Great Barrier Reef. Mar. Bcol. Prog. Ser. 110, Miller T. J., Crowder L. B., Rice J. A. & Marschall E. A. (1988) Larval size and recruitment mechanisms in fishes: toward a conceptual framewol'k. Can. J. Fish. Aquat. Sci. 45, Neilson J. D., Perry R. I., Valerio P. & Waiwood K. G. (1986) Condition of Atlantic cod Gadus morhua larvae after me transition to exogenolls feeding: morphometrics, buoyancy and predator avoidance. Mar. Bcol. Prog. Ser. 32, Ochi H. (1986) Growth of the anemonefish Amphiprion clarkii in temperate waters, Witll special reference to me influence of settling time on me growth of O-year olds. Mar. BioL 92, Pepin P., Shears T. H. & De Lafontaine Y. (1992) Significance of body size to me interaction between a larval fish (MalloM villosus) and a vertebrate predator (Gasterosteus aculeatus). Mar. BcoL J~g. Ser. 81, Post J. R. & Prankevicius A. B. (1987) Size-selective mortality in young-of-me-year yell:>w perch (Perca fiavescens): evidence from otolim microstructure. Can. J. Fish. Aquat. Sci. 44, Randall J. E. (1961) A concribution to me biology of me convict surgeonfish of me Ha'Naiian islands, Acanthurus sandvicensis. Paclj: Sci. 15, Rice J. A., Crowder L. B. & Binkowski F. P. (1987) Evaluating potential sources of mortality for larval bloater (Coregonus hoyi): starvation and vulnerability to predation. Can. J. Fish. Aquat. Sci. 44, Rice J. A., Miller T. J., Ros'~ K. A. et al. (1993) Growm rate variation and larval survival: inferences from an individualbased size-dependent ];Jredation model. Can. J. Fish. Aquat. Sci. 50, Sponaugle S. & Cowen R. K. (1994) Larval durations and recruitment patterns of two Caribbean gobies (Gobiidae): contrasting early life ilistories in demersal spawners. Mar. BioL 120, Tanaka M., Goto T., 1'omiyama & M. Sudo H. (1989) Immigration, settlerrlent and mortality of flounder (Paralichthys olivaceus:1 larvae and juveniles in a nursery ground, Shijiki Bay, Japan. Neth. J. Sea Res. 24, Theilacker G. H. (1978) Effects of starvation on me histological and morphological characteristics of jack mackerel, Trachurus symmetricus, larvae. Fish. Bull. 76, Thorrold S. R. & Milicich M. J. (1990) Comparison of larval duration and pre- and post-settlement growth in two species of damselfish, Chromis atripectoralis and Pomacentrus coelestis (Pisces: Pomllcentridae), from me Great Barrier Reef. Mar. BioL 105,

7 264 M. I. McCORMICK Tsukamoto K., Kuwada H., Hirokawa J. et ai. (1989) Sizedependent mortality of red sea bream, Pagrus major, juveniles released with fluorescent otolith-tags in News Bay, Japan. J. Fish. BioI. 35, Tupper M. (1994) Settlement and post-settlement processes in the population regulation of a temperate [eef fish: the role of energy. PhD thesis, Dalhousie University, Halifax. Tupper M. & Boutilier R. G. (1995a) Effects of conspecific density on settlement, growth and post-settlement survival of a temperate reef fish. J. Exp. Mal: BioL Eco!; 191, Tupper M. & Boutilier R. G. (1995b) Size: and priority at settlement determine growth and competitive success of newly settled Atlantic cod. Mar. EcoL Prog. Ser. 118, Van der Veer H. W & Bergman M. J. N. (1987) Predation by crustaceans on a newly settled O-group plaice PIeuronectes platessa population in the western Wadden Sea. Mar. EcoL Prog. Ser. 35, Van Winkle W., Rose K. & Chambers R C. (J,993) Individual- based approach to fish pc'pulation dynamics: an overview. Trans. Am. Fish. Soc. 122, Victor B. C. (1986a) Larval settlement and juvenile mortality in a recruitment-limited ccral reef fish population. Ecol. Monogr. 56, Victor B. C. (1986b) Delayed metamorphosis with reduced larval growth in a coral rc:ef fish (Thalassoma bijasciatum). Can. J. Fish. Aquat. Sci. 4B, Victor B. C. (1991) Settlement strategies and biogeography of reef fishes. In: The Ecology of Fishes on Coral Reefs (ed. P. F. Sale) pp Academic Press, San Diego. Wellington G. M. & Victor B. c=:. (1992) Regional differences in duration of the planktonic larval stages of reef fishes in the eastern Pacific Ocean. Mar. BioI. 113, Yamashita Y., Nagahora S., Yamada H. & Kitagawa D. (1994) Effects of release size on survival and growth of Japanese flounder ParaIichthyS olivaceus in coastal waters off Iwate Prefecture, northeastern japan. Mar. Ecol. Prog. Ser. 105,