Mechanisms of density- and number-dependent population regulation of a coral-reef fish

Transcription

1 Mar. Freshwater Res.,, 53, Mechanisms of density- and number-dependent population regulation of a coral-reef fish Jeffrey S. Shima Department of Ecology, Evolution, and Marine Biology, and the Marine Science Institute, University of California, Santa Barbara, CA 9316, USA. Present address: School of Biological Sciences, Kirk Building, Kelburn Parade, PO Box 6, Victoria University of Wellington, Wellington, New Zealand Abstract. Density-dependent post-settlement losses are a common feature of many reef fish populations, and resent observations suggest that losses may also scale with population size independent of density (i.e. number-dependence ). Despite the potential importance of these two forms of compensatory loss, there have been relatively few attempts to determine the mechanisms underlying these demographic patterns. A factorial experiment was conducted to test whether density- and/or number-dependent losses observed for newly settled six bar wrasse (Thalassoma hardwicke) are attributable to predation or another factor (e.g. migration). Losses of recently settled fish from reefs within predator exclosures were 6% over a 7-day period and apparently independent of density and number of residents. Losses from reefs that were accessible to predators averaged 6% over 7 days, and were dependent upon both the density and number of resident fish. Behavioural observations indicate the frequency of agonistic interactions between resident six-bar wrasse scales with the number of fish independent of density. Overall, results attribute both density-and number-dependent losses to predation, and suggest that number-dependent behavioural interactions (perhaps important for the social control of sex change) rather than proximate resource limitation may underlie observed number-dependent mortality. Extra keywords: density-dependence, number-dependence, predation, recruitment, reef fish. MF113 Popul Jeffrey ation S. Shi r egul ma ation of a coral-reef fish Introduction Local population density may influence rates of growth, migration, and mortality to reshape patterns of larval settlement and contribute to the dynamics of marine reef populations (reviewed in Doherty 1991; Hixon 1991; Jones 1991). Because these density-dependent (i.e. compensatory) demographic rates potentially regulate local populations (Murdoch 199; Turchin 1995), they have served as a focal point for reef fish ecology (Booth and Brosnan 1995; Caley et al. 1996). Although numerous studies have documented density-dependent mortality in reef fishes (reviewed in Schmitt and Holbrook 1999; Shima 1a), there have been relatively few investigations of the mechanisms producing this density dependence. Studies that have manipulated predator access or prey refuges (e.g. Hixon and Beets 1989, 1993; Steele 1999) coupled with circumstantial and correlative evidence for post-settlement predation in reef fish systems (reviewed in Hixon 1991) have contributed to the widely held view that density-dependent losses arise from predation upon individuals competing for a limited number of prey refuges. Only in rare instances has such a mechanism been confirmed in experimental studies (e.g. Hixon and Carr 1997). Sinclair (1988) discusses the importance of separating demographic consequences of population density from population size, and more recent work has demonstrated that compensatory losses of a reef fish may also result from numerical effects independent of density (Shima 1a). Such number-dependence is characterized by per capita loss rates that scale with the absolute number of individuals per site rather than with numbers per site area (i.e. the ratio of individuals to resources is inconsequential). For example, per capita losses in a group of 1 individuals occupying a 1 m patch are greater than a group of individuals in a m patch, despite the fact that in both cases density is 1fishm. On the assumption that reef area is a reasonable proxy for resources including refuges from predators, the existence of number-dependent losses appears to require a different mechanism than one where prey species compete for limited refuge space. The present study employs a factorial experiment to test whether density- and/or number-dependent losses observed for the six-bar wrasse (Thalassoma hardwicke) may be attributable to predation or another factor (e.g. migration). Larval stages of six-bar wrasse develop in pelagic environments for 7 days (Victor 1986) and subsequently settle to CSIRO 1.171/MF //175

2 176 Jeffrey S. Shima small patch reefs on Moorea during new moons from January through June (Shima 1999a, 1a, 1b). Newly settled individuals experience strong density-dependent losses within weeks (Shima 1a) to months (Shima 1999a, 1b) of settlement, and early post-settlement losses are also influenced by the number of individuals resident on a patch reef independent of density effects ( number-dependence, sensu Shima 1a). This study addresses potential mechanisms of density- and number-dependent losses experienced by newly settled six-bar wrasse. Materials and methods Research was conducted within the shallow lagoons of the island of Moorea, French Polynesia (17 3 S,19 W), and focused on post-settlement survival and behaviour of the six-bar wrasse (Thalassoma hardwicke). Density- versus number-dependent mortality and the role of predators Decoupling effects of density and number. Shima (1a) presents the details and rationale behind the factorial experiment conducted in May 1999 to decouple variation in per capita loss rates attributable to density (no. fish per reef area) from those attributable to the number of residents per reef (i.e. independent of density). This experiment followed survival over 7 days of newly settled six-bar wrasse that were transplanted to patch reefs (depopulated of conspecifics prior to experiment) at two typical densities (.5 or. fish m ). Fish densities were achieved by manipulating the number of fish (either 1 or individuals; most common range for this species) on reefs of three typical size categories (,, or 8 m ). This design resulted in replicate fish (n = fish per treatment; see Table 1) experiencing a group size of 1 at densities of.5 or. fish m, or a group size of at densities of.5 or. fish m. Per capita loss rates were estimated for each patch reef as the fraction of transplanted individuals that were lost over a 7-day period, and were analysed by logistic ANOVA to accommodate a trinomial distribution of the data (i.e. fractional losses were %, % or 1%). The design incorporated samples of each treatment equally distributed across 5 sites separated from each other by 1 km. These were treated as randomized blocks in the analysis, and block effects were subsequently deemed non-significant. Effects of predators on losses At one of these sites, I repeated the factorial manipulation of density and number of fish on a subset of patch reefs that were enclosed in cages. Using a random number table, I selected reefs for predator exclusion from a larger set of reefs that conformed to reef size and substratum attributes detailed in Shima (1a). Cages were custom-designed to exclude potential predators (i.e. large piscivorous fishes and invertebrates) while still allowing emigration of new settlers (verified by observing emigration of individuals through mesh when cages were placed over barren sand). Cages were constructed of.635 cm square knotless mesh (Delta Style, Memphis Net & Twine Co.), and were cylindrical, measuring either 1.83 or 3.5 m diameter, and 3.66 m in height. Cylinders were weighted with galvanized chain (.95 cm link diameter) flush with the reef flat surrounding the base of patch reefs, and floated at the surface with a contiguous ring of foam buoys to exclude predator immigration. Prior to transplantation of new settlers, I attempted to remove all resident piscivores from caged reefs by use of hand nets and quinaldine anaesthetic. Because I was working with a limited number of cages (n = 1), densities number treatments were conducted over field seasons in 1998 and 1999 (concurrent with un-caged factorial treatments in 1999 only, Table 1); hence results necessarily include the assumption that treatment effects were constant between years. Caged reefs were censused daily for predators; caged reefs containing predators were excluded from statistical analyses (no. of excluded reefs, 3 for 1998, for 1999). The role of predators was evaluated along with density- and number-dependent effects with the aid of a categorical analysis of variance (CATMOD Procedure, SAS). This procedure estimates linear parameters based on weighted least squares (response function = mean), but does not assume the response (i.e. mortality, in this case %, %, or 1%) to be normally distributed. Non-significant interactions were sequentially excluded from ANOVA models. Behaviour patterns dependent upon density or number? I conducted a set of behavioural time-budget observations to explore patterns of density- and/or number-dependence in behavioural attributes that may contribute to observed patterns of mortality of newly settled six-bar wrasse. For seventy focal individuals haphazardly selected from 7 different patch reefs (reefs were selected randomly with the aid of a random number table), I recorded the number of agonistic encounters (i.e. chases by other conspecifics or heterospecific residents) in a 1-min period. I recorded all behavioural data while on snorkel, positioned >3 m from the focal individual, and my presence did not appear to alter the behaviour patterns of residents on the focal patch reef. All observations were made on focal individuals 5 mm in total length (corresponding to fish < months post-settlement age; Shima 1999a) between 11 and 1 hours (time of peak activity), May June Following each 1-min observation, I estimated the number of resident conspecifics and quantified the size of each reef (to facilitate estimates of density as number of six-bar wrasse per area of reef) using Table 1. Experimental design used to explore effects of predators on density- and number-dependent mortality Predator Population Population Reef Reef Fish Year exposure size (no. reef 1 ) density (no. m ) area (m ) n n Uncaged 1.5 A 1999 Uncaged 1. A 1999 Uncaged A 1999 Uncaged. 5 A 1999 Caged Caged Caged Caged A Reefs were evenly divided among five blocks separated by ~1 km; block effects were not significant (Shima 1a)

3 Population regulation of a coral-reef fish 177 methods of Shima (1a, 1b). Chase frequencies were analysed by ANCOVA (GLM Procedure, SAS), with number of resident conspecifics treated as a categorical variable (, 1,, or 3 or more ; only three reefs had values >3), and conspecific density as a covariate. Non-significant interactions were excluded from analyses. Results Density- versus number-dependent mortality and the role of predators In the absence of predators, newly settled six-bar wrasse experienced rates of loss estimated to be 6% over a 7-day period. Losses from reefs exposed to predators were significantly greater ( 6% over 7 days), and suggest that 36% of the losses in this experiment resulted from predation while the remaining 6% may be attributable to some combination of handling mortality, emigration, starvation or disease. Patterns of losses from caged reefs appear independent of both density and number (Fig. 1). In contrast, reefs exposed to predators experienced significant densityand number-dependent losses (Fig. 1; details in Shima 1a). Although statistical power to detect a significant interaction between predator-exposure and density and/or number treatments was quite low in this study ( predator exposure density P =.; predator exposure number P =.39; Table ), overall results present a compelling pattern suggestive of predator-mediated densityand number-dependent mortality (Fig. 1). Behaviour patterns dependent on density or number? Resident conspecifics accounted for 67% of all chases incurred by juvenile six-bar wrasse. Heterospecific juvenile 1 labrids (primarily Pseudocheilinus hexataenia) accounted for 18% of the chases, while territorial damselfish (Stegastes nigricans) were responsible for 7%. Only two chases from potential predators were observed in >7 min of focal observations (one from a hawkfish Paracirrhites arcatus, the Table. Analysis of variance of per capita mortality over 7 days of newly settled six-bar wrasse as affected by predators (either caged or uncaged reefs), number of newly settled wrasse per reef (either 1 or ), or the density of newly settled wrasse per reef (either.5 or.5 fish m ) Results were obtained by fitting linear models to functions of categorical data (response function = mean ) by the CATMOD Procedure of SAS. Non-significant interactions were sequentially dropped from the analysis. Non-significant residual χ indicates a significant model fit Source df χ P Intercept <.1 Predator exposure <.1 Number per reef Density Residual A. Per capita loss Chases incurred (no. per 1 min) B. No. per patch reef Density Fish / m. Fish / m Fig. 1. Mean per capita mortality over 7 days (±1 s.e.) for fish on reefs caged to exclude predators (open bars) and uncaged reefs (shaded bars). Fish were stocked to reefs at low or high density, and either as solitary individuals or in groups of two. Statistics given in Table indicate significant effects of predator exposure, density, and number per reef, with no significant interactions between main-effects Density of conspecifics (no. per m reef) Fig.. Chases incurred by focal six-bar wrasse over a 1 min period as a function of their density (No. six-bar wrasse m reef). Frequencies of (A) total incurred chases and (B) chases by conspecifics did not scale significantly with conspecific densities (A: P =.1, r =.; B: P =.13, r =.3; see supporting statistics in Table 3).

4 178 Jeffrey S. Shima Table 3. Analysis of covariance of chases incurred by focal individuals over 1 min, as affected by the number of neighbouring six-bar wrasse per reef (, 1,, or 3 or more ) and the density (no. per reef area) of six-bar wrasse per reef (treated as a continuous covariate) Non-significant interactions were sequentially dropped from the analysis A. Chases from all species Source df MS F P Number per reef Density Error B. Chases from conspecifics Source df MS F P Number per reef Density Error Chases incurred (no. per 1 min) OR MORE Number of conspecific neighbors (per patch reef) Fig. 3. Mean chases incurred by focal six-bar wrasse over a 1 min period (±1 s.e.) as a function of number of neighbouring conspecific fish per reef. Frequencies of total incurred chases (open bars) and chases by conspecifics (shaded bars) scaled with the number of conspecific fish per reef, but not with their densities (Table 3, Fig. ). other from a triplefin: Family Tripterygiidae). Frequencies of chases (both the total number of chases, and those from conspecifics only) were explained by the number of individual six-bar wrasse per patch reef, with no effects attributable to density (Fig., Table 3). Number of chases increased with the number of conspecifics resident on a reef (Fig. 3); if such agonistic interactions increase the likelihood of predation, these number-dependent behaviour patterns may contribute to the predator-induced number-dependent mortality observed in the above experiment. Discussion Results of the factorial manipulation of density, number, and predator exposure suggest that newly settled six-bar wrasse populations may be regulated by predator-mediated density- and number-dependent mortality. Although the occurrence of both density- and number-dependent losses has been documented elsewhere for this species (Shima 1a), the mechanisms potentially responsible for these compensatory effects have heretofore remained unexplored. Losses resulting from density-dependent emigration (i.e. movement from a focal reef to a neighbouring reef) are likely to have vastly different consequences for population and community dynamics at larger scales than losses resulting from mortality events. In this study I constructed cages that excluded predators from patch reefs but still allowed migration of newly settled six-bar wrasse between reefs. Although it is conceivable that cages may have slowed rates of migration between reefs, the fact that fish were physically capable of navigating the cage mesh to move from barren sand to nearby patch reefs, coupled with circumstantial evidence that this species rarely migrates between patch reefs in the absence of cages (Shima 1999b), suggests that any such bias was likely to be quite low. Elevated survivorship of individuals (apparently independent of density and number of fish per reef ) within cages was strongly indicative of predation as an important mechanism of compensatory loss. Recent studies have confirmed the important role of predators in the regulation of local reef-fish populations (Hixon and Carr 1997), and density-dependence is commonly viewed as arising from interference competition between individuals for refuges from predators (Hixon 1991; Caley 1993; Hixon and Beets 1993; Caley and St John 1996). The conceptual model underlying many of these studies is one of refuges (e.g. branching corals, seagrass beds, macroalgae) that vary in quantity and/or quality, such that the likelihood of being consumed by a predator is dependent upon the number of fish relative to the number/quality of refuges. For patterns of mortality that appear to scale with the number of fish independent of the number of potential refuges (i.e. number-dependence ), some other mechanism is likely to be responsible for compensatory mortality (e.g. Connell ). Behavioural observations of six-bar wrasse suggest that frequencies of agonistic encounters between conspecifics scale with the number of individuals on a patch reef more so than with their density. Because the six-bar wrasse is a sex-changing species, there exists the potential that this numerical scaling may reflect interactions directed at establishment of dominance hierarchies controlling sex-change rather than those that result from interference competition for refuges from predators. Although such interactions prior to sexual maturity have received little attention, recent work on another sex-changing reef fish (Amphiprion spp.) suggests that establishment of social dominance may begin early in the juvenile stage for some species (P. Buston, personal communication). Such

5 Population regulation of a coral-reef fish 179 interactions, if important, may increase the likelihood of emigration for the loser, and this may provide a partial explanation for the non-significant trend of increased losses on reefs with higher numbers of individuals in the absence of predators. If such agonistic encounters also attract the attention of nearby predators (e.g. Elkin and Baker ), and/or if chase-time is inversely proportional to vigilance (because chased fish may not be mindful of predators), number-dependent behaviour patterns interacting with predation may constitute an alternative mechanism that can account for number-dependent compensatory mortality of recently settled six-bar wrasse. In such a situation, behavioural interactions (e.g. social posturing related to sex change) that are decoupled from proximate limiting resources (e.g. food availability, refuges from predators) may indirectly result in patterns of compensatory mortality capable of regulating local populations. This work underscores the need to consider indirect effects of behavioural interactions in addition to more traditional views of resource limitation as potential mechanisms contributing to the regulation of local populations. Acknowledgments This work would not have been possible without field assistance from S. Kleinschmidt. Logistic support was provided K. Seydel, B. Williamson, and the staff of the Gump Research Station on Moorea. The contents of this manuscript benefited from discussions with R. Schmitt, S. Holbrook, S. Gaines, R. Warner, N. Phillips, A. Stewart-Oaten, and A. Brooks, and comments on versions of the manuscript were kindly provided by S. Holbrook and R. Schmitt. Funding for this work was provided by RTG and GRT Programs in Spatial Ecology (NSF BIR and NSF GER93 587, both to W. Murdoch), an NSF award to R. Schmitt and S. Holbrook (OCE ), and the Partnership for the Interdisciplinary Study of Coastal Oceans (PISCO Supported by the Packard Foundation). This is contribution No. 8 of the UC Berkeley Gump Research Station and No. of PISCO. References Booth, D. J., and Brosnan, D. M. (1995). The role of recruitment dynamics in rocky shore and coral reef fish communities. Advances in Ecological Research 6, Caley, M. J. (1993). Predation, recruitment, and the dynamics of communities of coral reef fishes. Marine Biology 117, Caley, M. J., and St John, J. (1996). Refuge availability structures assemblages of tropical reef fishes. Journal of Animal Ecology 65, 1 8. Caley, M. J., Carr, M. H., Hixon, M. A., Hughes, T. P., Jones, G. P., and Menge, B. A. (1996). Recruitment and the local dynamics of open marine populations. 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