Behavioral interactions among individuals both influence

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1 Behavioral Ecology Vol. 11 No. 5: Integrating individual behavior and population ecology: the potential for habitat-dependent population regulation in a reef fish Phillip S. Levin, a Nicholas Tolimieri, b Matthew Nicklin, c and Peter F. Sale d a Northwest Fisheries Science Center, National Marine Fisheries Service, 2725 Montlake Boulevard E, Seattle, WA 98112, USA, b University of Auckland, Leigh Marine Laboratory, PO Box 349, Warkworth, New Zealand, c Department of Biology, Northeastern University, Boston, MA 02115, and d Department of Biology, University of Windsor, Windsor, Ontario N9B 3P4, Canada We used the predictions of the ideal free and ideal despotic distributions (IFD and IDD, respectively) as a basis to evaluate the link between spatial heterogeneity, behavior, and population dynamics in a Caribbean coral reef fish. Juvenile three-spot damselfish (Stegastes planifrons) were more closely aggregated in patch reef habitat than on continuous back reef. Agonistic interactions were more frequent but feeding rates were lower in the patch versus the continuous reef habitat. Growth rates were lower in patch reef habitat than on the continuous reef, but mortality rates did not differ. A separate experiment using standard habitat units demonstrated that the patterns observed in natural habitat were the result of the spatial distribution of the habitat patches rather than resource differences between habitats. Our results do not follow the predictions of simple IFD or IDD models. This deviation from IFD and IDD predictions may be the result of a number of factors, including lack of perfect information about habitat patches, high movement costs, and higher encounter rates of dispersed patches. Our results demonstrate that behavioral interactions are an integral part of population dynamics and that it is necessary to consider the spatial organization of the habitat in both behavioral and ecological investigations. Key words: damselfish, habitat structure, ideal free distribution, recruitment, Stegastes planifrons. [Behav Ecol 11: (2000)] Behavioral interactions among individuals both influence and are influenced by demographic processes. Many of the ecological processes that determine population size or dynamics are explicitly behavioral, and fully understanding ecological phenomena such as predator prey interactions, some forms of interference competition, dispersal, and patterns of habitat use often requires knowledge of specific behavioral interactions occurring among individuals (Fryxell and Lundberg, 1998; Hassell and May, 1985; Mangel and Clark, 1988; Smith and Sibly, 1985; Sutherland, 1996). Behavior can also profoundly affect the dynamics of populations by adding or modifying density dependence (Chesson and Rosenzweig, 1991). Although there is a compelling body of theory linking behavioral and population ecology (e.g., Abrams, 1989, 1992; Fryxell and Lundberg, 1998; Holt, 1983; Houston and Mc- Namara; 1997; Ives and Dobson, 1987; Sih, 1984; Sutherland, 1996), empirical work exploring this linkage is sparse (Anholt, 1997; Dunbar, 1985; Fryxell and Lundberg, 1998; Gilliam, 1987). The effects of spatial heterogeneity of resources on patch use and movement of animals has been a mainstay of behavioral ecology. Fretwell (1972; Fretwell and Lucas, 1970) deduced that individuals should distribute themselves among patches that vary in resources and conspecific density such that the average reward is the same for individuals in different patches. Thus, individuals will distribute themselves such that the ratio of density between any two patches will equal the Address correspondence to P. S. Levin. phil.levin@noaa.gov. Received 23 August 1999; revised 3 April 2000; accepted 5 April International Society for Behavioral Ecology ratio of the resource levels of those patches (Hugie and Grand, 1998). This model assumes that individuals have perfect information about the relative availability of resources and are free to move among patches. Following these assumptions, it is referred to as the ideal free distribution (IFD). Although the IFD model was originally conceived in terms of birds choosing nesting habitats, it has been widely applied to a diversity of animal taxa (Kacelnik et al., 1992; Milinski and Parker, 1991; Tregenza, 1994) and recently to plants (Gersani et al., 1998). Because IFD models directly address the behavioral mechanisms producing density-dependent growth, fecundity, and mortality, they have clear implications for population dynamics (Fryxell and Lundberg, 1998; Sutherland, 1996). Fretwell (1972) also acknowledged that frequency-dependent habitat selection need not necessarily result in IFDs. In particular, Fretwell proposed the ideal despotic distribution (IDD) as an alternative to IFD when territorial behavior prevents free entry to or movement among patches. In IDD models, the suitability of a patch for an individual declines with the order of settling, but the presence of new individuals does not decrease the suitability for those that have already settled (Sutherland, 1996). The IDD differs from IFD in that the average reward differs among patches, even though at any time, settling individuals obtain the same reward in both places (Kramer et al., 1997). In addition to resource levels, the structure of a habitat can affect local densities of animals as well as the frequency or intensity of behavioral interactions. For example, animals in structurally complex habitats may encounter each other at lower frequencies than in structurally simple habitats (Chesson and Rosenzweig, 1991). As a consequence, aggressive interactions will be reduced in complex habitats, and thus, the

2 566 Behavioral Ecology Vol. 11 No. 5 strength of interference competition will also be reduced (Anholt, 1990; Dye, 1984). The pattern of dispersion of a population and thus local densities often reflects responses of individuals to structural attributes of the habitat (Brown, 1975; Wilson, 1975). For instance, the degree of aggregation of endophytaphagous insects and reef fishes can be closely linked to the dispersion pattern of the vegetation they use as foraging and refuge habitat (e.g., Levin, 1993; Morris et al., 1992). In sites where vegetation is clumped, individual animals will experience a higher local density relative to sites in which plants are randomly or regularly dispersed. If increased density influences the occurrence of aggressive interactions (Boccia et al., 1988; Ens and Goss-Custard, 1984; Goss-Custard and Sutherland, 1997; Jones, 1984; Sale, 1972), the degree of patchiness of a habitat will affect the frequency of behavioral interactions. Foraging rates of animals are affected by at least two conflicting parameters: the density of prey and the density of conspecific and heterospecific competitors and thus levels of interference (Sutherland, 1996). IFD models describe a solution to this conflict in which consumers adjust their densities in relation to prey levels such that foraging rates are equal in all prey patches. For animals in which local densities and thus levels of interference are determined, at least in part, by the structure of the habitat, attributes of the habitat must also be included in assessment of foraging behavior. Two patches that vary in structural complexity, for example, may have the same prey levels, but for given consumer densities, levels of interference will be lower in structurally complex than in simple habitat (Anholt, 1990; Dye, 1984). As a result, the effect of habitat structure on encounter rates will increase the strength of density dependence even though both prey and consumer densities are identical. The increased interference can influence population size or dynamics by reducing rates of growth, survivorship, or reproduction (Sutherland, 1996). Although theory and individual empirical studies suggest that habitat structure, behavioral interactions, and demography should be linked, few studies have explicitly explored these links. This is especially true in marine habitats in general and coral reefs in particular, where simple linkages between habitat and demography have only recently received attention (Booth and Wellington, 1998). In the present study, we extended previous work linking habitat and demography or behavior by exploring linkages between habitat structure, behavioral interactions, and juvenile demography in the three-spot damselfish Stegastes planifrons. Specifically, we asked: (1) Does the spatial pattern of juvenile fish vary among habitats? (2) Are foraging rate or the frequency of aggressive interactions affected by the structure of the habitat? and (3) Do habitat-dependent differences in behavior result in changes in growth or mortality rates? METHODS Study species Three-spot damselfish are common members of Caribbean reef communities (Emery, 1973). Adults vigorously defend small territories year-round on the corals Acropora palmata or A. cervicornis against numerous fish and invertebrates (Itzkowitz, 1977; Myrberg and Thresher, 1974; Thresher, 1976; Williams, 1978). Within territories, three-spot damselfish cultivate algal lawns as a food resource and guard demersal eggs (Itzkowitz, 1977; Kaufman, 1977; Williams, 1978). Both adults and juveniles feed on benthic algae as well as on benthic and planktonic crustacea (Emery, 1973; Randall, 1967). Threespot damselfish spawn throughout the year on a lunar cycle and produce demersal eggs that are defended by males (Williams, 1978). After hatching, larvae enter an approximately 26-day dispersive planktonic stage before settling primarily to habitat dominated by the mounding coral Montastrea annularis (Tolimieri, 1995). Settlement occurs episodically around new moons (Robertson, 1992), and fish average 10.5 mm (SL) at settlement. Spatial patterns of fish recruitment We quantified nearest neighbor distances of juvenile threespot damselfish ( 45 mm SL) in two reef habitats within Tague Bay on the northeast shore of St. Croix in the United States Virgin Islands in 1991 and again in A well-developed bank barrier reef separates Tague Bay from open water. The reef surface is composed mostly of dead Acropora palmata rubble. Heads of Montastrea annularis and Porites porites and massive corals such as Siderastea sideria are scattered throughout the back reef area. Small patch reefs (frequently 1 m 3 ) composed mostly of M. annularis as well as massive corals were scattered just landward of the backreef. Tolimieri (1995, 1998) provides a more detailed description of this site. We sampled along the continuous back reef and patch reefs m shoreward of the main reef. To measure nearest neighbor distances, we haphazardly selected individual fish and noted the point of first observation. We then searched for other three-spot damselfish in the vicinity and measured the distance between the original fish and its nearest neighbor. No fish was sampled twice (i.e., once as the focal animal and again as a nearest neighbor). We used a two-factor ANOVA to compare nearest neighbor distances between continuous reef and patch reef habitat with habitat type and sampling year as the main effects. Before analysis we tested for homogeneity of variances using Levene s test (Wilkinson et al., 1996). Variances of log-transformed data were homogeneous. Behavioral observations We conducted focal animal observations (Altman, 1974) on juvenile three-spot damselfish in both continuous and patch reef habitat in 1991 and In 1991, we conducted 5-min focal observations, and in 1997 we performed 10-min observations. Fish were observed from a distance of at least 2 m, which was sufficient to allow fish to behave normally. When fish were not in view for the entire observation period, sampling was abandoned and restarted when the fish reappeared. This only rarely occurred, and there was no systematic difference between back and patch reefs in our ability to observe fish. Thus, all data reported here are from individuals that were in full view during the entire observation period. All observations were conducted between 1100 and 1530 h. During each observation, we quantified the number of bites at food items and the number of agonistic interactions in which juvenile damselfish in each habitat were involved. In July 1991, we considered all agonistic behavior including lateral displays, chases, and nips both directed at other fish and received from other fish. In July 1997, we quantified only chases directed at other fish (some of which concluded with nips at other fish) because this was the most prevalent agonistic behavior we observed. Because foraging rate (i.e., the number of bites at food) and the number of agonistic interactions were recorded on individual fish during the same observation period, these behaviors may not be independent of each other. Consequently, we refer to these two parameters collectively as behavior and used multivariate analysis of variance (MANOVA) to compare the behavior of three-spot damselfish on continuous versus patch reefs. MANOVA is used to deal with multiple dependent variables that may be correlated.

3 Levin et al. Linking individual behavior with demography 567 Such variables cannot be tested separately because it is unclear what the correct would be given the correlation between the two variables. Thus, we first used MANOVA to test the hypothesis that habitat affects behavior, and then tested each behavior (foraging and aggression) individually. We performed two separate MANOVAs on data collected in 1991 and 1997 because the duration of the observational period varied. Before analysis we tested for homogeneity of variances using Levene s test (Wilkinson et al., 1996). Variances of log-transformed data were homogeneous. Because continuous and patch reefs differ from each other in both the degree of patchiness and physical location, we performed an experiment on standard habitat units (SHU) in a single location to remove this potentially confounding effect from our observations. SHUs consisted of four PVC pipes (10.2 cm long, 7.6 cm diam) bolted in a cross pattern to a 0.25-m 2 Plexiglas base (Itzkowitz and Makie, 1986). Coral rubble was placed in the center of each unit. SHUs were arrayed in two spatial configurations on a barren sand flat in Discovery Bay, Jamaica (18 30 N, W) in February In the first treatment we positioned four SHUs in the corners of a square such that the center of adjacent SHUs were 1 m apart. In our second treatment SHUs were arrayed in an identical fashion, except the centers of adjacent SHUs were separated by 0.5 m. These distances were selected to reflect average nearest neighbor distances between fish (see Results). Five replicates of each treatment were arrayed in a complete randomized block design such that treatments were separated from each other by 10 m and blocks were separated from each other and natural habitat by 15 m. Juvenile three-spot damselfish ( 45 mm SL) were captured on adjacent natural habitat. We then measured fish (SL) and transplanted one fish to each SHU. Fish were assigned haphazardly to experimental locations. Thus, each experimental plot of four SHUs received four fish. All transplanted fish remained on SHUs. Three days after we transplanted fish, we commenced 5-min focal observations. We recorded both foraging bites and agonistic behavior as we did in our 1997 observations in natural habitat. Data were analyzed with MAN- OVA as described above. Where MANOVA detected significant differences, we tested each dependent variable (feeding rate, aggression rate) with t tests. Effects of habitat on growth and mortality Although demography typically includes age-specific rates of movement, mortality, growth, and reproduction, we limited our demographic analyses to rates of mortality and growth. We first compared the change in standard length of fish on natural continuous and patch reefs to determine whether differences in nearest neighbor distance and behavior might affect fish growth. From 26 May to 10 June 1997, we searched both continuous and patch reef habitat in Tague Bay for newly recruited three-spot damselfish. Fish were collected after being anesthetized with quinaldine and were placed in plastic bags and measured to the nearest 0.5 mm SL. We then gave each fish a unique mark using florescent elastomer (Malone et al., 1999) and returned fish to their original location on continuous or patch reefs. We censused marked fish at approximately weekly intervals until we terminated the sampling between 26 and 31 July 1997 by collecting and remeasuring all marked fish. During each census and upon termination of the sampling, we searched the surrounding habitat for marked individuals that were not at their initial capture/release point. We did not find any marked individuals that were classified as missing during the regular censuses. Because three-spot damselfish have extremely small home ranges (Itzkowitz, 1977; Myrberg and Thresher, 1974; Thresher, 1976; Figure 1 Mean distance among nearest neighbor Stegastes planifrons in continuous and patch reef habitats (n 30 in 1991 and 55 in 1997). Statistical results are given in text. Bars are 1 SE. Williams, 1978), losses of marked fish were ostensibly due to mortality rather than migration. We used analysis of covariance (ANCOVA) to compare change in SL per day between fishes on continuous and patch reef. Initial SL was included as the covariate to control for differences in the starting size of damselfish. Before analysis, we checked data for normality, homogeneity of variance, and homogeneity of slopes. To determine whether mortality rates differed between habitats, we used Fisher s Exact test to compare the number of fish missing on continuous and patch reefs. We included only those fish that survived to their first census to control for mortality that might be attributable to handling effects. We have thus defined mortality rate as the presence of fish from the first census to the final collection. We also examined growth rates of fish on our SHUs. After fish were captured and measured, individuals on sets of four SHUs were individually marked using fin clips. After 15 days, fish were recaptured, placed in plastic bags, and measured to the nearest 0.5 mm SL. RESULTS Spatial patterns of fish recruitment In both habitats, nearest neighbor distances were never 2.5 m. However, nearest neighbor distances were consistently shorter in patch than in continuous reef habitat (F 1, , p.001; Figure 1). In both 1991 and 1997, nearest neighbor distances on patch reefs averaged about 47 cm, while on continuous reefs nearest neighbor distances averaged about 105 cm (Figure 1). We were unable to detect a difference in nearest neighbor distance between years (F 1, , p.98), nor was there a significant interaction between habitat type and year (F 1, ; p.85). Behavioral observations Natural habitat Our focal observations of three-spot damselfish revealed clear differences in behavior between continuous and patch reef habitats in both 1991 (MANOVA, Pillai trace 0.64, df 1,50, p.001) and 1997 (MANOVA, Pillai trace 0.56, df 1,61, p.001). In 1991, fish in continuous habitat took significantly more bites at food than fish on patch reefs (Figure 2; t 6.70, df 52, p.001). Likewise, in 1997, on continuous reefs, we observed three-spot damselfish foraging

4 568 Behavioral Ecology Vol. 11 No. 5 Figure 2 Mean number of bites at food or chases per focal animal observation in 1991 and 1997 in continuous and patch reef habitats by Stegastes planifrons (n 30 in 1991 and 55 in 1997). ***p.001. Bars are 1 SE. at more than double the rate seen on patch reefs (Figure 2; t 7.50, df 61, p.001). The number of agonistic interactions in which three-spots were involved was lower on continuous and than on patch reef habitat (Figure 2). In 1991, damselfish were involved in an average of fourfold more agonistic interactions on patch than continuous reefs (t 6.028, df 49, p.001). Similarly, in 1997 we observed three-spot damselfish in more than twice the number of agonistic interactions on patch than on continuous reefs (t 4.88, df 61, p.001). Standard habitat units SHUs were arrayed such that they were 0.5 m or 1 m apart, and this closely mimicked nearest neighbor distances in patch and continuous reefs, respectively (Figure 1). Our behavioral observations of transplanted three-spot damselfish on SHUs also resembled our observations in natural habitat with clear differences in behavior between fish on SHUs separated by 0.5 m and 1 m (MANOVA, Pillai trace 0.24, F 6.623, df 2,42, p.003). Fish tended to forage at a higher rate on SHUs separated by 1 m than on SHUs 0.5 m apart, although this was not significant at an of 0.05 (T 1.92, p.06; Figure 3). Damselfish on SHUs separated by 0.5 m were involved in nearly double the agonistic interactions as those on SHUs 1.0 m apart (one-tailed t test, df 43, T 2.94, p.001). Effects of habitat on growth and mortality In natural habitat we observed a strong effect of habitat type on growth rate (Figure 4; ANCOVA, F 1, , p.001), with fish on continuous reef growing more quickly than those on patch reefs. Initial size of the fish also affected the change in SL per day (Figure 4; ANCOVA, F 1, , p.001). On SHUs, we were able to unambiguously identify eight fish on SHUs separated by 0.5 m and nine fish on SHUs separated by 1.0 m. Daily percent growth of fish on SHUs separated by 1.0 m averaged 0.60%, and this was significantly greater than the 0.03% daily growth we observed on SHUs separated by 0.5 m (F 1, , p.05). We did not detect a difference in mortality rates between continuous and patch reefs (Fisher s Exact test, p.816). Fifty-two fish survived on patch reefs to the first census, while 46 fish survived on continuous reefs. Of these survivors, 76% were recovered on patch reefs and 73.9% on continuous habitats at the end of the experiment. DISCUSSION Species interactions have been the traditional domain of population and community ecologists. However, it is clear that aspects of individual behavior underlie such interactions and may thus have important ecological consequences (Real, 1992). In this study, we examined how habitat structure affected patterns of fish dispersion, how fish behavior was influenced by habitat-induced differences in aggregation, and how growth and mortality rates differed as a function of these behavioral differences. Juvenile three-spot damselfish occupy home ranges 1 m 2 on coral and do not stray far from the core of their home range (Itzkowitz, 1977). As a result, the dispersion of juvenile three-spot damselfish is closely tied to Figure 3 Mean number of bites at food or agonistic encounters on standardized habitat units separated by 0.5 or 1 m by Stegastes planifrons. ***p.001. Bars are 1 SE.

5 Levin et al. Linking individual behavior with demography 569 Figure 4 Change in the length of Stegastes planifrons plotted against their length at the beginning of the study on both continuous and patch reefs (n 24 on continuous reefs and 23 on patch reefs). Statistical results are given in the text. the patch structure of the reef, and density of juvenile damselfish was higher on patch reef than on continuous reef habitat (nearest neighbor distances were shorter on patch than on continuous reef). The higher aggregation of fish on patch versus continuous reef appears to have resulted in a greater number of agonistic interactions on patch reef than on continuous habitat. The increased time spent on aggression on patch reefs apparently occurred at the expense of foraging, as fish on patch reefs spent less time foraging than their counterparts on continuous reefs. The elevated rates of aggression and reduced rates of foraging on patch versus continuous reef habitat were associated with a decrease in growth rates of fish on patch reefs, although survivorship did not differ between the two habitats. Reduced growth rates have a strong potential to feed back to population dynamics in fishes. When food or access to food is limited, growth rates of fish tend to be low, and mortality rates tend to be high and negatively size selective (reviewed by Sogard, 1997). Houde (1987) termed this the stage duration hypothesis. Reduction in juvenile growth rate is coupled with increased mortality rates because fish remain in vulnerable size classes for longer periods of time. Although we were unable to detect differences in mortality rates between patch and continuous reef habitats with short-term monitoring, such differences may have become apparent had we sampled longer. Indeed, such effects are common in fishes (e.g., Blom et al., 1994; Holtby et al., 1990; Levin et al., 1997; Post and Prankevicius, 1987). Patch and continuous reef habitats vary in many aspects other than the dispersion of coral habitat for juvenile threespot damselfish. At our study site, patch reefs occurred in deeper water (4 5 m) than the continuous back reef (1.5 2 m). Thus, light levels, flow regime, flux of planktonic food, species and densities of potential competitors, species of corals, and other factors may have differed between the two habitats. However, when we experimentally created standard habitats in a single location that varied only in the distance between habitat patches (which reflected the nearest neighbor distance in the two natural habitats), our results were similar to those from natural habitat. On SHUs separated by 0.5 m (average nearest neighbor distance on patch reefs), the number of agonistic interactions was greater, while foraging and growth rates were lower than on SHUs separated by 1.0 m (average nearest neighbor distance on continuous reef). Thus, it is likely that differences in behavior and growth between the two natural habitats were largely the result of differences in patch structure. Resource levels clearly affect foraging rates; however, the similarity of SHU results that were conducted in Jamaica to those of St. Croix strengthens the argument that the spatial patterning of the habitat is important. IFD and IDD models provide a framework for linking behavior to population processes. They are clearly useful when evaluating reef fishes, but there are problems with the application of both models to such species. Both distributions assume that animals can correctly assess the suitability of a patch. The IFD also assumes that new settlers are free to enter a patch (Fretwell, 1972). The territoriality and high rates of aggression displayed by three-spot damselfish suggest that new settlers may not be free to enter a patch, indicating that an IDD may be more appropriate. However, even though threespot damselfish are highly territorial and aggressive, the IDD may not be appropriate for settlement of juvenile fishes. Because settlement generally occurs at night when diurnally active residents, including three-spot damselfish, are inactive, residents may not have the opportunity to prevent settlement into the patch (e.g., Doherty, 1983; Jones, 1984; Tolimieri, 1995; but see Sweatman, 1985) Moreover, most workers have failed to detect postsettlement movement for coral reef fish, especially in damselfish (Doherty, 1983; Forrester, 1990, 1995; Jones, 1987a,b, 1988, 1990; Tolimieri, 1995), suggesting that these new settlers may not be forced out by residents after settlement has occurred. IFD models predict that fish should leave patch reefs where interference is high for other habitats where the density of potential competitors relative to available food resources is lower. However, juvenile three-spot damselfish remained on patch reefs despite experiencing lower growth rates than those on continuous reef. Higher than predicted use of poor patches has been observed in number of different taxa (Kohlmann and Risenhoover, 1997; Messier et al., 1990; Tregenza et al., 1996). There are several reasons to explain why juvenile three-spots overused patch reef habitat, and these fall into a number of traditionally proposed categories: (1) inability to correctly assess patches, (2) high cost of movement among patches, (3) factors related to perceptual ability or encounter rate, and (4) unquantified costs or benefits, which in our study would most likely be early, postsettlement mortality or survivorship over a longer period than the duration of our experiments. A likely explanation for the patterns we observed combines points one and two. Settling individuals may not be capable of correctly (or completely) assessing patch quality in terms of conspecific density, and the costs of postsettlement movement may be high enough to prevent redistribution of juveniles after settlement. Many reef fishes respond to the presence of conspecifics presumably because the presence of conspecifics indicates high-quality habitat (Booth, 1992; Sweatman, 1985; Tolimieri, 1998); however, settling three-spot damselfish do not appear to respond to conspecifics (Tolimieri, 1995). Even when fish respond to conspecifics, settlers may still have only partial information on the quality of the patch. Settlement occurs at night when most diurnal residents have retreated into the reef and are inactive. Although settlers may be able to use olfactory cues to detect conspecifics (Sweatman, 1988), this may only provide them with information on presence or absence of conspecifics, not density. Once fish settle, patch movement, especially in damselfish, is minimal (Doherty, 1983; Forrester, 1990, 1995; Jones, 1987a,b,

6 570 Behavioral Ecology Vol. 11 No , 1990; Tolimieri, 1995). In the present study, we recorded no cases of juvenile three-spots moving among patches, although they are known to move to different substrata upon reaching maturity (Williams, 1978). Lack of movement after settlement alone should not exclude IFD because fish are free to choose among patches during settlement. However, the inability to completely assess patch quality at the time of settlement in concert with lack of movement among patches after settlement may produce the deviation from predictions of both IFD and IDD models that we observed. The ability of individuals to perceive patches may also affect distribution. Small, dispersed patches will be encountered more often than less numerous large ones (e.g., Levin, 1993). Many ecological studies have found that rates of patch colonization are higher in small than in larger patches (Bell et al., 1987; Eggleston et al., 1998, 1999; Keough, 1984; McNeil and Fairweather, 1993; Paine and Levin, 1981; Sogard, 1989; Sousa, 1984). Thus, three-spot damselfish may settle in high densities on patch reefs simply because these habitats are more easily detected. In an experiment similar to the one here, Levin (1993) found higher settlement of a temperate wrasse to patchily distributed artificial habitat units than to clumped ones. His results are relevant here because mortality rates of these recently settled fish differed such that mortality was higher on the preferred settlement patch. The action of factors that we were unable to measure could affect both our choice between the IFD and IDD and the fit of our data to the appropriate model. For example early postsettlement predation may have been important. Many IFD and IDD models, as well as empirical studies examining the predictions of these models, ignore habitat differences in predation ostensibly because predation on adult birds, the subject of many of these studies, is rare (Houston and McNamara, 1997). However, even when predation is rare, it can have significant effects on individual behavior (Abrams, 1993; Houston et al., 1993; Houston and MacNamara, 1997). Although differences in predation rates among varying habitats are well known in fishes (Beukers and Jones, 1997; Hixon, 1991; Werner and Gilliam, 1984), we did not detect a difference in mortality rates between patch and continuous reef habitats. Juvenile three-spot damselfish recruit to reefs when they are about 10.5 mm, and the fish we observed ranged from 15 to 45 mm. Because predation on newly settled fish is often size dependent (Levin et al., 1997; Sogard, 1997), it is possible that predators affected fish smaller than those we used in this study. Although predation rates are often higher at habitat margins, continuous back reefs, with their diversity of habitats, may harbor a more diverse and thus more effective suite of a predators than patch reefs (Hixon and Beets, 1993; Hixon and Carr, 1997). For example, Connell (1996) reported that mortality rates of Acanthochromis polycanthus were higher on continuous reef than on patch reef, and this difference was associated with the distribution of large predators. Consequently, the apparent preference for lower quality patches by three-spot damselfish may be incorrect, and they may actually follow IFD or IDD predictions. Regardless of why the patterns we observed deviated from basic IFD and IDD predictions, our results suggest strong linkages between habitat, behavior, and growth rate. Patches used by juvenile three-spot damselfish varied in their spatial distribution and dispersion. This habitat-level pattern was associated with higher levels of aggression and lower feeding rates in patchy habitat, and this was correlated with a decrease in growth. These results illustrate that behavioral interactions are an integral part of population dynamics and that it is necessary to consider the spatial organization of the environment in both behavioral and ecological investigations. We thank K. Gestring, M. Ganger and students from Northeastern University s East/West program for diving assistance. R. Petrik, F. Michelli, D. Westneat, and R. Zabel provided critical comments on various drafts of this paper. Funding was provided by National Science Foundation (NSF) grants OCE to P.F.S. and OCE to P.S.L. and P.F.S. Supplemental support was provided by NSF grant DEB to P.S.L. and J. A. Coyer. This is contribution number 17 from PISCO, the Partnership for Interdisciplinary Studies of Coastal Oceans: A Long-Term Ecological Consortium, funded by the David and Lucile Packard Foundation. REFERENCES Abrams PA, Decreasing functional responses as a result of adaptive consumer behavior. Evol Ecol 3: Abrams PA, Ecological effects of the interaction of adaptive foraging behaviors in food webs. Am Nat 140: Abrams PA, Optimal traits when there are several costs: the interaction of mortality and energy costs in determining foraging behavior. Behav Ecol 4: Altman J, Observational study of behavior: sampling method. Behaviour 49: Anholt BR, An experimental separation of interference and exploitative competition in a larval damselfly. Ecology 76: Anholt BR, How should we test for the role of behaviour in population dynamics. Evol Ecol 11: Bell JD, Westoby M, Steffe AS, Fish larvae settling in seagrass beds of different leaf density? J Exp Mar Biol Ecol 111: Beukers JS, Jones JP, Habitat complexity modifies the impact of piscivores on a coral reef fish population. Oecologia 114: Blom GT, Svåsand T, Jøstad KE, Otterå H, Paulson OI, Holm JC, Comparative survival and growth of two strains of Atlantic cod (Gadus morhua) through the early life stages in a marine pond. Can J Fish Aquat Sci 51: Boccia ML, Landenslager M, Reite M, Food distribution, dominance and aggressive behavior in bonnet macaques. Am J Primatol 16: Booth DJ, Larval settlement patterns and preferences by domino damselfish Dascyllus albisella Gill. J Exp Mar Biol Ecol 155: Booth DJ, Wellington G, Settlement preferences in coral-reef fishes: effects on patterns of adult and juvenile distributions, individual fitness and population structure. Aust J Ecol 23: Brown JL, The evolution of behavior. Toronto: Norton. Chesson P, Rosenzweig M, Behavior, heterogeneity, and the dynamics of interacting species. Ecology 72: Connell SD, Variations in mortality of a coral-reef fish: links with predator abundance. Mar Biol 126: Doherty PJ, Tropical territorial damselfishes: is density limited by aggression or recruitment? Ecology 64: Dunbar RIM, Population consequence of social structure. In: Behavioural ecology: ecological consequences of adaptive behaviour (Sibly RM, Smith RH, eds). Oxford: Blackwell; Dye C, Competition among larval Aedes aegypti: the role of interference. Ecol Entomol 9: Eggleston DB, Elis WE, Etherington LL, Dahlgren CP, Posey MH, Organism responses to habitat fragmentation and diversity: habitat colonization by estuarine macrofauna. J Exp Mar Biol Ecol 236: Eggleston DB, Etherington LL, Elis WE, Organism response to habitat patchiness: species and habitat-dependent recruitment of decapod crustaceans. J Exp Mar Biol Ecol 223: Emery AR, Comparative ecology and functional osteology of fourteen species of damselfish (Pices: Pomacentridae) at Alligator Reef, Florida Keys. Bull Mar Sci 23: Ens BJ, Goss-Custard JD, Interference among oystercatchers, Haematopus ostralegus, feeding on mussels, Mytilus edulis, on the Exe estuary. J Anim Ecol 53: Forrester GF, Factors influencing the juvenile demography of a coral reef fish. Ecology 71: Forrester GE, Strong density-dependent survival and recruitment regulate the abundance of a coral reef fish. Oecologia 103: Fretwell SD, Populations in a seasonal environment. Princeton, New Jersey: Princeton University Press.

7 Levin et al. Linking individual behavior with demography 571 Fretwell SD, Lucas HL, On territorial behavior and other factors influencing habitat distribution in birds. Acta Biotheor 19: Fryxell JM, Lundberg P, Individual behavior and community dynamics. London: Chapman and Hall. Gersani M, Abramsky Z, Falik O, Density-dependent habitat selection in plants. Evol Ecol 12: Gilliam JF, Individual behavior and population dynamics (book review). Ecology 68: Goss-Custard JD, Sutherland WJ, Individual behaviour, populations and conservation. In: Behavioural ecology: an evolutionary approach (Krebs JR, Davies NB, eds). London: Blackwell Science; Hassell MP, May RM, From individual behaviour to population dynamics. In: Behavioural ecology (Sibly RM, Smith RH, eds). Oxford: Blackwell; Hixon MA, Predation as a process structuring coral reef fish communities. In: The ecology of fishes on coral reefs (Sale PF, ed). San Diego, California: Academic Press; Hixon MA, Beets JP, Predation, prey refuges, and the structure of coral-reef fish communities. Ecol Monogr 63: Hixon MA, Carr MH, Synergistic predation, density dependence, and population regulation in marine fish. Science 277: Holt RD, Optimal foraging and the form of the predator isocline. Am Nat 122: Holtby LN, Andersen BC, Kadowaku RK, Importance of smolt size and early ocean growth to interannual variability in marine survival of coho salmon (Oncorhynchus kisutch). Can J Fish Aquat Sci 47: Houde ED, Fish early life dynamics and recruitment variability. Am Fish Soc Symp 2: Houston AI, McNamara JM, Patch choice and population size. Evol Ecol 11: Houston AI, McNamara JM, Hutchinson JMC, General results concerning the trade-off between gaining energy and avoiding predation. Phil Trans R Soc Lond B 341: Hugie DM, Grand TC, Movement between patches, unequal competitors and the ideal free distribution. Evol Ecol 12:1 19. Itzkowitz M, Spatial organization of the Jamaican damselfish community. J Exp Mar Biol Ecol 28: Itzkowitz M, Makie D, Habitat structure and reproductive success in the beaugregory damselfish. J Exp Mar Biol Ecol 97: Ives AR, Dobson AP, Antipredator behavior and the population dynamics of simple predator prey systems. Am Nat 130: Jones GP, The influence of habitat and behavioural interactions on the local distribution of the wrasse, Pseudolabrus celidotus. Anim. Behav. 10: Jones GP, 1987a. Competitive interactions among adults and juveniles in a coral reef fish. Ecology 68: Jones GP, 1987b. Some interactions between residents and recruits in two coral reef fishes. J Exp Mar Biol Ecol 114: Jones GP, Experimental evaluation of the effects of habitat structure and competitive interactions on the juveniles of two coral reef fishes. J Exp Mar Biol Ecol 123: Jones GP, The importance of recruitment to the dynamics of a coral reef fish population. Ecology 71: Kacelnik A, Krebs JR, Bernstein C, The ideal free distribution and predator-prey populations. Trends Ecol Evol 7: Kaufman LS, The threespot damselfish: effects on benthic biota of Caribbean coral reefs. Proc Int Coral Reef Symp 3(1): Keough MJ, Effects of patch size on the abundance of sessile marine invertebrates. Ecology 65: Kohlmann SG, Risenhoover KL, White-tailed deer in a patchy environment: a test of the ideal-free-distribution theory. J Mammal 78: Kramer DL, Rangeley RW, Chapman LJ, Habitat selection: patterns of spatial distribution from behavioural decisions. In: Behavioural ecology of teleost fishes (Godin JJ, ed). Oxford: Oxford University Press; Levin PS, Habitat structure, conspecific presence and spatial variation in the recruitment of a temperate reef fish. Oecologia 94: Levin P, Petrik R, Malone J, Interactive effects of habitat selection, food supply and predation on recruitment of an estuarine fish. Oecologia 112: Malone JC, Forrester GE, Steele MA, Effects of subcutaneous microtags on the growth, survival, and vulnerability to predation of small reef fishes. J Exp Mar Biol Ecol 237: Mangel M, Clark CW, Dynamic modeling in behavioral ecology. Princeton, New Jersey: Princeton University Press. McNeil SE, Fairweather PG, Single large or several small marine reserves? An experimental approach with seagrass fauna. J Biogeogr 20: Messier F, Virgil JA, Marinelli L, Density-dependent habitat selection in muskrats: a test of the ideal free distribution model. Oecologia 84: Milinski M, Parker GA, Competition for resources. In: Behavioural ecology (Krebs, JR, Davies NB, eds). Oxford: Blackwell; Morris WF, Wiser SD, Klepetka B, Causes and consequences of spatial aggregation in the phytophagous beetle Altica tombacina. J Anim Ecol 61: Myrberg AA, Thresher RE, Interspecific aggression and its relevance to the concept of territoriality in reef fishes. Am Zool 14: Paine RT, Levin SA, Intertidal lanscapes: disturbances and the dynamics of pattern. Ecol Monogr 51: Post JR, Prankevicius AB, Size-selective mortality in young-ofthe-year yellow perch (Perca flavescens:) evidence from otolith microstructure. Can J Fish Aquat Sci 44: Randall JE, Food habits of the fishes of the West Indies. Stud Trop Oceanogr 5: Real LA, Introduction to the symposium. Am Nat 140:S1 S4. Robertson DR, Patterns of lunar settlement and early recruitment in Caribbean reef fishes at settlement. Mar Biol 114: Sale PF, Influence of corals in the dispersion of the pomacentrid fish, Dascyllus aruanus. Ecology 53: Sih A, The behavioral race between predators and prey. Am Nat 123: Smith RH, Sibly R, Behavioural ecology and population dynamics: towards a synthesis. In: Behavioural ecology: ecological consequences of adaptive behaviour (Sibly RM, Smith RH, eds). Oxford: Blackwell; Sogard SM, Colonization of artificial seagrass by fishes and decapod crustaceans importance of proximity to natural eelgrass. J Exp Mar Biol Ecol 133: Sogard CM, Size-selective mortality in the juvenile stage of teleost fishes: a review. Bull Mar Sci 60: Sousa WP, Intertidal mosaics: patch size, propagule availability, and spatially variable patterns in succession. Ecology 65: Sutherland WJ, From individual behaviour to population ecology. Oxford: Blackwell. Sweatman H, Field evidence that settling coral reef fish larvae detect resident fishes using dissolved chemical cues. J Exp Mar Biol Ecol 124: Sweatman HPA, The influence of adults of some coral reef fishes on larval recruitment. Ecol Monogr 55: Thresher RE, Field analysis of the territoriality of the threespot damselfish, Eupomacentrus planifrons (Pomacentridae). Copeia 1976: Tolimieri N, Effects of microhabitat characteristics on the settlement and recruitment of a coral reef fish at two spatial scales. Oecologia 102: Tolimieri N, Effects of substrata, resident conspecifics and damselfish on the settlement and recruitment of the stoplight parrotfish, Sparisoma viride. Environ Biol Fish 53: Tregenza T, Common misconceptions in applying the ideal free distribution. Anim Behav 47: Tregenza T, Thompson DJ, Parker GA, Interference and the ideal free distribution: oviposition in a parasitoid wasp. Behav Ecol 7: Werner EE, Gilliam JF, The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst 15: Wilkinson L, Blank G, Gruber C, Desktop data analysis with SYSTAT. Upper Saddle River, New Jersey: Prentice Hall. Williams AH, Ecology of threespot damselfish: social organization, age structure, and population stability. J Exp Mar Biol Ecol 34: Wilson EO, Sociobiology. Cambridge: Harvard University Press.