Does increased habitat complexity reduce predation and competition in coral reef fish assemblages?

Transcription

1 OIKOS 106: 275/284, 2004 Does increased habitat complexity reduce predation and competition in coral reef fish assemblages? Glenn R. Almany Almany, G. R Does increased habitat complexity reduce predation and competition in coral reef fish assemblages?. / Oikos 106: 275/284. Greater habitat complexity is often associated with a greater abundance and diversity of organisms. High complexity habitats may reduce predation and competition, thereby allowing more individuals to occupy a given area. Using 16 spatially isolated reefs in the Bahamas, I tested whether increased habitat complexity reduced the negative effects of resident predators and competitors on recruitment and survival of a common damselfish. Two levels of habitat complexity were cross-factored with the presence or absence of two guilds of resident fishes: predators (sea basses and moray eels) and interference competitors (large territorial damselfishes). I monitored subsequent recruitment and recruit mortality for 60 days. Residents had strong negative effects on recruitment regardless of habitat complexity. In the presence of residents, recruits suffered high mortality immediately after settlement that was similar on low and high complexity reefs, although high complexity reduced mortality of recruits that survived this early postsettlement period. Comparisons between shelter hole diameters and the sizes of residents suggest that territorial damselfishes and small resident predators could access most shelter holes, whereas large resident predators were excluded from many shelter holes. This study demonstrates that whether habitat complexity reduces predation and competition may depend on several key factors, such as the availability of appropriate shelter, behavioral attributes of interactors, and developmental stage of prey/inferior competitors. G. R. Almany, Dept of Zoology, Oregon State Univ., Corvallis, OR , USA. Present address: School of Marine Biology and Aquaculture, James Cook Univ., Townsville QLD 4811, Australia (glenn.almany@jcu.edu.au). Habitats with high structural complexity typically support more species and individuals than nearby less complex habitats (Bell et al. 1991). One mechanism proposed to explain this general pattern is that high structural complexity reduces competition and predation (Holt 1987, Hixon and Menge 1991). For example, complex habitats may reduce competition when they provide more competitive refuges or a greater spectrum of discrete resources (e.g. food and shelter) and microhabitats, thereby allowing for enhanced niche partitioning (MacArthur and Levins 1964). Although these mechanisms have typically been proposed to explain positive relationships between local species diversity and habitat complexity (Schoener 1968, Emmons 1980), an implicit prediction is that abundance, pooled across species, will also be greater in high complexity habitats. Similarly, complex habitats may reduce predation by providing more prey refuges and/or reducing encounter rates between predators and prey (Murdoch and Oaten 1975). Predation risk is often lower in complex habitats for a wide range of taxa (Schneider 1984, Dickman 1992, Babbitt and Tanner 1998). Prey often increase their use of high complexity habitats as refugia in the presence of predators (Holbrook and Schmitt 1988, Sih et al. 1992), and predators may be less efficient foragers in high complexity habitats (Greenberg et al. 1995, Beukers and Jones 1997). Despite the potential importance of habitat complexity in mediating biotic interactions, few studies Accepted 23 December 2003 Copyright # OIKOS 2004 ISSN OIKOS 106:2 (2004) 275

2 have experimentally examined the combined impacts of habitat complexity, predation and competition on local assemblages. Coral reefs are structurally heterogeneous environments consisting of many microhabitats, which vary in their complexity depending on coral architecture (Jones and Syms 1998). Several studies of coral reef fishes have suggested that habitat complexity is a major determinant of abundance. For example, abundance is often greater in high complexity habitats (Hixon and Beets 1993, McCormick 1994), positively related to the number of potential shelter sites (Roberts and Ormond 1987, Friedlander and Parrish 1998), and the availability of suitably-sized shelter can influence both the abundance and size distribution of fishes (Hixon and Beets 1989). Furthermore, reef fish are known to compete for shelter (Munday et al. 2001, Holbrook and Schmitt 2002). These patterns illustrate the potential importance of habitat complexity in coral reef fish communities, although most studies have not identified causative mechanisms. Relationships between habitat complexity and abundance could also arise from several processes. For example, positive relationships between the abundance of newly settled fishes (recruits) and habitat complexity (Tolimieri 1995, Caselle and Warner 1996) could be caused by larvae selecting specific microhabitats as settlement sites, although the unequivocal demonstration of active habitat selection by settling larvae is rare (Elliot et al. 1995, Danilowicz 1996). Relationships between habitat complexity and recruit abundance could also arise from postsettlement movement (Frederick 1997, Lewis 1997) and when recruit mortality is influenced by habitat complexity (Jones 1988). Because experimentally separating the effects of these various processes has been difficult, we currently know little about the underlying causes of relationships between abundance and habitat complexity. Patterns of abundance can also be influenced by predation and competition in ways that are independent of habitat complexity. For example, the presence of sedentary reef-associated (resident) predators typically results in lower recruit abundance of most species, presumably because newly settled fishes are especially vulnerable to predation (Webster 2002, Almany 2003). Furthermore, predation by widely-ranging non-resident (transient) predators, such as jacks and snappers, can reduce recruit abundance (Hixon and Carr 1997). Prior residency by interference competitors, such as territorial damselfishes, can result in both positive and negative effects on recruit abundance. For example, damselfishes have been shown to either depress (Shulman et al. 1983, Jones 1987, Almany 2003) or enhance (Almany 2003) heterospecific recruit abundance, and either depress (Sale 1976, Almany 2003) or enhance (Jones 1987, Booth 1992) conspecific recruit abundance. However, the extent to which predation and competition are influenced by habitat complexity is not well understood. In the only previous study to manipulate both predation and habitat complexity, Beukers and Jones (1997) found that juvenile damselfishes suffered lower mortality on high complexity coral. In a previous study, I demonstrated that prior residency by predators and territorial damselfishes negatively affected subsequent damselfish recruitment, and that effects were due to direct interactions between recruits and residents rather than differential settlement (Almany 2003). In the present study, conducted in the same system, I tested whether effects of predators and damselfishes differed on reefs of relatively low and high habitat complexity and explored underlying mechanisms. I predicted that (1) recruitment would be greatest on high complexity reefs free of predators and damselfishes and lowest on low complexity reefs where these fishes were present, (2) where predators and damselfishes were present, recruitment would be greater on high complexity reefs, and (3) where predators and damselfishes were present, recruit mortality would be greater on low complexity reefs. Methods Study site This study was conducted near the Caribbean Marine Research Center at Lee Stocking Island, Bahamas (Fig. 1A). I utilized a matrix of live-coral patch reefs that were translocated to a large sand/seagrass flat on the leeward side of Norman s Pond Cay between 1991 and 1994 (Carr and Hixon 1995). The matrix included 32 reefs in five rows, and water depth varied between 2 and 5 m. Reefs were separated by 200 m of sand and seagrass, and the closest naturally occurring reef was /1 km from the edge of the matrix (Fig. 1B). Prior to habitat manipulations, each reef consisted of 9 /13 coral heads (mean/ 10.8, SD/1.5) of primarily three species: Montastrea annularis (Ellis & Solander), Porites asteroids (Pallas) and Siderastrea siderea (Ellis & Solander). Each reef had a surface area of 6.6 m 2 (SD/1.0 m 2 ) and height of 0.5 m (SD/0.07 m). A tagging study demonstrated that resident fishes seldom moved between reefs, although transient predators, such as jacks (Caranx spp.), snappers (Lutjanus spp.) and barracuda (Sphyraena barracuda Walbaum) did so (M. A. Hixon, pers. comm.). I assumed that each newly settled recruit arrived via natural settlement, and that the disappearance of a recruit was due to mortality rather than postsettlement movement for two reasons: (1) there is no evidence that newly settled recruits re-enter the plankton after their first day on the reef (Kaufman et al. 1992, Holbrook and Schmitt 1997) and (2) small reef fishes rarely move 276 OIKOS 106:2 (2004)

3 Fig. 1. Study site. (A) Position of translocated patch reefs with respect to nearby islands. (B) Spatial arrangement of reefs and the blocking scheme of live-coral reefs used in both experiments. Reefs were separated by 200 meters of sand and seagrass. between reefs separated by as little as 30 meters (Doherty 1982, Hixon and Beets 1989). Study species I tested whether increased habitat complexity reduced negative effects of residents on recruitment and mortality of the beaugregory damselfish (Stegastes leucostictus Müller & Troschel). The beaugregory is found throughout the western Atlantic from Brazil to the southern United States (Allen 1991) and is the most abundant damselfish on the shallow (B/6 m) reefs surrounding Lee Stocking Island (pers. obs.). After approximately one month of pelagic development (Robertson et al. 1993), larvae settle to and occupy a wide range of benthic microhabitats, including live and dead coral, coral rubble, sponges, mangrove roots, and empty mollusk shells (Longley and Hilderbrand 1941, Emery 1973, Itzkowitz 1977). In both laboratory and field choice experiments, beaugregory recruits did not show a preference for particular coral species or coral morphology, and in the absence of resident predators in the field, growth and mortality was unrelated to microhabitat (B. A. Byrne, unpubl.). Juvenile beaugregory feed primarily on benthic invertebrates (Wellington 1992), and are consumed by both resident and transient predatory fishes (Emery 1973). Prior residents consisted of two guilds of fishes: predators and interference competitors. Resident predators had two defining characteristics: (1) a diet of ]/10% fishes by volume (Randall 1967) and (2) a strong tendency to retreat to the reef (as opposed to fleeing the reef) when approached by a diver. Resident predators consisted of seven species: four diurnally active sea basses (Cephalopholis cruentata Lacepède [graysby], C. fulva L. [coney], Epinephelus striatus Bloch [Nassau] and Serranus tigrinus Bloch [harlequin bass]), one nocturnally active sea bass (Rypticus bistrispinus Mitchill [freckled soapfish]), and two nocturnally active moray eels (Gymnothorax moringa Cuvier [spotted] and G. vicinus Castelnau [purplemouth]). Interference competitors consisted of adults of the study species, Stegastes leucostictus, and the bicolor damselfish, S. partitus (Poey). Both species defend exclusive-use, single-owner, general-purpose territories against conspecifics, congeners, and most other fishes (Itzkowitz 1977, Gronell 1980, Robertson 1996). Adult Stegastes leucostictus are omnivorous, consuming algae, detritus, polychaetes, and fish material, whereas adult S. partitus are primarily planktivorous (Randall 1967, Emery 1973). Experimental design To test whether habitat complexity modifies the negative effects of prior residents on recruitment and mortality of Stegastes leucostictus, I conducted an experiment on 16 of the 32 patch reefs during the 1999 summer settlement season. I selected the 16 reefs with the most similar fish communities prior to manipulations based on Cluster Analysis (Bray /Curtis distance and group average). I then randomly assigned reefs to one of two habitat complexity treatments, high or low. On the eight high complexity reefs, I replaced half of the existing coral heads with an equal volume of Agaricia tenuifolia (Dana), a highly-branched foliaceous coral. On the eight low complexity reefs, I replaced half of the existing coral heads with an equal volume of low complexity massive coral of the same three species originally present on reefs: M. annularis, P. asteroides and S. siderea. After habitat manipulations, I estimated each reef s volume as a cylinder. To obtain quantitative measures of complexity, I established two perpendicular, 1.5-cm wide transects across each reef. Along the length and directly under each transect, I measured: (1) topographic complexity, defined as the ratio between the length of a fine-link chain allowed to conform to coral topography along the transect and the straight-line length of the transect OIKOS 106:2 (2004) 277

4 (Risk 1972), (2) depth of each potential shelter hole, (3) diameter of each hole, and (4) number of holes (Roberts and Ormond 1987). I averaged data from the two transects to obtain a reef average for complexity measures 1/3, and estimated the total number of potential shelter holes on each reef by summing hole counts from the two transects. Forty days after habitat manipulations, I crossfactored habitat complexity treatments (high or low) with the presence and absence of predators and territorial damselfishes (both guilds present or both guilds absent). I selected four blocks of reefs, each block containing four reefs (two high complexity and two low complexity), using two criteria: (1) reefs within each block had similar fish communities prior to the start of the experiment, thereby minimizing potential confounding effects of variable species composition, and (2) reefs within each block were close to each other, thereby minimizing potential confounding effects of patchy larval supply (Fig. 1B). To meet the first criterion, I manipulated the community on each reef via selective removals such that the relative and total abundance of each species was similar among the 16 reefs. Within each block, high and low complexity reefs were randomly assigned to one of two resident fish treatments, creating four treatments (n/4 reefs each): (1) predators and damselfishes present, low habitat complexity; (2) predators and damselfishes absent, low habitat complexity; (3) predators and damselfishes present, high habitat complexity; and (4) predators and damselfishes absent, high habitat complexity. Low complexity reefs with predators and damselfishes had an average (SE) of 4.8 (0.6) predators and 3.0 (0.4) damselfishes, while high complexity reefs with predators and damselfishes had an average of 4.5 (0.3) predators and 3.8 (0.3) damselfishes. Predator and damselfish densities reflected those found in the matrix prior to manipulations. All fish manipulations were conducted using the fish anesthetic quinaldine, hand nets, and a BINCKE net (Anderson and Carr 1998). After removing any existing recruits, I monitored subsequent recruitment by conducting a visual census of each reef every three days for 60 days. New settlers, recruits observed for the first time, were identified by their incomplete pigmentation and small size. For each reef, recruit mortality over the 60 days was calculated as the number of disappearances (D) divided by the number of observed new settlers (ONS). Additionally, because many new settlers were probably consumed before they were initially recorded on the two treatments where predators and competitors were present, I assumed that the average number of new settlers observed on the two treatments where predators and competitors had been removed, the estimated number of settlers (ENS), also settled to the two treatments where predators and competitors were present, and re-calculated mortality for these two treatments as ((ENS/ONS/D)/ENS). At the experiment s conclusion, I estimated the total length (TL) of each resident predator and territorial damselfish. To determine whether recruits could use shelter holes to escape predation and/or interference competition, I assumed that a fish s body depth must be equal to or less than the diameter of a hole for the fish to enter that hole, and compared the frequency distribution of resident predator (excluding moray eels) and territorial damselfish body depth with that of hole diameter on low and high complexity reefs. I converted total length estimates to body depths using the average ratio of these two measures from five specimens of each predator and damselfish species. Variation (SE) in the ratio between total length and body depth for each species, expressed as a percentage of the mean, ranged between 0.5% and 1.8% for predators and 1.0% and 1.5% for damselfishes. Analyses I compared differences in reef volume, topographic complexity, hole depth, hole diameter, and number of potential shelter holes among high and low complexity reefs using two-sample t-tests. I compared differences in recruit abundance on the final day of the experiment and recruit mortality during the experiment among the four treatments with ANOVA. The full ANOVA model included the following terms: blocks (random effect), complexity, prior residents, complexity/prior residents, block/complexity, and block/prior residents (Sokal and Rohlf 1995). I found no evidence for significant block/complexity or block/prior residents interactions in either visual inspections of data or ANOVA F-tests. I have therefore reported P-values for these interactions from the full ANOVA model and based subsequent analyses on the reduced model (blocks (random effect), complexity, prior residents, and complexity/prior residents). When the complexity/prior residents interaction was significant (P5/0.05), I calculated a parameter estimate and 95% confidence interval (95% CI), derived from the linear model, for each fixed effect at each level of the other fixed effect (Ramsey and Schafer 1997). When the complexity/prior residents interaction was not significant (P/0.05), I analyzed the additive model (blocks (random effect), complexity, prior residents) to obtain estimates of the effect size and 95% confidence interval, derived from the linear model, for each fixed effect. To insure ANOVA assumptions had been met, I tested for variance homogeneity using Levene s F-test and normality by examining normal probability plots (Ramsey and Schafer 1997). 278 OIKOS 106:2 (2004)

5 Results In the following, treatments (n/4 reefs each) are abbreviated as: (L) /low habitat complexity, (H) / high habitat complexity, ( /) /predators and damselfishes removed, and (/) /predators and damselfishes present. The four treatments were L/, L/, H/, and H/. Recruit abundance I observed 174 newly settled Stegastes leucostictus over the 60 days. Recruitment was greatest on the two treatments where resident predators and territorial damselfishes had been removed (Fig. 2). In the full ANOVA model, there was no evidence for significant block/complexity (P/0.634) or block/prior residents (P/0.418) interactions. In the reduced ANOVA model, abundance was marginally influenced by habitat complexity, strongly influenced by prior residents, and there was no evidence for a complexity/prior residents interaction (Table 1A). Independent of habitat complexity, removing prior residents increased average abundance (9/95% CI) by 10.09/2.3 recruits per reef. Independent of prior residents, high habitat complexity increased recruit abundance by 2.39/2.3 recruits per reef. Summed across the four reefs in each treatment, the total number of new settlers observed on each treatment over the 60-day experiment was: L/ /77 new settlers, L/ /22 new settlers, H/ /62 new settlers and H/ /22 new settlers. Fig. 2. Differential effects of habitat complexity and prior residents on recruitment of beaugregory damselfish (Stegastes leucostictus). Relationship between recruitment (larval settlement minus mortality) and treatments (n/4 reefs each). Treatments consisted of habitat complexity (low or high) cross-factored with the presence (/residents) and absence (/residents) of resident predators and territorial damselfishes. Error bars are 9/1 SE. Recruit mortality In the full ANOVA model, there was no evidence for significant block/complexity (P/0.932) or block/ prior residents (P/0.774) interactions. In the reduced ANOVA model, there was a significant complexity/ prior residents interaction (Table 1B, Fig. 3A). Where prior residents were present, high habitat complexity reduced recruit mortality (9/95% CI) by 63%9/25%, while in the absence of prior residents, high habitat complexity reduced recruit mortality by 22%9/25%. On high complexity reefs, prior residents increased recruit mortality by 14%9/25%, and on low complexity reefs, prior residents increased recruit mortality by 55%9/25%. However, when per-treatment mortality was re-calculated by assuming that approximately 70 new settlers recruited to each treatment, there was no interactive effect of habitat complexity and prior residents (Fig. 3B, parallel lines indicate no interaction). Summed across the four reefs in each treatment, the number of mortalities observed on each treatment during the 60-day experiment was: L/ /33 mortalities, L/ /19 mortalities, H/ /10 mortalities and H/ /9 mortalities. Habitat complexity and fish body depth After habitat manipulations, reef volume was similar on low and high complexity reefs (t-test: t/0.93, P/0.370, mean [SE] reef volume: L/2.6 [0.1] m 3,H/2.8 [0.1] m 3 ). In contrast, low and high complexity reefs differed significantly in each measure of habitat complexity. High complexity reefs had greater topographic complexity (t-test: t/7.94, PB/0.0001, mean [SE] topographic complexity: L/1.50 [0.02], H/1.95 [0.05]). Potential shelter holes were more abundant on high complexity reefs (t-test: t/10.35, PB/0.0001, mean [SE] hole abundance: L/4.9 [1.0] holes, H/21.6 [1.3] holes), deeper on low complexity reefs (t-test: t/2.90, P/ 0.012; mean [SE] hole depth: L/12.2 [0.8] cm, H/ 9.3 [0.6] cm), and had smaller diameters on high complexity reefs (Fig. 4A, t-test: t/4.44, P/0.0006, mean [SE] hole diameter: L/6.5 [0.8] cm, H/2.8 [0.1] cm). Comparing frequency distributions of shelter hole diameter and resident fish body depth indicates small predators and territorial damselfishes could access most holes on both low and high complexity reefs (Fig. 4B, D), whereas large predators were excluded from many holes (Fig. 4C). Discussion Relationships between recruit abundance and habitat complexity could result from several processes, such as immigration, emigration, differential mortality, and in OIKOS 106:2 (2004) 279

6 Table 1. ANOVAs comparing Stegastes leucostictus recruit abundance on the last day of the experiment (day 60), and S. leucostictus recruit mortality observed during the experiment. Source df SS MS F P Levene s F- test P A) Recruit abundance Block Complexity Prior residents B/ Interaction Error B) Recruit mortality Block Complexity Prior residents Interaction Error Levene s F-test tests the assumption of equal variance among treatments. P/0.05 indicates this assumption has been met. species with bipartite life histories, habitat selection by dispersive larvae. In the present study, immigration and emigration were unlikely due to the spatial isolation of Fig. 3. Differential effects of habitat complexity and prior residents on mortality of beaugregory damselfish (Stegastes leucostictus) recruits over 60 days. Treatments (n/4 reefs each) consisted of habitat complexity (low or high) cross-factored with the presence (/residents) and absence (/residents) of resident predators and territorial damselfishes. (A) Observed mortality of recruits followed via censuses. (B) Observed mortality plus estimates of unobserved mortality (see Methods). Error bars are 9/1 SE. experimental reefs, and previous studies indicate that the focal species settles randomly with respect to microhabitat. I therefore focused on how habitat complexity influences interactions between newly settled recruits and residents that affect recruit survival. Factorial manipulation of habitat complexity and the presence of resident predators and territorial damselfishes resulted in uniformly high recruitment where residents had been removed regardless of habitat complexity, and where residents were present, recruitment was slightly greater on high complexity reefs. Prior residency by predators and damselfishes clearly had a stronger influence on recruitment than did habitat complexity. These results support the predictions that recruitment would be greatest on high complexity reefs free of resident predators and damselfishes, lowest on low complexity reefs with residents, and that in the presence of residents recruitment would be greatest on high complexity reefs. Recruitment differences among treatments were most likely caused by (1) differential recruit mortality and/or (2) differential larval settlement. Is there evidence for differential settlement? The number of new settlers observed during the 60-day study was approximately three times greater on reefs where resident predators and damselfishes had been removed compared to where they were present. This suggests that settling larvae may have selected reefs where residents had been removed as settlement sites. However, in a previous study in this system I demonstrated that beaugregory larvae do not select settlement sites based on the presence or absence of predators and damselfishes (Almany 2003). As a result, recruitment differences in the present study were more likely caused by differential recruit mortality. Such mortality must have been substantial between settlement and recruit censuses (up to 72 hours) to generate the three-fold difference in the number of new settlers among reefs with and without residents. This conclusion adds to the growing list of studies demonstrating that mortality is typically greatest shortly after settlement, 280 OIKOS 106:2 (2004)

7 Fig. 4. Frequency distributions of shelter hole diameter and body depth of resident predators and territorial damselfishes on high and low complexity reefs. (A) Shelter hole diameter on high complexity reefs (n/173 holes) and low complexity reefs (n/39 holes). (B) Body depth of small resident predators (n/ 24): Cephalopholis cruentata, C. fulva, Serranus tigrinus, and Rypticus bistrispinus. (C) Body depth of large resident predators (n/9): Epinephelus striatus. (D) Body depth of territorial damselfishes (n/ 25): Stegastes leucostictus and S. partitus. Note that y-axis scale varies among plots. and that such mortality can quickly obscure initial patterns of abundance generated by larval supply (Planes and Lecaillon 2001, Webster 2002, Webster and Almany 2002, Almany 2003). On reefs where predators and damselfishes were present, recruitment was only marginally greater on high complexity reefs. Why were negative effects of residents similar on low and high complexity reefs? Based on comparisons between hole diameter and the body depths of predators and damselfishes, only large resident predators (Epinephelus striatus) were excluded from most holes on high complexity reefs. In contrast, small resident predators and territorial damselfishes likely had access to most holes on both high and low complexity reefs. As a result, while recruits on high complexity reefs may have avoided interactions with E. striatus, recruits on both low and high complexity reefs were similarly exposed to small predators and damselfishes. If the weak positive effect of high complexity was due to recruits avoiding E. striatus, recruit mortality was clearly most strongly influenced by small predators and/ or damselfishes. Consistent with this conclusion, Holbrook and Schmitt (2002) found that damselfish recruits were five times more likely to fall prey to small predatory fishes than large predatory fishes. Besides its possible influence on interactions between residents and recruits, habitat complexity could affect interactions between recruits and widely ranging transient predators, which are important sources of recruit mortality in this system (Hixon and Carr 1997). Because high complexity reefs had a greater number of smalldiameter shelter holes, transient predators, which are typically 20/30 cm TL in this system (pers. obs.), were likely excluded from more shelter holes on high complexity reefs than on low complexity reefs. Thus, recruits may have suffered lower mortality from transient predators on high complexity reefs. Consistent with this hypothesis, where residents had been removed (i.e. where transient predators were the likely source of most recruit mortality) recruit mortality was greatest on low complexity reefs. Previous studies suggest that predator behavior may determine whether increased complexity reduces predation mortality. For example, increased complexity may actually improve the capture success and foraging efficiency of predators that employ ambush tactics by providing more sites from which predators attack (Janes 1985) and by decreasing the visibility of predators to prey (Coen et al. 1981). In contrast, predators that actively search for and pursue prey are often less efficient in high complexity habitats, presumably because increased complexity interferes with their ability to maneuver and/or visually detect prey (Flynn and Ritz 1999). Resident predators in the present study typically ambush prey, whereas transient predators actively pursue prey (pers. obs.). As a result, resident predators might have been unaffected by increased complexity, which could OIKOS 106:2 (2004) 281

8 explain the relatively weak influence of habitat complexity in this study. Where predators and damselfishes were present, observed recruit mortality was significantly lower on high complexity reefs. However, this conclusion is based on comparing mortality estimates that did not include mortality occurring between settlement and censuses, a period of as much as 72 hours. Estimating mortality during this period by assuming that approximately equal numbers of new settlers arrived to each of the four treatments indicates that where predators and damselfishes were present, approximately 70% of new settlers were consumed before censuses. Adding this estimate of unobserved mortality indicates that increased complexity did not significantly reduce recruit mortality. However, after some initial period of reef occupancy, recruit survival was clearly greater on high complexity reefs. Why might the positive effect of complexity increase with time on the reef? The frequent observation that recruit mortality is greatest immediately after settlement and quickly declines thereafter (review by Hixon and Webster 2002) suggests that recruits may acquire behaviors and/or physical capabilities (e.g. improved swimming and sensory systems) that have important consequences for mortality, perhaps because they allow recruits to more effectively utilize shelter. Additionally, recruits may need time to gain experience with predators. For example, mice that have been previously exposed to predators increase their use of complex habitats and experience lower predation mortality, whereas predator-naïve mice remain in the open and suffer higher mortality (Dickman 1992). In the only previous coral reef study to manipulate both predators and habitat complexity, Beukers and Jones (1997) found that transplanted damselfish recruits suffered lower mortality on high complexity corals. Three important differences between their study and the present study may have led to contrasting conclusions. First, Beukers and Jones (1997) only manipulated predators, whereas in the present study predators occurred with territorial damselfishes. Evidence suggests that aggressive interactions between damselfishes and recruits make recruits more susceptible to predation from both resident and transient predators (Carr et al. 2002, Holbrook and Schmitt 2002, Almany 2003). Thus, the combined effects of predators and damselfishes may have negated any positive effects of increased habitat complexity. Second, Beukers and Jones (1997) transplanted recruits that had been on the reef for one or more days, whereas in the present study recruits settled naturally to reefs. Early recruit mortality in the present study was not influenced by habitat complexity, whereas in both studies mortality after some period on the reef was reduced by high complexity. Finally, the high complexity coral species used by Beukers and Jones (1997), Pocillopora damicornis (L.), is more finelybranched than the high complexity coral used in the present study (Agaricia tenuifolia, pers. obs.). Thus, P. damicornis may provide more refuge space that excludes predators than A. tenuifolia. This study suggests that whether habitat complexity reduces predation and competition likely depends on a variety of factors. First, relationships between shelter characteristics (e.g. hole diameter) and interactor size could determine whether individuals can use shelter to avoid negative interactions. Second, behavioral attributes of predators (e.g. ambush vs pursuit predation) or physical capabilities of prey (e.g. swimming ability) may influence whether and how interactors respond to habitat complexity. Finally, indirect effects resulting from multi-species interactions could obscure effects of habitat complexity. Further multifactor studies of how habitat complexity influences species interactions will improve our ability to predict how anthropogenic disturbance, which often reduces habitat complexity, is likely to impact communities. Such investigations are critical given the ongoing, worldwide degradation of coral reefs and other systems. Acknowledgements / I am grateful to Jeanine Almany, Karen Overholtzer, Denise Piechnik, and Michael Webster for assistance in the field. For logistical support, I thank the staff of the Caribbean Marine Research Center. Financial support was provided by an NSF Graduate Predoctoral Fellowship and International Research Fellowship, a Fulbright Postgraduate Award, Oregon State University Zoology Research funds, and NSF grants (OCE and OCE ) and NOAA- NURP grants (CMRC and CMRC ) to Mark Hixon. Reviews of this manuscript were provided by Peter Bayley, Mark Carr, Mark Hixon, Geoff Jones, Bruce Menge, Philip Munday, Karen Overholtzer, Susan Sogard, and Michael Webster. References Allen, G. R Damselfishes of the world. / Mergus. Almany, G. R Priority effects in coral reef fish communities. / Ecology 84: 1920/1935. Anderson, T. W. and Carr, M. H Bincke: a highly efficient net for collecting reef fishes. / Environ. Biol. Fish. 51: 111/ 115. Babbitt, K. J. and Tanner, G. W Effects of cover and predator size on survival and development of Rana utricularia tadpoles. / Oecologia 114: 258/262. Bell, S. S., McCoy, E. D. and Mushinsky, H. R. (eds) Habitat structure: the physical arrangement of objects in space. / Chapman and Hall. Beukers, J. S. and Jones, G. P Habitat complexity modifies the impact of piscivores on a coral reef fish population. / Oecologia 114: 50/59. Booth, D. J Larval settlement patterns and preferences by domino damselfish Dascyllus albisella Gill. / J. Exp. Mar. 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