Abstract
Fish schooling provides individuals with potential benefits such as predator avoidance, increased foraging efficiency and access to food resources. We tested whether schooling affects foraging rates of adult and juvenile Ocean Surgeonfish in Grape Tree Bay on Little Cayman Island. We hypothesized that 1) individual feeding rates would be greater in heterospecific than conspecific groups, and 2) individual feeding rates would be greater in groups than alone. Juveniles foraged mostly in heterospecific groups while adults foraged mostly alone. Juveniles fed significantly faster in heterospecific groups than with conspecifics or alone, in contrast to adults, whose feeding rates did not change when individuals associated with either con- or heterospecifics. The number of Ocean Surgeonfish did not differ between conspecific (same species) and heterospecific (mixed species) groups, but heterospecific groups were always larger. Thus, we could not determine whether the benefits of heterospecific associations were a function of individual behavior influenced by species composition, or group size. Large, heterospecific groups may reduce predation risk in addition to increasing foraging rates, leading to the prediction that juveniles should associate with heterospecific groups whenever possible.

Introduction
Mixed-species schooling is common in herbivorous coral reef-fish. Potential benefits include predator avoidance, increased foraging efficiency, and improved access to food resources (1, 2). In many species, individuals have different schooling behavior and diet preferences at different lifestages (3).

Ocean Surgeonfish (Acanthurus bahianus) is a generalist herbivore that lives individually, in mixed-species groups, and (during adulthood) in conspecific groups (4). We evaluated the effects of schooling and lifestage on feeding rate of Ocean Surgeonfish in the back reef of Grape Tree Bay on Little Cayman Island. Con- and heterospecific schooling may allow individuals to spend more time foraging and less time being viligant due to improved predator detection (1). If so, the feeding rate of individuals in groups would be higher than that of solitary foragers. Alternatively, schooling could increase competition among individuals, leading to decreased feeding rate, which would favor solitary foraging. Competition may also be higher among conspecifics than among heterospecifics, leading to a lower feeding rate of individuals in conspecific groups than those in heterospecific groups.

As diet, habitat and behavior changes with lifestage (5), adult Ocean Surgeonfish may school less often than juveniles. Damselfish defend patches of algal garden in their territories and limit access of other herbivorous fish (4). Overcoming damselfish territoriality may be more difficult for solitary juveniles than juveniles in foraging groups or solitary adults, favoring schooling in juveniles. Predator-vigilance could be more important for juveniles than adults, which also favors schooling behavior (6).

We investigated the effects of schooling on foraging rates of adult and juvenile Ocean Surgeonfish, predicting that 1) individual feeding rates would be greater in hetereospecific than conspecific groups, and 2) individual feeing rates would be greater in groups than alone.

Methods
We measured feeding rates of adult and juvenile Ocean Surgeonfish on February 29 and March 1-2, 2008 along a 400 m stretch of the back reef in Grape Tree Bay, near Little Cayman Research Center. Each morning and afternoon, we haphazardly sampled Ocean Surgeonfish by snorkeling over the reef until an actively traveling or feeding individual was located 1-10 m from the reef crest. We observed one focal fish per group encountered. We categorized individuals of 10-13 cm in length as adults, 4-6 cm as juveniles, and ignored fish outside these size classes.

After habituating fish to our presence for approximately 1 minute, we counted the number of bites made by the focal fish for up to 5 minutes, and calculated bite rate (bites min-1). We recorded schooling behavior (solitary, conspecific, or heterospecific groups), group size, species composition, and whether foraging during each observation period occurred in damselfish territory. We ended an observation period before five minutes elapsed if the individual changed group association, began non-foraging activities (such as hiding or visiting a cleaning station), or swam out of sight. For analysis, we retained all observations longer than 30 s.

We equalized variances with a log10 transformation of bite rate and ran two-way ANOVAs for the effects of grouping and damselfish territory on feeding rates, for both adults and juveniles. We did not include interactions between the two factors because we had no a priori hypotheses about the effect of damselfish territory on grouping. We were also unable to include the interaction term in the model since we observed no solitary juveniles feeding in damselfish territories.
We tested for the specific hypothesized differences in feeding rate using linear contrasts. We compared feeding rates of solitary individuals and individuals in heterospecific and conspecific groups (μH + μC – μS = 0), and of individuals in heterospecific and conspecific groups (μH + μC = 0).

Results
We observed a total of 38 adult and 48 juvenile Ocean Surgeonfish over the period of three days. Fourteen focal adults and 36 juveniles foraged in groups. On average, conspecific groups contained 2.12 ± 0.08 fish (mean ± SE), while heterospecific groups contained 6.88 ± 0.52 fish. Of the 20 fish species observed foraging with Ocean Surgeonfish in heterospecific groups, juvenile Blueheaded Wrasse, juvenile Striped Parrotfish, and adult Striped Parrotfish were the most common (Table 1).
Schooling behavior affected feeding rate of juveniles and adults differently (Table 2, Figure 1).

Feeding rate of individuals in con- and heterospecific groups differed for juveniles (linear contrast F1,44 = 10.11, p < 0.01) but not adults (linear contrast F1,33 = 1.33, p = 0.23). When combined, feeding rates of individuals in conspecific and heterospecific groups did not differ from those of solitary foragers, for either adults (linear contrast F1,33 = 1.17, p = 0.29) or juveniles (linear contrast F1,44 = 2.64, p = 0.11). Juveniles in heterospecific groups fed the fastest (Figure 1).

Feeding rate of adults and juveniles did not differ significantly (t = 0.74, df = 85, p = 0.46). Feeding rates also did not differ in and out of damselfish territories for adults or juveniles (Table 2). Although neither adults nor juveniles foraged extensively in damselfish territory, adults and juveniles did spend similar percentages of foraging time in damselfish territories (22.9% and 16.2% of observations respectively; Pearson’s χ2 = 0.59, p = 0.44). Adults, which mainly fed alone (57.9%), differed from juveniles, which fed mostly in heterospecific groups (59.2%; Pearson’s χ2 = 15.75, p = 0.0004). Although heterospecific groups were over three times larger on average than conspecific groups (F = 80.43, df = 1, p < 0.0001), the mean number of Ocean Surgeonfish in conspecific (mean ± SE, 2.7 ± 0.27) and heterospecific groups (2.1 ± 0.21) did not differ (df = 1, 47, t = 3.14, p = 0.08).

Discussion
Adult feeding rate was unaffected by schooling behavior, whereas juveniles fed faster when associated with heterospecifics. Larger, mixed-species groups increase predator detection and allow individuals to spend more time foraging (1). If predator detection is more important for juveniles than adults, and juveniles can feed faster in heterospecific groups, juveniles should forage in groups whenever possible.

The significantly lower feeding rate of juveniles in conspecific versus heterospecific groups may be due to differences in behavior influenced by species composition of groups, or by group size. Since heterospecific groups were always larger than conspecific groups, we were unable to isolate the effect of group composition versus group size on feeding rate. Previous studies suggest that juvenile Ocean Surgeonfish avoid conspecifics in favor of mixed-species schools to minimize the cost of direct competition for food sources, while still benefiting from schooling (3, 7). We found no evidence of conspecific avoidance, as both conspecific and heterospecific groups contained the same number of Ocean Surgeonfish. Assuming intraspecific competition in con- and heterospecfic groups is equal, juveniles’ tendency to school in heterospecific groups must be explained by mechanisms other than competition avoidance (i.e. increased predator detection or improved foraging efficiency).

By estimating the proportion of damselfish territory in potential foraging areas, it would be possible to test whether Ocean Surgeonfish feed in damselfish territories more often than by chance alone (suggesting they do so to gain access to higher quality food), or less often than by chance (suggesting active avoidance).

Insights into how schooling affects individual behavior could be gained by measuring the time individuals spend schooling versus alone, and evaluating how the potential costs of schooling, such as within-group aggression and resource competition, differ between con- and heterospecific groups.

The benefits of heterospecific schooling for juvenile Ocean Surgeonfish seem clear and unequivocal. Literature on schooling behavior in fish focuses on two main components of fish fitness, feeding rate and predation risk. While there may be tradeoffs between these in some cases, no such tradeoffs are apparent here. Our findings indicate a substantial advantage in feeding rate. The extensive literature on how schooling reduces predation risk (1, 8) makes it implausible that predation risk would be increased by joining a large, heterospecific group, especially for these relatively small juveniles, who could be vulnerable to a wide range of predatory fish on the reef. Indeed, the benefits of reduced predation risk may contribute strongly to the feeding benefits of heterospecific group membership that we demonstrated. High juvenile feeding rates in these groups may be result of less time spent individually on predator vigilance. Further, large heterospecific groups may be able to forage in areas rich in resources but relatively exposed to predators.

In summary, our findings lead to the conclusion that juvenile Ocean Surgeonfish associate with heterospecific schools wherever possible, as this behavior allows for higher feeding rate. Juveniles that associate with smaller, conspecific groups, or forage alone, should have lower fitness, causing this behavior to be selected against. However, a tradeoff may exist between foraging rate and amount of nutrients ingested that may maintain a small population of juveniles that continue to forage alone.

Acknowledgements
The authors would like to thank David Peart for his guidance in forming the research questions, interpreting the data, and writing the report and Elizabeth Wolverich and Jeffrey Garner for their help in analyzing the data.

References
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