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Ecology, 64(6), 1983, pp. 1508-1513 <1983 by the Ecological Society of America PRIORITY EFFECTS IN THE RECRUITMENT OF JUVENILE CORAL REEF FISHES' MYRA J. SHULMAN2 Department of Zoology, University of Washington, Seattle, Washington 98195 USA JOHN C. OGDEN West Indies Laboratory, Teague Bay, St. Croix, United States Virgin Islands 00820 JOHN P. EBERSOLE Department of Biology, University of Massachusetts, Boston, Massachusetts 02125 USA WILLIAM N. MCFARLAND Section of Ecology and Systematics, Cornell University, Ithaca, New York 14853 USA STEVEN L. MILLER Department of Botany, University of Maine, Orono, Maine 04473 USA NANCY G. WOLF Section of Ecology and Systematics, Cornell University, Ithaca, New York 14853, USA Abstract. Competing models of community structure in assemblages of coral reef fishes have suggested that (1) these assemblages are structured by deterministic interactions between species, or between species and resources, or (2) the composition of these assemblages are determined by highly variable settlement from planktonic larvae. We examined interactions among newly recruited juvenile fishes and between juvenile fishes and transplanted resident damselfish on artificial reefs in St. Croix, United States Virgin Islands. Two kinds of priority effects occurred: (I) recruitment of three species of settling juveniles significantly decreased in the presence of the territorial damselfish, and (2) prior settlement of a juvenile predator lowered successful recruitment of two juvenile prey species. The first effect increases determinism in the structure of coral reef fish assemblages, while the second decreases their predictability. Key words: artificial reefs; Caribbean; community structure; competition; coral reeffish assemblages; interference competition; predation; recruitment. INTRODUCTION Priority effects, in which the presence of one species in a habitat decreases the probability of invasion by another, have been hypothesized as important in maintaining high regional species diversity and determining local species distributions (Levins and Culver 1971, Sutherland 1974, Connell and Slatyer 1977). One species can lower the juvenile recruitment of another in several possible ways. (I) Competition: adult and subadult residents or settling juveniles can actively interfere with juvenile settlement through aggression (interference competition) or passively influence settlement by altering or preempting resources (exploitative competition). (2) Predation: predatory subadult and adult residents can decrease recruitment directly, by preying on juveniles, or evolutionarily, by selecting for settlement in areas not occupied by predators. Similarly, predatory juveniles settling first can prevent subsequent successful recruitment by prey species. These I Manuscript received 3 November 1981; revised I September 1982' accepted 8 September 1982; final version received 15 October 1982. 2 Present address: Smithsonian Tropical Research Institute, APO Miami 34002. mechanisms are not mutually exclusive, and there are examples of at least two of them operating together (Sutherland 1974). The existence of priority effects among coral reef fishes would have significant implications for our understanding of the processes controlling these assemblages, a subject of much current controversy. The controversy centers on whether fish assemblages are structured by deterministic competitive and predatory interactions or by stochastic recruitment of juveniles into unpredictably available space (Sale 1977, 1980, Smith 1978, Gladfelter et al. 1980, Anderson et al. 1981, Ogden and Ebersole 1981). Priority effects between residents (adults and subadults) and juveniles, in which residents control which species recruit into the local habitat, suggest that assemblage composition is more deterministic. Juvenile-juvenile priority effects, in which order of settlement determines local species composition, suggest an unpredictable assemblage structure, strongly controlled by the vagaries of settlement of juveniles from the plankton. The importance of order of settlement in determining community structure has been shown for sessile organisms in experimental space-limited systems (Sutherland 1974, Sutherland and Karlson 1977) but has not yet been This content downloaded from 195.113.56.251 on Mon, 14 Apr 2014 18:21:02 PM All use subject to JSTOR Terms and Conditions December 1983 RECRUITMENT OF JUVENILE CORAL REEF FISHES documented for mobile species. In this study, we report the existence of two kinds of priority effects among coral reef fish assemblages, a system involving mobile species with strong behavioral interactions. 0 METHODS 0. C, The present study was conducted utilizing the facilities of the underwater habitat Hydrolab operated by the National Oceanographic and Atmospheric Administration on St. Croix, United States Virgin Islands. Hydrolab is located in Salt River Canyon, a 70100 m wide submarine canyon flanked by two coral reef walls. Thirty artificial reefs, each consisting of 11 concrete construction blocks placed in a pyramid two blocks wide and three blocks high, were built on the sand/seagrass (Halophila decipiens) floor of the canyon at depths of 16-20 m. Ten replicate reefs were constructed at each of three different times: 4 wk ("'old" reefs), 2 wk ("intermediate" reefs), and l/2 d (''young' reefs) prior to the start of the 7-13 July 1979 Hydrolab mission. The reefs were placed in a grid pattern, with a minimum distance of 5 m between them. Because of the small size and regular structure of these reefs, all fish species could be seen with relative ease. All the fishes on the artificial reefs were visually censused by two observers approximately twice weekly before the mission and several times daily during the mission. Weekly censuses were continued afterwards, until the artificial reefs were destroyed by Hurricanes David and Frederick in late August and early September 1979. RESU LTS Small artificial reefs, isolated by sand or seagrass from natural reefs, attract a fish fauna similar to that found on small isolated patch reefs (Talbot et al. 1978) and similarly situated reefs constructed from coral rubble (Shulman 1982). Compared to major reefs, all these small habitats show higher rates of successful recruitment by juveniles due to lower encounter rates with reef-associated predators and the increased shelter available from the seagrasses and algae surrounding the habitat (Shulman 1982). In addition, certain fishes, particularly those closely associated with particular coral habitats as adults, rarely recruit to isolated artificial reefs (Shulman 1982). A total of 44 species colonized the artificial reefs; 26 of these were found on at least five reefs (Table 1). The colonization curves (Fig. I) show that numbers of individuals and species increase monotonically to an apparent asymptote on young and intermediate reefs but peak early and then decrease on the old reefs. Each set of reefs was censused 12 d after construction. Using these 12-d censuses, comparisons among the three sets of reefs could be made that were independent of the amount of time the reefs were available for colonization. Grunts (Haemulidae) were excluded from analyses involving total numbers of recruits be- 1509 4)5 0 z 25 4) 20. / CL 0 5-a 7 JUN 22 JUN 7 JUL 22 JUL 6 AUG 21 AUG Date (1979) FIG. 1. Colonization curves of species and individuals (excludinggrunts)on the three sets of artificialreefs. Points represent means of all 10 reefs in each set. (O = old reefs; * = intermediatereefs; O = young reefs.) cause they far outnumbered all other species combined; analyses that included grunts would reflect only the trends in that family. There are significant differences among the three sets of reefs in both numbers of species and numbers of individuals (excluding grunts) recruited in the first 12 d after each set was built (ANOVA, P < .001). Young reefs were colonized by the fewest individuals and species, and old reefs by the most. This may represent a seasonal decrease in number of juvenile fish settling from the plankton (Munro et al. 1973), or it may be due to a dilution effect, there being only 10 reefs present to which fish could recruit during the 12 d following construction of the old reefs, but 20 d for the intermediate and 30 d for the young reefs. The reefs were censused intensively during the 6 d of the Hydrolab mission and censused again 6 d later. Because the intervals between these censuses were short, and therefore relatively few recruits could colonize and then disappear without being observed, the data from this period were used to examine net recruitment rates and interspecific effects on recruitment patterns. At any given time, reefs that had been in the water longer had higher resident fish populations (Fig. 1). During the period of intensive censusing, net recruitment rates (changes in number of individuals or species from one census to the next) to the three differentaged sets of reefs were compared. The youngest reefs, with the lowest resident populations, showed the high- This content downloaded from 195.113.56.251 on Mon, 14 Apr 2014 18:21:02 PM All use subject to JSTOR Terms and Conditions MYRA J. SHULMAN ET AL. 1510 TABLE 1. Species colonizingthe reefs. Number of reefs occupied by species Species 2 10 Gv mnothorax moringa (spotted moray) Clupeidae(herring) 7 3 8 8 I Svnodus intermedius (sand diver) Adiorvx coruscus (reef squirrelfish) Mvripristis jacobus (blackbar soldierfish) Diplectrum sp. Epinephelus guttatus (red hind) Serranus baldwini (lantern bass) Serranus tabacarius (tobaccofish) Serranus tigrinus (harlequinbass) Rvpticus subbifrenatus (spotted soapfish) Apogon binotatus (barred cardinalfish) Apogon maculatus (flamefish) Apogon townsendi (belted cardinalfish) Phaeoptyx conklini (freckled cardinalfish) Malacanthus plumieri (sand tilefish) Lutjanus buccanella (blackfin snapper) Lutjanus mahogoni (mahogany snapper) Ocv'urus chrvsurus (yellowtail snapper) Haemulon aurolineatum (tomtate) Haemulon flav~olineatum (frenchgrunt) Hoemulonmelanurum(cottonwick) 17 3 4 4 22 9 30 18 25 15 30 I Equetus lanceolatus (jackknife fish) Odontoscion dentex (reef croaker) Equetus acuminatus (high-hat) Pseudupeneus maculatus (spotted goatfish) Pomacanthus paru (french angelfish) Chaetodon sedentarius (reef butterflyfish) Chromis cyaneus (blue chromis) Eupomacentrus partitus (bicolor damselfish) Eupomacentrus v'ariabilis (cocoa damselfish) Halichoeres biv'ittatus (slippery dick) Thalassoma bifasciatum (bluehead wrasse) Callioni'mus bairdi (lancer dragonet) Corvphopterus glaucofraenum (bridled goby) Gnatholepis thompsoni (goldspot goby) Acanthurus bahianus (ocean surgeon) Acanthurus chirurgus (doctorfish) Acanthurus coeruleus (blue tang) Scorpaena plumieri (spotted scorpionfish) Bothus lunatus (peacock flounder) 3 10 1I 2 3 16 I 4 4 14 8 14 24 25 9 4 7 13 Balistidae I 24 1 Canthigaster rostrata (sharpnose puffer) Sphoeroides spengleri (bandtail puffer) est rate of net recruitment of individuals (excluding or including grunts) and species, with intermediate and old reefs having significantly lower net recruitment rates (ANOVA, P < .05). This difference is reflected in the colonization curves for both individuals and species, which appear to reach an asymptote after I mo (Fig. 1). There were also species-specific differences in net recruitment to different-aged reefs; grunts (Haemulidae), tobaccofish (Serranus tabacarius), cardinal fish (Apogonidae), and sharpnose puffers (Canthigaster rostrata) showed significantly higher net recruitment to young, relatively unoccupied reefs, while no such significant difference was found for mahogany snappers (Lutjanus inahogoni), blackfin snappers (Lutja- Ecology, Vol. 64, No. 6 nus buccanella), yellowtail snappers (Ocyurus chrysurus), high-hats (Equetus acuminatus), and surgeonfish (Acanthurus bahianus and A. chirurgus). These results may reflect differences between species in ability to settle and survive on occupied reefs, or important differences in recruitment strategies. To determine the effect of a resident on recruitment, one adult beaugregory (Eupomacentrus leucostictus), a territorial damselfish, was transplanted onto each of 5 of the 10 replicates for the three sets of reefs on 7 July 1979. Successful recruitment of surgeonfishes (Acanthurus bahianus and A. chirurgus) and reef butterflyfish (Chaetodon sedentarius) to reefs with beaugregories present was significantly lower relative to reefs that lacked beaugregories (Tables 2 and 3). The most common group of piscivorous fish recruiting to the reefs were snappers of the genus Lutjanus. Juveniles of two species were present (mahogany, L. mahogoni; blackfin, L. buccanella), the mahogany snapper being more abundant. These snappers were observed to prey on grunts and presumably attacked other small juvenile fishes. Grunts showed a nonrandom recruitment pattern relative to the presence or absence of Lutjanus during the first 12 d after the reefs were built. Reefs on which snappers were present showed a significant decrease (of 20%) in the numbers of grunts subsequently recruited, while reefs that lacked snappers recruited grunts in numbers slightly greater than expected (x2 test, P < .001). A similar result was obtained for the relationship between snappers and high-hats (Equetus acuminatus). High-hats only settled on "full-moon reefs" (see below); of these 20 reefs, 9 were colonized by highhats in the 12 d following construction. No juvenile snappers were present on those 9 reefs before or during the settlement of high-hats; 6 of the remaining II reefs were occupied by snappers, thus demonstrating a statistically significant effect of snapper presence on high-hat recruitment (binomial test, P < .05). The timing of recruitment of planktonic larvae is important if order of settlement affects species coexistence. Old reefs and young reefs were built within 3 d of full moons, and intermediate reefs within 3 d of a new moon. The recruitment data from the first 7 d after each set of reefs was built were used to determine lunar periodicity in settlement. The 7-d period represents recruitment during one-quarter of a lunar cycle. The numbers of fishes settling on old and young ("fullmoon") reefs were compared with those settling on intermediate ("new-moon") reefs (Table 4). The data, analyzed with the median test (P determined from Fisher's exact test) showed significantly higher recruitment of mahogany snappers and Diplectrum sp. to new-moon reefs as compared to full-moon reefs (P < .05). The data are suggestive for greater settlement on new-moon reefs by blackfin snappers, doctorfish, and sharpnose puffers (P < . 10). Only one species, the high-hat, showed significantly higher re- This content downloaded from 195.113.56.251 on Mon, 14 Apr 2014 18:21:02 PM All use subject to JSTOR Terms and Conditions December 1983 TABLE 2. RECRUITMENT OF JUVENILE CORAL REEF FISHES 1511 Effect of the presence of an adult beaugregory (Eupomacentrus leucostictus) on the recruitment of acanthurids. Number of reefs on which: Acanthurid settles and stays more than one census Beaugregory present Beaugregory absent No acanthurid stays more than one census Observed Expected Observed Expected 4.5* 14.0 7.4 11.1 7.5* 4.0 4.6 6.9 18.5 2 11.5 = 4.94; df = Number of reefs 12t 18 30 1;P < .05 * On one reef, an acanthurid was present before the beaugregory transplant and remained on the reef for more than two censuses. No more acanthurids arrived; the result therefore was split between the two categories. t Three of the 15 beaugregories transplanted onto the reefs disappeared in the first few days. cruitment to full-moon reefs (P < .05), settling only on those reefs. There is also very strong evidence that French grunts (Haemulon flaiolineatum) have semimonthly peaks in recruitment (W. N. McFarland, personal observation). DiSCUSSION Our study suggests that at least two kinds of priority effects exist in juvenile coral reef fish recruitment. The underlying mechanisms producing these two effects are very different, as are their implications for community structure. The presence of an adult resident (beaugregory) decreases the settlement of juveniles of three other species. This territorial damselfish is extremely aggressive, particularly towards potential trophic competitors and egg predators (Eggs are laid in territories of male beaugregories.) (Ebersole 1977). On our artificial reefs, the presence of the herbivorous beaugregories was associated with a significant decrease in successful recruitment of surgeonfishes, a family of herbivores. The presence of beaugregories was also correlated with lowered recruitment of reef butterflyfish, a member of a family known to include fish eggs in its diet (Birkeland and Neudecker 1981). The second kind of priority effect occurs between juvenile piscivores and their prey. The order of settlement is critical; if snappers settle on a reef first, the numbers of successfully settling grunts and high-hats are likely to be reduced. The reverse, however, is not true; snappers do settle on reefs already occupied by their prey. It is likely that the prey quickly outgrow the size-range in which they are susceptible to predation by newly settling snappers, thus allowing coexistence of these species in areas where the prey settle first. This situation is analogous in mechanism and effect to size-limited predation found in temperate intertidal and freshwater communities (Dodson 1970, Paine 1976, Zaret 1980). Our results are similar to those found in a number of studies on sessile marine communities. Order of settlement can determine the species composition in fouling communities (Sutherland 1974, Sutherland and Karlson 1977), and depending on the species identity of the resident and the larvae, residents may prevent or decrease larval recruitment (Sutherland and Karlson 1977, Sutherland 1978, Kay and Keough 1981). The suppression of juvenile recruitment by residents is in accordance with Connell and Slatyer's (1977) inhibition model of plant succession, a model which has also been supported by research on succession in algal 3. Effect of the presence of adult beaugregories (Eupomacentrus leucostictus) on the recruitment of reef butterflyfish (Chaetodon sedentarius). TABLE Number of reefs on which: Reef butterfly arrives and stays more than one census Beaugregory present Beaugregory absent Observed Expected 0.0 6.5t 2.6 3.9 6.5 No reef butterfly stays more than one census Expected Observed 9.4 14.1 12.0 ll .5t N umber of reefs 12* 18 23.5 X2 = 5.53; df = 1; P < .025 * Three of the 15 beaugregories transplanted onto the reefs disappeared in the first few days. t On one reef, a reef butterflyfish was present before the beaugregory transplant and remained on the reef for more than two censuses. No new reef butterflyfish arrived, so the result was split between the two categories. This content downloaded from 195.113.56.251 on Mon, 14 Apr 2014 18:21:02 PM All use subject to JSTOR Terms and Conditions 1512 MYRA J. SHULMAN ET AL. 4. Comparison of recruitment to "new-moon" and "full-moon" reefs the first 7 d after they were built. TABLE No. recruits per reef New moon (intermediate) Full moon (young + old) Median test Species x SD X SD Mahogany snapper Diplectrum sp. Blackfin snapper Doctorfish Sharpnose puffer High-hat 1.10 0.30 0.40 0.40 0.60 0.00 1.45 0.48 0.70 0.97 0.86 0.00 0.75 0.00 0.05 0.00 0.10 0.75 1.16 0.00 0.22 0.00 0.31 1.29 P .006 .03 .09 .10 .06 .04 Ecology, Vol. 64, No. 6 ment into a habitat. The existence of priority effects may have evolutionary significance by producing selection of potential prey for settlement before potential predators. It is probable that there exist other priority effects, of varying degrees of subtlety, among juvenile coral reef fish. Indeed, our results show that the higher the density of the resident population, the lower the net recruitment to a reef. It is likely that a large number of intra- and interspecific interactions, of which the ones elucidated in this study are examples, combine to produce this result. ACKNOWLEDGMENTS communities (Sousa 1979) and terrestrial plant communities (see examples in Drury and Nisbet 1973, Connell and Slatyer 1977). The ecological implications of the two kinds of priority effects found in our study are diametrically opposed. If residents can successfully exclude certain species from a habitat while allowing the recruitment of others, fish assemblages become more predictable. The composition of these assemblages can be stable if residents allow their own species to settle while excluding others, "successional" if residents replace each other in a transitive order, and cyclical if multispecies priority effects are nontransitive (Jackson and Buss 1975, Buss and Jackson 1979). In contrast, the existence of juvenile-juvenile priority effects, in which an unpredictable order of settlement of juveniles alone determines community composition, introduces a stochastic element into the structure of fish assemblages and increases their variability. This variability may be prolonged by subsequent, deterministic resident-juvenile priority effects, depending on which juveniles are permitted to recruit. The present controversy about the structure of reef fish assemblages centers on the degree of determinism and stochasticity inherent in the processes that govern this system. Data of the type presented here are critical to this issue and suggest the following conclusion: in unoccupied habitat (created by storms, mortality, changes in reef structure), the order of settlement, particularly of predators and prey, will partially determine composition of the initial assemblage; in occupied areas, residents are likely to determine which species can possibly invade, but within this group of "permissible" invaders, order of settlement may determine which will successfully recruit into the habitat. The order of settlement of juveniles will be influenced by the lunar and seasonal periodicities in settlement patterns. Lunar cycles of settlement are reported here and elsewhere; many studies have also show seasonality of spawning and settlement of reef fishes (Johannes 1978 and included references). The timing of settlement of potential prey species relative to their predators can be a crucial factor in successful recruit- We thank the MannedUndersea Science and Technology programof the National Oceanic and AtmosphericAdministrationfor financialsupportand use of the Hydrolabfacilities. The Hydrolabstaff, B. Walden, Dr. W. Shane, and R. Catanack, and support divers, F. Pecora and M. Pacifico, providedexcellent logisticalsupport.We thankthe manycolleagues who commented on the manuscript.This is contribution No. 74 from the West Indies Laboratory, Fairleigh Dickinson University. LITERATURE CITED Anderson, G. R. V., A. H. Ehrlich, P. R. Ehrlich, J. D. Roughgarden, B. C. Russell, and F. H. Talbot. 1981. The community structure of coral reef fishes. American Naturalist 117:476-495. Birkeland, C., and S. 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