MARINE ECOLOGY PROGRESS SERIES Vol. 169: 251-261, 1998 Published August 6 Mar Ecol Prog Ser l
Effects of predators on growth, mortality and abundance of a juvenile reef-fish: evidence from manipulations of predator and prey abundance
S. D. Connell*
School of Biological Sciences A08, University of Sydney, New South Wales 2006, Australia
ABSTRACT: Studies of open populations, in which offspring are dispersed away from their natal site, often emphasise density-independent processes, namely stochastic variation in the input of newly arrived young (recruitment). Studies of closed populations, in which offspring remain close to their natal site, emphasise the role of density-dependence, particularly through competition and predation. The usefulness of th~sdichotomy was tested on spiny chromis Acanthochromispolyacanthus, which is one of the few marine fish that lack a pelagic larval phase and is thought to be the archetypal species for closed population status among reef-fishes. Experimental manipulations showed that juvenile A. polyacanthus suffered lower rates of mortality in locat~onswhere large predatory fish were excluded. The magnitude of differences in n~ortalitybetween treatments (cages and open plots) matched natural differences in mortality between locations representing low and high numbers of predators, suggesting that large predatory fish were a primary source of juvenile mortality. Growth did not Increase when prey and predator abundances were reduced. This finding rejected 2 models: that growth was reduced in large schools and these slower growing individuals suffered greater rates of predation; and that intraspecific competition occurred. Growth of prey increased when released from predation pressure, a process not previously considered in studies of growth in reef-fish. The repression of growth in response to predation pressure indicates that predators may have a more far-reaching effect on demog- raphy of reef-fish than previously thought. Predation was density-dependent in that juveniles in larger schools suffered greater rates of mortality in the presence of predators but not In their absence. Preda- tion appeared to limit the upper size of schools, but this d~dnot eliminate a linear relationship between input and subsequent abundance. Hence, dens~ty-dependent predation was weak and large fluctua- tions in recruitment (births) persisted and contributed importantly to fluctuation in prey density. These results support the model that when density-dependent mortality is weak, both input and subsequent mortality will be important limiting factors. Consequently, this study questions the assumption that variation in predation and competition has greater consequences for closed populations.
KEY WORDS: Reef-fish Predation Mortality Open populations . Growth . Experiment
INTRODUCTION 1968). However, many populations are 'open'. For example, the majority of marine fish have a dispersive Early studies of ecology focused on 'closed' popula- phase in which sedentary adults produce larvae that tions (sensu Caswell 1978) in which offspring remain disperse from their natal reefs to new reefs (Doherty close to their natal site. Historically, ideas of density- 1991). Most studies of open populations of reef-fish dependent regulation have arisen from the study of have emphasised the role of stochastic variation in the closed populations (e.g. MacArthur et al. 1966, Cody input of new individuals (recruitment); an increase in recruitment is thought to lead to an increase in popula- tion size (for reviews see Doherty & Williams 1988, 'Address for correspondence: Centre for Research on Ecolog- ical Impacts of Coastal Cities, Marine Ecology Laboratones Doherty 1991, Booth & Brosnan 1995). The implicit All, University of Sydney, New South Wales 2006, Aus- assumption is that the rate of demographic processes tralia. E-mail: sconnellOb~o.usyd.edu.au (e.g. mortality) do not alter patterns of recruitment.
O Inter-Research 1998 Resale of fullarticle not permitted 252 Mar Ecol Prog SE
The western Pacific pomacentrid Acanthochromis and size structure of Carribbean reef-fishes shortly polyacanthus (spiny chromis) is the only well docu- after settlement (Shulman & Ogden 1987, Hison & mented reef-fish that lacks a dispersive larval phase Beets 1993) and may also affect the structure of these (Thresher 1983a, 1984) and, as such has been argued to reef-fish communltles by altering the relative abun- be the archetypal candidate for closed population sta- dances of prey established at settlement (Carr & Hixon tus among reef-fishes (Booth & Brosnan 1995). A. poly- 1995). Reduced predation pressure at One Tree Reef acanthus do not disperse into the water column as on the Great Barrier Reef resulted in increased abun- eggs or after hatching from eggs, but remain within dance of prey (Doherty & Sale 1985) and alteration of their parents' territory for a number of days (Thresher patterns of recruitment (Caley 1993). Moreover, these 1984). Such direct development results in extremely studies suggest that the effect of predation on patterns limited dispersal of new young. Therefore, if the of prey abundance depends largely on the modifica- closed/open population-density-dependenthndepen- tion by predators of peaks in abundance of new juve- dent dichotomy is useful, I predict density-dependence niles (Caley et al. 1996, Stee1.e 1997). Despite this evi- in this reef-fish. dence, debate centres on the notion that variation in Although many marine organisms by-pass the recruitment to open populations swamps any effect planktonic larval period, most have a planktonic phase due to predation (Doherty 1991, Doherty & Fowler where dispersal varies from a few meters (Olson 1985) 1994). to thousands of kilometres (Scheltema & Williams Using a closed population of reef-fish, Acantho- 1983). Contrary to the current paradigm, not all coral chromis polyacanthus, this paper presents the results reef-fishes with pelagic larvae live in open popula- of field experiments designed to (1) test whether large tion~.In some atoll lagoons, some taxa h.ave predomi- predatory fish were the primary source of mortality nantly closed populations in which they complete their observed in 2 habitats, (2) determine whether school- life-cycles (Leis 1994). Most studies of reef-fish focus size affects per capita rates of mortality under different on solitary species with widely dispersed young, hence regimes of predator pressure, and (3) assess the rela- insights into species of a very different nature, such as tive contributions of recruitment and predation in Acanthochromis polyacanthus, may offer new percep- structuring patterns of juvenile abundance. tions of the more intensely studied species and a greater understanding of population dynamics of reef- fish in general. Indeed, comparisons of life-history METHODS traits of species with contradictory dynamics have pro- vided clues about the nature of differences in popula- The prey species and links to predators. The work tion dynamics of other systems (e.g. Cappuccino & was done between October 1991 and December 1993 Price 1995) for which dispersal distance has been in the largest lagoon of One Tree Reef (23"30'S, hypothesised to be an important trait (Hunter 1995). 152'06' E),a lagoonal platform reef in the Capricorn- Mortality is the most direct way population abun- Bunker group, Great Barrier Reef, Australia (described dance may be mod.ified. Predation, particularly by in Jones 1987). The prey examined, juvenile Acan- large fish, is a major source of mortality in juvenile thochromls polyacanthus (Pomacentndae), are known reef-fish (Shulman & Ogden 1987, Hixon & Beets 1993, to be consumed by the most abundant serranid, Plec- Carr & Hixon 1995) and this is thought to be the tropomus leopardus (Kingsford 1992), and a lutjanid, case for juvenile Acanthochromis polyacanthus. These Lutjanus carponatatus (S. Connell pers. obs.), within juveniles suffer high rates of mortality which can be the main lagoon of One Tree Reef. Other common correlated to the abundance of large predatory fish large predatory fish (>200 mm total length, TL) have (Connell 1996) Although large predatory fish make also been documented to consume fish within the main up a large proportion of coral reef-fish assemblages lagoon of One Tree Reef (Connell 1998). (Williams & Hatcher 1983), there are many other Adult Acanthochromis polyacanthus are generally predators (Hixon 1991) and sources of mortality in territorial and form stable heterosexual pairs. Females fish, e.g. parasitism (Minchella & Scott 1991), disease lay eggs in crevices (Thresher 1985a, Nakazano 1993). (Schmale 1991) and cannibalism (Nakazono 1993). producing up to 300 fry at hatching (Thresher 1983a). Hence, explanatory statements about the causes of Hereafter I refer to the fry as juveniles (sensu Leis & mortality may have little predictive power until there is Rennis 1983, Thresher 1983a, b, 1984). These free- a greater understanding of the contrib.ution of alter- swimmlng juveniles form a small school that is nate sources of mortality. defended by both parents untll they reach an age New evidence suggests that predation may play a of approximately 30 d and a total length of approxi- larger role in open populations of reef-fish than previ- mately 20 mm (Thresher 1983a). During this time, ously thought. Resident predators can alter the density juveniles live within their parents' territories and are Connell: Predation on a ju\~enilereef-fish 253
protected by their parents from the attack of p~scivores The experiment was based on the same caging treat- (Nakazano 1993). These juveniles are unlikely to sur- ments as in Expt I, plus an additional treatment in vive in the absence of their parents because if one or which prey density was manipulated prior to cage con- both are removed from the school, disappearance of struction. Abundances of both predator and prey were the school through predation is almost certain manipulated in a 2-way design between October and (Thresher 1985b, Nakazano 1993).Hence, the loss of December 1993. Schools were manipulated to be small small individuals (<20 mm TL) from within a school is (ranging from 13 to 65 individuals) or large (ranging more likely to represent mortality than emigration. The from 85 to 170 ~ndividuals).These 2 ranges in abun- current study focused on smaller individuals (
population density, similar to Murdoch & Walde (1989). with a high body profile. Cages were accessible to The number and rational for replication of treatments small invertebrates (e.g.Sto~natopoda), small fish (e.g. is described below ('Replication and statistical evalua- Pseudochromidae, Synodontidae), elongate predators tions'). All replicates were haphazardly located among (e.g. Muraenidae, Synodont~dae,Fistularidae) and ju- 3 locations on continuous reef where predator abun- veniles of the large predatory fish (<200 mm TL) (e.g. dance was high. Serranidae, Scorpaenidae, Lutjanidae). Monitoring abundance and mortality of prey. Adult The literature was reviewed for major artefacts asso- pairs of Acanthochrornis polyacanthus without juve- ciated with caging fish from hard substrata, and spe- niles were visited every second day to determine cial attention was given to these artefacts in planning whether hatching had occurred. The number and and interpreting the experiments (see Connell 1997). mean total length of new juveniles observed with an In cases where artefacts could not be minimised or adult pair within a 48 h period defined recruitment. eliminated from the experimental design, controls Hatching within a batch of eggs appeared to occur were augmented with additional data to determine the simultaneously, but hatching among batches occurred importance of these artefacts. It was concluded that between mid October and at least late November. caging artefacts were minimal, and that the experi- Mortality rates were based on the loss rate of a cohort mental effects of excluding large predatory fish could of individuals hatched from a single batch, and indi- be interpreted (Connell 1997). vidual batches or schools could be followed through Replication and statistical evaluations. The level of time because they continuously occupied a discrete replication for each experiment was based on the area of reef. Mortality was calculated using the per- potential effect-size of predation observed in the previ- centage of individuals lost between hatching (gener- ous year. For Expt I, observations of mortality in the ally 6 mm TL) and mean total length of 18 mm, after previous year (1991) indicated that survivorship was which some individuals were observed to pass briefly 30 % greater In locations containing fewer large preda- outside their cages. Errors in counting and length esti- tory fish (patch vs continuous reef) (Table 1).The num- mation in the field were quantified by comparing esti- ber of replicates needed to detect this effect-size was mates of abundance and length with collections of the determined using a statistical procedure that calcu- same fish (Connell 1996). Because these errors did not lates sample size and power for a 1-factor ANOVA alter the results, uncorrected data are presented. (Underwood 1981). This calculation indicated that Manipulation of predator abundance. Three treat- 6 replicates per treatment were required to detect a ments manipulating predator abundance included: 30% difference (power = 0.89 at a = 0.05), hence (1) exclusion cages (full cages) which allowed access of 6 replicate treatments were used in Expt I. small fishes but excluded large fishes (>ZOO mm TL); The level of replication for Expt I1 was calculated to (2) cage controls (partial cages) that allowed access of detect at least a 14 % difference in survival, that is, the all fish while controlling for the presence of the cage; difference in magnitude of mortality found between and (3) unmanipulated controls (open plots) that had full cage and open plot treatments in Expt I. The calcu- no structure and allowed access of all fish. Four steel lation determined that 12 replicates per treatment stakes (3.2 m length) were driven approximately 1 m (open plots, full and partial cages) would be needed to into the substratum and acted as corner posts for a have a 95% chance of detecting a 14% difference roughly square cage enclosing a surface area of among the 3 treatments (power = 0.80 at a = 0.05). 3.6 * 0.3 m2 Galvanised wire mesh (with a mesh size of Hence 12 replicate treatments were used for Expt 11. 50 mm) was fastened to the stakes to create a top and All data were analysed with ANOVA. Data were 4 sides. Partial cages were of similar configuration to tested for homogeneity with Cochran's C test and full cages, except that only half of each side was transformation of data followed procedures suggested covered in mesh (see Connell 1997). Full and partial by Underwood (1981). Percentage data were trans- cages were constructed around individual Acantho- formed using arc-sine square root; abundance data did chromispolyacanthus schools and their parents and not require transformation. completed before dark on the day hatching was first The use of size-related mortality. In this study sur- detected. To determine whether cage construction vivorship was estimated by the size, not age, of the influenced immediate juvenile survival, school size individual, because size may be more important in was counted immediately before and after construc- determining life-history characteristics for fishes, as it tion. No immediate losses were detected. is for many other organisms with indeterminate growth Full cages used in this study were effective in exclud- rates (see Kirkpatrick 1984). It is often suggested that lng large predatory fish. Hence, losses within cages growth rates in fish may influence mortality, especially were considered to be due to any source of mortality, if mortality is size-dependent (e.g Doherty & Sale except predation by large predatory fish (>200 mm TL) 1985).Moreover, growth rates of fish are often the most Connell: Predation on a juvenile reef-fish 255
sensitive demographic parameter to changes in envi- (a) Experiment I ronmental conditions (review Jones 1991) and can identify the important life-stages for which members of a population are likely to undergo profound changes in their abundance. In this study, the response of prey to predation pressure was strongly related to growth.
RESULTS
Expt I: Are large predatory fish the primary cause of prey mortality? There was a trend for survival to be enhanced in full cages for both Expt I and I1(Fig. 1). This phenomenon in itself is not surprising given that the exclusion of piscivores, which by definition eat fish, is likely to affect prey mortality. Importantly, the differ- ence in survivorship between full cages (no large predators) and open plots (large numbers of predators) was similar to the difference in survival between habi- (b) Experiment II tats containing naturally high or low numbers of these same predators (Table 2). This observation provided strong evidence that large predatory fish were primar- ily responsible for the difference in mortality observed between continuous and patch reef. Interpretation of statistical results for Expt I (1992) was equivocal. Although all treatments started with similar numbers of recruits (ANOVA: F2,2= 0.01, p > 0.50) and there was a trend for mortality to be greater among open plots (Fig. l), no differences were detected in survival (ANOVA: F2,2= 1.92, p > 0.10) and subsequent numbers of juveniles (ANOVA: F2,2= 0.36, 0 Full cage p > 0.50). Post-hoc power analysis, however, indicated Partial cage that the experiment may not have been powerful Open plot enough to detect the effects of the treatments on sur- vival (power = 0.42). This result may have occurred because the differences between cages and open plots Total length (mm) were less than expected. Although power analysis based on preliminary (1991) estimates of the predation Fig 1 Acanthochromis polyacanthus. Mean percentage sur- effect (30%) was used to establish replicate number, vival (t SE) per school among the 3 caging treatments versus such an effort can only be used as a rough guideline total length of juvenile individuals. Shown are the results from (a) Expt I (n = 6) and (b) Expt 11 (n = 12) since effect magnitudes could be less (reduced to 14 % in this study) or more than the preliminary estimates. The apparent importance of predation but equivocal school-size in the presence of predators (Fig. 2a: statistical result motivated Expt I1 (1993). This second Spearman's rank correlation cofficient = 0.39, n = 24, experiment not only retested the importance of preda- p < 0.05 for l-tailed test), but not in their absence tion using the revised effect-size of 14 % (1992), but it (Fig. 2a: Spearman's rank correlation cofficient = 0.18, also assessed whether mortality rates associated with n = 12, p > 0.05 for l-tailed test). Although this suggests predation would respond to variation in prey abun- that mortality was structured by density-dependent dance. predation, this relationship was weak (Fig. 2a) and Expt 11: Does predation cause density-dependent ANCOVA did not detect differences in school-size- mortality? If mortality is caused by density-dependent related mortality between treatments with and without predation, per capita mortality should increase with predators (interaction for the slopes: FlOs2= 0.75, p > increasing school-size in the presence of predators, but 0.25). show no trend in the absence of predators. The data Although small schools (475 individuals) are more show a positive relationship between mortality and defensive towards attacks from predators (Thresher 256 Mar Ecol Prog Ser 169: 251-261, 1998
(a) 1985a) this behaviour did not greatly affect the rate of mortality (Fig. 2b). Similar proportions of juveniles were lost from small and large schools (Fig. 3). Juve- nile survivorship was significantly greater In full cages than in partial cages and open plots (Fig. lb, Table 3a; SNK test, full > open = partial). Final and initial patterns of abundance were decou- pled among cage treatments but not between density treatments. Between dens~tytreatments, large schools remained, larger than small schools (cf. Fig. 3a, b, Table 3b, c). Among cage treatments, final abundance follolved a simple pattern (Table 3c; SNK test, full = 2 open > partial), whereas initial abundance showed an rh rl 01 = .lt. interaction between cage and density treatments 0 50 100 150 200 (Table 3b; SNK test, open > cage > partial among large Initial number of juveniles per school schools and open = cage = partial among small schools). This indicates that predation can modify small variation in recruitment (Fig. 3a, b: compare ra.nk abundance for large schools), but not the largest varia- tion in recruitment (Fig. 3a, b: compare rank abun- dance between small and large schools). A positive correlation between input and subsequent abundance has been used as evidence for recruitment limitation (Doherty & Fowler 1994). While there was a significant positive correlation between initial and remaining number of prey in both the presence (Spear-
-- - p Fig. 2. Acanthochromspolyacanthus. Expt 11 Effect of school- slze on (a) mortal~ty of juveniles among treatments with predators (0 = open plots and partial cages, n = 24) and wi.th- out predators (0 = full cages, n = 121; and (b) mean percent- age survival (* SE)per small and large school among all treat- ments (n -18). Numbers above symbols represent repeated Total length (mm) (superimposed) counts
Table 2. Acanthochromis polyacanthus Comparison of natural and experimental surv~vorshlp(between hatchlng and 18 mm TL) among locations and treatments of hlgh and low predation pressure. Predation pressure IS Inferred from the density of large predatory fish that was (1) high on continuous reef and open plots, (2)low on patch reefs, and (3)zero in tullcages X=mean per- cent survivorship per school, s = 1 standard deviation of the mean
Natural survivorship Experimental survivorship ------L (a) Experiment I Predation pressure locv Patch reef Full cage X=826,s=122,n-30 X=87.7, S = 7.6, n = 6 Predat~onpressure high Continuous reef Open plot a=68.6, s = 17.3. n = 30 X=71.4, s = 13.8, n = 6 Llkely effect due to predators Patch -Continuous = 14.0 Full - Open -16.3
(b) Experiment I1 Predation pressure low Patch reef Full cage R=87.1, S= 157, n=30 X=90.9,s=7.4,n=12 Predation pressure hlgh Continuous reef Open plot X= 68.2, s = 21.0, n = 30 P = 69.8, s = 19.5, n = 12 Likely effect due to predators Patch - Continuous -18.9 F1111 - Open = 2 1.1 Connell: Predation on a juvenile reef-fish 257
(a) Initial abundance at hatching a suggestion that predation limited the abundance of 10U, older prey (Fig. 4). In the absence of predators all L W schools that started with > 100 individuals finished with 120 >l00 individuals, but in the presence of predators all .-W C schools that started with > 100 individuals finished with 9 80 .- 5100 individuals. This result is unlikely by chance -o alone (p < 0.009; Fisher's Exact Test) and suggests that Db 40 predators limited the number of older fish to 1100 fish S per school. = 0 Cage Open Partial Is growth influenced by the abundance of con- specifics and predators? The nlaxilnum age at which a (b) all schools remained inside cages was 12 d, hence the c U effects of density and cages on growth were calculated U) L for 12 d old fish ( (c) Percentage survivorship DISCUSSION I I Reef fish, which predominantly have open popula- tion~,are thought to differ from organisms with closed populations because variation in input (recruitment) from planktonic larvae is considered to have dispro- portlonate effects on population abundance (reviews: Doherty & Williams 1988, Booth & Brosnan 1995). The validity of this recruitment-limitation model depends on the extent to which patterns of input are modified Cage Open by mortality, predation often being assumed to be the Treatment main source of mortality. Therefore, if closed popula- Fig. 3. Acanthochromispolyacanthus. Expt 11. Mean number t'OnS are less affected by I predicted (+ SE) of juveniles per school for large and small schools, that predation, and not variation in input, would among caging and density treatments(n = 6) at (a) the begin- primarily contribute to the abundance of Acantho- ning of the experiment and (b)the end of the experiment; and chromispolyacantllus (closed population), (c) mean percentage survival (t SE) per school at the end of the exper~~nent Predation influences both mortality and growth man's rank correlation coefficient = 0.86, n = 24, p < 0.05) and absence of predators (Spearman's rank cor- Predation was the major cause of mortality in Acan- relation coefficient = 0.97, n = 12, p < 0.05) there is also thochrornis polyacanthus. Similar results have been Table 3. Acanthochromis polyacanthus.Results of 2-way ANOVAs showing variation In (a) survival. (b) initial abundance, and (c) abundance of juveniles at 18 mm TL among treatments of Expt 11. Cochran's C test, variances = 6, df = 5 Source df (a)C = 0 361 (b) C = 0 349 (c) C = 0.378 MS F P MS F P MS F P Cages (= Cg) 2 872 4.07 <0.05 2909 10.9 <0.01 2438 9.5 <0.01 Density 1 386 1.80 >0.10 422849 160.6 <0.01 21121 81.9 <0.01 Cg X Density 2 37 071 >0.50 937 3.5 <0.05 280 1.1 >0.25 Residual 30 214 266 258 Mar Ecol Prog Ser 1996, Jones 1997) may be explained by a combination of small and larger predatory fish. Variation in growth of coral reef-fish is seldom dis- cussed in relation to regimes of predation pressure. Instead, such variation is more often linked to variation in conspecific density and/or food availability (Jones 1986, Forrester 1990, Kerrigan 1994, Booth 1995). In the current study, however, a reduction in predation pressure resulted in the increase in growth of prey, a phenomenon which has not previously been reported in coral reef-fishes. Differences in growth between dif- ferent levels of predation pressure are most likely due to a lower level of harassment, facilitating uninter- rupted feeding (see Sih 1997). A number of studies have established that young fish can recognise their predators (review: Stein 1979) and subsequently alter their feeding behaviour (Schmitt & Holbrook 1985). For Initial number of juveniles per school example, the duration (Holbrook & Schmitt 1988) and rate (Prejs 1987) at which fish feed can alter when they Fig. 4. Acanthochromis polyacanthus. Expt 11. Relationship are at risk of predation. The present data offer 2 impor- between the surviving number of juveniles per school and initial density among treatments with predators (0 = open tant insights. First, variation in growth of prey may not plots and partial cages, n = 24) and without predators (0 = always be a simple response to prey density and/or full cages, n = 12) Each point represents a school and a quad- food availability; and second, if predation affects rates ratic line has been fitted to hollow and filled points using of growth, it may also affect rates of maturation and SYGRAPH (Wilkinson 1990) fecundity. Both are likely to be more closely related to size than age in fish (Jones 1991). found in other experimental studies, suggesting that predation (particularly predation by large fish) can be Density-dependent predation and its effect on a major cause of juvenile mortality (Shulman & Odgen abundance 1987, Caley 1993, Hixon & Beets 1993, Carr & Hixon 1995, Hixon & Carr 1997). Despite such observations, Although density-independent mortality can modify the extent to which large predatory fish are responsi- patterns of recruitment (Warner & Hughes 1988) the ble for natural mortality is often not known. Hence, a documentation of density-dependent mortality has strength of the current study was the ability to com- been a major focus of fish ecologists. This is largely pare experimental mortality to natural mortality. Here, because density-dependent mortality provides a mortality experimentally attributable to large preda- mechanism for limiting population abundance after tory fish was similar to the difference in natural mor- recruitment, and evidence for the lack of density- tality between reefs with high and low densities of dependent mortality has been used to infer recruit- predators. This equivalence suggests that large preda- ment limitation (see Doherty & Fowler 1994). How- tory fish were the primary source of early juvenile mor- ever, the usefulness of this dichotomy has been tality between locations with low and high densities of recently questioned (Steele 1997) and this doubt is these predators. well illustrated here. Mortality was weakly density- It has been suggested the mortality of juvenile reef dependent in the presence of predators. Conse- fish may also be strongly affected by small predatory quently, predators did not eliminate the largest peaks fish (Connell 1998). Small piscivorous fish, such as in abundance (large vs small schools), but variation in Thalassoma lunare (Connell 1998), appear to con- predation pressure did eliminate smaller peaks tribute to the pattern of greater mortality of juvenile among large schools. Hence, patterns of abundance Acanthochromis polyacanthus on continuous than were set simultaneously by input and subsequent patch reef. Encounter rates of small predatory fish with density-dependent predation. While this possibility is schools of juvenile A. polyacanthus have been posi- not a new idea (Warner & Hughes 1988) and many tively correlated with this pattern of mortality at these studies have tested for density-dependent mortality reefs (Connell unpubl. data). Hence, patterns of (reviews Jones 1991, Booth & Brosnan 1995, Caley et greater mortality of juvenile and adults at the perime- al. 1996), data supporting this model are few (see ter of the lagoon than the centre of the lagoon (Connell Steele 1997). Connell: Predation on a juvenile reef-fish 259 (a) Among cages Solitary species are by far the most studied reef-fish (review Jones 1991), but they tend to recruit in smaller numbers and suffer smaller rates of mortality than their gregarious congeners (Connell & Gillanders 1997). Gregarious species tend to have very high initial density, but then suffer extraordinarily high rates of mortality (e.g. Eckert 1987, Shuln~an & Ogden 1987, Connell 1996) which may bound fluctuations in abundance of older fish from year to year. If predators target abundant, aggregating prey, density- dependent predation may be an impor- 0 2 4 6 8 10 12 14 tant population regulator of schooling Time (day) species and less important for the more commonly studied solitary species (c.f. Carr & Hixon 1995, Hixon & Carr 1997). (b) Between densities 15 - - Conclusions E The exclusion of large predatory fish, WE some of which were known to consume 5 10 - - reef-fish and juvenile Acanthochro- C0 mis polyacanthus, resulted in the en- al - hanced growth and survivorship of juve- -m @ Large niles. Large predatory fish, at least in P some years, may be the primary source of 5 Small - juvenile mortality in A. polyacanthus between continuous and patch reef. 0 2 4 6 8 10 12 14 Strong support for the reality of these Time (day) experiments can be derived from the observation that the maanitude of exDer- Fig. 5.Acanthochrornjs polyacanthus. Mean total length (i SE) per school imental mortality to versus time for schools: (a) among caging treatments (n = 12) and (b) be- tween densitv treatments fn = 181 magnitude of mortality occurring in the natural environment. Nonetheless, the large differences in survivorship be- The possibility that predators are highly likely to tween years illustrate the variable nature of predatory respond differently to large aggregations of prey impacts over time. The results also indicated that rather than to smaller aggregations or to isolated indi- intraspecific competition was unimportant as a factor viduals has been recognised in other systems such as contributing to growth, mortality and juvenile abun- insects (e.g. Cappuccino 1991), marine invertebrates dance. Although predation was the primary source of (e.g Eggleston et al. 1992) and mammals (Sinclair et mortality, because it was weakly density-dependent, al. 1990), but not so much for reef fish. Little is known large fluctuations in recruitment (births) persisted and about prey selection in piscivorous fish, but it seems contributed importantly to fluctuation in prey density. that large predatory fish target Acanthochromispolya- Density-dependent processes may not only directly canthus in larger schools. Kingsford (1992) suggested influence abundance through mortality, but also indi- that much of the spatial and temporal variation in the rectly through growth. If early juvenile mortality is diet of a large grouper could be attributed to the pref- high, slower-growing individuals may be subject to erence for and availability of abundant, aggregating higher age-specific mortality rates (see reviews: prey. Similarly, such prey selection has been proposed Doherty & Williams 1988, Mapstone & Fowler 1988). In to explain why abundant, schooling species suffer this study, the failure to detect negative effects of den- greater rates of mortality than solitary species from sity on growth indicates that density-dependence did those families (Connell & Gillanders 1997). not influence mortality through heavier predation on 260 Mar Ecol Prog Ser 169: 251-261, 1998 slower growing schools. In conclusion, this study sup- Connor EF. Beck MW (1993) Density-related mortality 11, ports the model that when density-dependent mortal- Cameraria hamadryadella (Lepidoptera: Graclllariidae) at epidemic and endemic densities. Oikos 66:515-525 ity is weak, both Input and su.bsequent mortality will Doherty PJ (1991) Spatial and temporal patterns in recruit- be important limiting factors. Furthermore, it questions ment. In: Sale PF (ed)The ecology of fishes on coral reefs. the assumption that variation in predation and compe- Academic Press, San Diego, p 261-293 tition has greater consequences for closed populations Doherty PJ, Fowler AJ (1994) Demographc consequences of than open populations. variable recruitment to coral reef fish populations: a con- generic comparison of two damself~shes.Bull Mar Sci 54: 297-313 Acknowledgements Th~s manuscript was Improved by Doherty PJ, Sale PF (1985) Predation on juvenile coral reef N. Andrew, M. Beck. S. Holbrook, C. Buxton, B. Gillanders, fishes: an exclus~onexperiment. Coral Reefs 4:225-234 M. Kingsford, B. Menge and A. Underwood. A large number Doherty PJ, Wilhams DMcB (1988) The replenishment of coral of people assisted in the field: T. Crowe, N. 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