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Home , Coral reef fish, Lethrinus nebulosus, Teleost

MARINE ECOLOGY PROGRESS SERIES Published March 3 Mar. Ecol. Prog. Ser.

Fish feeding and dynamics of soft-sediment mollusc populations in a reef

G. P. Jones*,D. J. Ferrelle*,P. F. Sale***

School of Biological Sciences, University of Sydney, Sydney 2006, N.S.W., Australia

ABSTRACT: Large were experimentally excluded from enclosed plots for 2 yr to examine their effect on the dynamics of soft sediment mollusc populations from areas in One Tree lagoon (). Three fish which feed on benthic molluscs. nebulosus, Diagramrna pictum and Pseudocaranx dentex, were common in the vicinity of the cages. Surveys of feeding scars in the sand indicated similar use of cage control and open control plots and effective exclusion by cages. The densities of 10 common of prey were variable between locations and among times. Only 2 species exhibited an effect attributable to feeding by fish, and this was at one location only. The effect size was small relative to the spatial and temporal variation in numbers. The power of the test was sufficient to detect effects of fish on most species, had they occurred. A number of the molluscs exhibited annual cycles in abundance, with summer peaks due to an influx of juveniles but almost total loss of this cohort in winter. There was no evidence that altered the size-structure of these populations. While predation by fish is clearly intense, it does not have significant effects on the demo- graphy of these molluscs. The results cast doubt on the generality of the claim that predation is an important structuring agent in tropical communities.

INTRODUCTION batididae), derive their energy resources from these soft sediments. The abundance of these groups on Coral reefs are surrounded by and frequently coral reefs may be more dependent upon the sur- enclose expansive areas of soft sediments which are rounding sediments than the reef itself. An under- rich in (Taylor 1971, Birtles & Arnold standing of the interactions between these 2 systems 1983, Jones 1984, St. John et al. 1989). Our knowledge requires more information on the impact of fish of the basic patterns of species composition and their feeding, firstly on the soft-sediment assemblages, and distributions is limited (St. John et al. 1989, Jones et ultimately, on the coral reef system itself. al. 1990).The dynamics of populations living in these It has been argued that the impact of predation by sediments and the processes affecting these popula- on benthic marine communities may be higher tions are poorly understood, yet these areas adjacent in tropical than in temperate regions (Bakus 1969, to coral reefs may be an important component of 1981, 1983, Vermeij &Veil 1978, Bertness 1981, Gaines the reef system itself (Hatcher et al. 1989, Parrish & Lubchenco 1982, Lubchenco et al. 1984),despite the 1989). A variety of reef-associated fishes, particularly fact that to date, most of the experimental work on large (families , , predation has been done in temperate waters (Choat Carangidae) and elasmobranchs (Dasyatididae,Mylio- 1982, Sih et al. 1985) and predation is an integral part of the ecological models developed for these cooler, Present addresses: lower-diversity systems (e.g. Menge & Sutherland ' Department of , James Cook University, 1976). There is some evidence that fish do affect the Townsville, 481 1 Queensland. Australia distribution of (Neudecker 1977, 1979, Welling- ' ' Research Institute, PO Box 21, Cronulla, N.S.W. ton 1982, Fitz et al. 1983), other sessile invertebrates 2230, Australia " ' Department of Zoology and Center for Marine Biology, (Bakus 1964, Day 1977, 1985, Lubchenco et al. 1984) University of New Hampshire. Durham. New Hampshire and mobile invertebrates on the reef (Bertness 1981, 03824. USA Wolf et al. 1983, Reaka 1985, McClanahan & Muthiga

0 Inter-ResearcNPrinted in Germany Mar.Ecol. Prog. Ser. 80: 175-190, 1992

1989; see Jones et al. 1991 for review). The quality of of cage control and open control sites (do cage controls this information varies, but assuming there are keep fish out?). This was assessed by monitoring predation effects, there is no reason to believe they teleost feeding scars made in all plots of all treatments are any larger than for comparable temperate assem- throughout the study. blages. Predation is thought to play a key role in structuring soft-sediment communities in temperate METHODS waters (Reise 1977, Peterson 1979, Sih et al. 1985; reviewed by Wilson 1991), although this conclusion is This study was carried out between May 1986 and by no means universal (e.g. Berge & Valderhaug 1983, May 1988 in the lagoon of One Tree Reef, near the Thrush 1986). By comparison, predation in the soft- southern limit of the Great Barrier Reef (23'30' S, sediment or communities adjacent to coral 152'06' E). The 10 km2 lagoon primarily consists of reefs have received less attention (Alheit 1981, Alheit carbonate soft sediments separated by reticulated reef & Scheibel 1982, Keller 1983, Jones et al. 1988, St. John structures and isolated patch reefs. Temporal patterns et al. 1989). The data presented in these papers are in the abundance and structure of mollusc populations, inconclusive as to whether or not fish are important in and the effects of fish predators, were monitored in a these systems (Jones et al. 1991). zone of deeper water near the perimeter of the lagoon The aim of this study was to assess the contribution (see Jones et al. 1990). This was the region of greatest of ilsh feeding to natural variation in mollusc numbers mollusc diversity and highest fish feeding pressure on and population structure in One Tree Lagoon, at the a lagoon-wide scale (Jones et al. 1990, 1991). These southern end of the Great Barrier Reef. The soft-sedi- studies had also shown mollusc numbers and fish ment communities within this lagoon contain a rich feeding intensity to vary among locations within this and a'uundaril iduna of moiluscs (Jones et ai. 1990). zone. in view of this we examined temporal patterns These are preyed upon by a number of large, wide- and predation effects at 3 different, randomly selected, ranging fishes such as Lethnnus nebulosus and locations: South, Alley and North. Diagramma pictum (Jones et al. 1991). At each of the 3 locations, there were six 25 m2 plots, A pilot experimental exclusion of fish was carried out 2 of which were randomly allocated to each of the in a previous study, at a single location near the peri- 3 treatments - full exclusion cage ('full cage'), cage meter of the lagoon, to assess the potential of this tech- control and open control. Cages to exclude the large nique for examining the role of predation (Jones et al. teleost fishes were 5 m on each side and 1.4 m high to 1988). Impacts of fish predation/disturbance were allow easy access to divers for sampling. The cages suggested but could not be distinguished from were constructed of an extruded plastic square mesh selection by mobile prey. The latter could have oc- (12 X 12 cm and 1.5 mm thick). They effectively ex- curred in response to changes in sediment composition cluded rays and the 3 species of large teleosts com- inside full exclusion fences, which were quantified monly observed to feed over large, open expanses of over the course of the experiment. sand (Lethrinus nebulosus, Diagramma pictum and In designing this experiment, attention was given Pseudocaranx dentex). Small such as most to the descriptive information already collected on labrids were not excluded but were only observed mollusc abundances and fish feeding pressure and feeding adjacent to reefs. The cages were framed with lessons learnt from the pilot experiment. These con- 2.1 m steel fencing posts driven into the sand and laced siderations included: (1) Given the patchy nature of together with rope around their tops. The structure teleost feeding, it was essential to carry out the same was made taut with guy-ropes at the corners. Skirts of manipulations at a number of locations, to assess the caging mesh 30 cm wide were buried in the sand at the generality of any observed effects. (2) The pilot experi- bottom of the cages and anchored with steel pegs. The ment suggested that mollusc numbers fluctuate control structures for the cages were made in an iden- annually, and treatment effects may not be apparent tical fashion except that the walls only covered half of for at least a year. Two years was considered ample the 5 m sldes, allowing access to fishes. time to detect any substantial effect of predation. (3) The cages were cleaned and any holes repaired after Given the possible mobility of the infauna, exclusion sampling at each period. The large mesh and small cages needed to be as large as possible. (4) The mesh diameter of the mesh material meant that fouling of the used on the exclusion cage should be as large as cage material was only a slight problem and possible to minimize effects on sediments, while still could be removed easily with brooms. The mesh excluding the fish to be tested. (5)The effectiveness of gradually accumulated small oysters and other en- the predator exclusion apparatus needed to be moni- crusting organisms and was replaced on all cages after tored (does it keep fish out?),as well as the relative use the first year. Substantial holes (30 to 100 cm) were Jones et al.: Fish feeding and mollusc population dynamics

infrequently found in some cages, possibly caused by sampled at the last 4 sampling dates using six 1 m2 or turtles. quadrats at each sampling time. Feeding scars in cages All treatments were sampled during May 1986, just were associated with holes in cages, so scars were after the cages were constructed and on 6 subsequent counted prior to sampling or repair of the cages; these occasions: August and November 1986, February, July counts are likely to indicate the hlghest level of fish and December 1987 and May 1988. Methods used to feeding inslde cages. Cages that remalned intact be- sample the abundances of molluscs have been fully tween sampling occasions had no feeding scars, nor described in Jones et al. (1990) and are briefly outlined were feeding scars observed inside cages for at least a below. All 25 m2 plots were sampled with 4 randomly month after repair. placed 0.1 m2 clrcular cores whose contents were Densities of feeding scars provide a relative rather extracted to 5 cm depth with a diver-operated airlift than an absolute measure of fish feeding intensity. The suction apparatus. The airlifted samples were collected latter required an estimate of the number of feeding into 1 mm mesh bags which were immersed directly bites per unit area made per unit time. To calculate this into 3 to 5 % formaldehyde solution for fixation. The we needed an estimate of the longevity of feeding fixative contained a vital stain, Biebrich scarlet, to aid scars. The rate with which the feeding scars filled in in sorting. All molluscs were extracted from the sedi- and became unrecognisable was established for each ment, identified to species level and counted. A check- location using a small coring device (a section of PVC list of most of the molluscan fauna from the present pipe 40 mm in diameter) to make artificial feeding sampling programme appeared in Jones et al. (1990). scars. The artificial scars were indistinguishable from This study concentrated on 10 abundant species real ones, but allowed precise knowledge of their time known to be consumed by large (Jones of formation. At each caging location, 2 plots contain- et al. 1991). These were the gastropods Umbonium ing 4 blocks of 10 artificial scars were created in the guamensis (Quoy & Gaimard, 1834), Pupa nitidula morning. The proportion of scars remaining distinguish- (Lamarck, 1916), Atys cylindricus (Helbing 1779), and able in each block of 10 was checked approximately the bivalves Exotica rhomboides (Quoy & Gaimard, every 3 h. The numbers of artificial scars fllling in over 1834),Exotica cf. virgulata (Hanley, 1845),Fragum sp., time was approximately linear and linear regression Solemya sp., Tellina cf. rnyaformis Sowerby, 1868, was used to estimate the time at which half the arti- Tellina obtusalis Destayes, 1845 and Tellina robusta ficial bites had become unrecognisable for each set of (Hanley, 1844). 10 artificial scars. This procedure gave an estimate of The effects of predators on spatial and temporal the mean life-span of a feeding scar, and allowed the patterns in the structure of mollusc populations were observed values of scars per m2 to be standardised to analysed by examining size-frequency distributions. scars m-2 h-'. This information, combined with an esti- The sizes of all molluscs were measured using a dis- mate of the average volume of each fish bite, was then secting microscope coupled to a high resolution video used to estimate the average time it took for all the camera and monitor. Measurements were made using surface sediment to be turned over by fish. a video position analyser (Four-A Company Ltd., A sediment grain-size analysis was done at all Tokyo, Japan) which superimposed an X-y axis and sampling dates to assess the stability of the sediments cursor on the video image, and data were compiled on and any effects attributable to the caging apparatus. a personal computer. Two 50 m1 jars of sediment were collected from Differences in fish feeding pressure among loca- random locations within all plots, and were processed tions, times and treatments were estimated by survey- by a method suggested by Folk (1974) for carbonate ing the scars left in the sediment by feeding episodes sediments. The samples, which were stored in ethanol, (see Jones et al. 1991). Actively feeding individuals of were first dried to constant weight (ca 7 d at 60 'C) and Lethrinus nebulosus, Diagrarnrna pictum and Pseudo- then wet-sieved through a 63 lmscreen. The retained caranx dentex were followed in to characterise sand fraction was dried, re-weighed and separated

the appearance of the feeding scars in the sediment. into standard 1 C$ fractions by shaking for 10 min on a All 3 species fed by biting into loose sediment, taking a geological sleve shaker. Each fraction was weighed large mouthful and sorting the sediment in the mouth. separately to produce sediment grain size-frequency The depressions left after each bite were uniformly distributions. round with gently sloping sides ending in a flat bottom A mixed model analysis of variance was used to test covered with highly sorted, fine sediment. The scars for the numerical effects of location (a random factor), made by the 3 fish species could not be distinguished time and treatment (fixed factors), and their inter- from each other but were easily differentiated from actions, on each of the common mollusc species. Post- other irregularities in the surface of the sediment. hoc pooling was done wherever p > 0.25 for effects of Scars in caged, partially caged and open plots were interactions, to increase the power of the test for de- Mar. Ecol. Prog. Ser. 80: 175-190, 1992

tecting treatment effects (Winer 1971). Where treat- species, there were inconsistent differences among ments were not significant, power analyses (Cohen times ('Location X Time' interaction; see Table la). 1988) were used to determine what magnitude of tre- indicating significant, location-specific changes over atment effects would likely have been detected in this the 2 yr period. Several taxa experienced peaks of size experiment. abundance in summer (December to February): Atys cylindricus, Umbonium guamensis, Exotica rhombo- ides, Fragum sp., Solern ya sp., and Tellina m yaformis. RESULTS Pupa nitidula and E. virgulata exhibited a tendency to Abundance be higher in the winter months. There were no obvious seasonal patterns for 7: obtusalis and T. robusta, with The abundance of all mollusc species differed patterns of temporal change in abundance differing among location and/or times (Fig. 1). For all but 2 among locations.

-C- sourn & North Fragum sp.

E '2 - 7 Umbonium guamensis 6 5 4 3 2 1 0

Tellina obtusalis

Tellina robusta

May Aug Nov Feb July Dec May May Aug Nov Feb July Dec May 86 86 86 87 87 87 88 86 86 86 87 87 87 88 Fig. 1. Temporal changes in mean densities of the 10 common mollusc species at the 3 sampling locations - North, Shark Alley and South, from 1986 to 1988. Error bars =standard errors. All treatments for each location pooled Jones et a1 : Fish feeding and mollusc population dynamics 179

Table 1. (a) Analysis of varlance results for the effects of time, location, treatment and plot on the dens~tiesof 10 mollusc specles. Homogeneity of varlances was achieved with ln(x+l)transformation ('significant at 0 05 level; "significant at 0.01 level; ns. not significant) (b) Percent variance expla~nedby each factor and the11 interactions Based on raw data. Species: A. C., Atys cylin- dricus, E r., Exotica rhomboides, E. v., Exotica virgulata; E sp., Fragum sp.; P n., Pupa nltidula; S. sp , Solemya sp , T n~.,Tellina myaformis; 7: o., Tellina obtusalis; 7: r., Tellina robusta; U. g., Umbonium guamensis

A.c. Er. E.v. F.sp. P.n Ssp. Tm T.o T. r. U. g

(a) ANOVA results df: Time. A 6 7.4" 49" 14.9" 39 5" 2.8"* 7.8' ' 4.7' 0 5"' 4.7' 4.1' Location, B 2 40.1' 0.8"' 10.8' 217' 5.1' 4.5' 26.7. 4 0' 0.5"' 9.2. Treatment, C 2 14.2' 0.6"' 4.0"' 2.5"' 1.7"' 16.9' 0.1 "VOnS0.7"' 0.4 Plot, D (BC) 9 1.8"' 6.5" 1.2"~ 5.5" 2.dnS 4.6' ' 3.5" 14.8" 11.4" 7.8" AXB 12 4.1" 34" 4.0' ' 12"' 2.4' 1.8"' 3.0" 5.4 ' 4.8" 3.8" AXC 12 2.8' 1.1"' 1.1"' 0 8"' l.OnS 2.6' 1.0"~ 1.2"~ 2.1ns 1.2"~ A X D(BC) 54 2.5" 1.2"~ 2.1'. 13"' 1.5' 1.4' 0.9"' 1.4" 1.5' 1.6" B X C 4 2.2"s 0.7"~ 5.6' 0.5"' 0.9"' 0.2"' 2.8"' 1.2"' 0.8"' 0.4"' AXBXC 12 1.0"~ 0.7"~ 1.6"' 1 1"' 1.0"' 0.6"' 1.1nV.4ns 1.0"' 0.8"' Residual 378

(b)Variance explained (%) T~me,A 2 2 20 33 24 5 8 7 0 33 7 Location, B 9 0 3 15 5 2 20 13 1 11 Treatment, C 6 0 6 1 1 4 0 0 0 0 Plot, D (BC) 0 10 1 3 2 9 5 2 1 11 8 AXB 11 3 7 9 7 3 2 11 10 15 AXC 6 1 10 0 0 3 0 0 5 1 A X D(BC) 11 7 12 4 14 8 0 5 3 7 BXC 4 0 4 0 0 0 4 0 0 0 AXBXC 7 0 5 7 0 0 1 12 3 0 Residual 2 5 59 20 37 65 63 6 1 39 3 6 5 2

Of the 3 sites, Shark Alley and North tended to were almost twice the density they were in areas support higher densities of molluscs than South. This exposed to fish predation. The densities of E. virgu- trend was most apparent for Atys cylindricus, Umbo- lata were higher at all locations following a large nium guamensis, Fragum sp., and Tellina obtusalis increase in their numbers recorded in July 1987. The (Fig. 1). By contrast, 7: myaformis was consistently treatment effects at North and South both appeared lowest in abundance at Shark Alley. to be due to cage artifacts (Fig. 3). A treatment effect There were no consistent or dramatic effects of the was observed for the bivalve Solemya sp. (Table la, caging treatments of the abundance of molluscs after Fig. 4). At Shark Alley, full cages supported con- cage construction, either at some locations or some sistently greater numbers than the controls over the times (Table la). Atys cylindncus exhibited a 'Treat- last 3 sampling dates. At North and South, both full ment X Time' interaction, which appeared to be due to cages and cage controls tended to increase relative to a difference among treatments detected during the open areas, suggesting a cage effect contributed to summer peaks in abundance (Fig. 2). At these times, the pattern. numbers tended to be higher in full cages. However, Two mollusc species dominant in the stomachs of numbers in cage controls were occasionally higher Lethrinus nebulosus and Diagramma pictum, the than in open areas, suggesting some cage artifacts gastropod Umbonium guamensis, and the bivalve were involved, e.g. dunng November 1986 at North. Fragum sp., showed no sign of significant effects of the The absence of summer peaks in abundance in treatments on their abundances (Table la, Figs. 5 & 6). completely open areas suggests that recruits were Both species' abundances changed seasonally, with preyed upon. highest values in the summer months. Another species for which a treatment effect was In general, although there were some apparent detected was Exotica virgulata (Fig. 3), for which the effects of predators and/or cages, these accounted for analysis exposed a 'Treatment X Location' interaction little of the overall variation in numbers (Table lb). (Table la). Inspection of the graph strongly suggests 'Treatments' (main effects), 'Treatment X Time', and that this was due to an effect of fish predation at 'Treatment X Location' interactions never accounted Shark Alley, which developed dunng the last year of for more than 10 % of the overall variation among the study. Densities of this small bivalve inside cages means and were usually much less. There was con- 180 Mar. Ecol. Prog. Ser. 80: 175-190,1992

Atys cylindricus E. virgulata - 1 North T

N 7E I00 Shark Alley 0 Shark Alley g) CT 1 8

'1 South " 1 South 4 T

May Aug Nov Feb July Dec May May Aug Nov Feb July Dec May 86 86 86 87 87 87 88 86 86 86 87 87 87 88 Fig. 2. Atys cylindricus. Effects of cage treatment (t-. full Fig. 3. Exotica cf. virgulata. Effects of cage treatment (H cage, M cage control, M open control) on temporal full cage, U cage control, M open control) on temporal changes in mean molluscs density (per 0.1 m') at the 3 sam- changes in mean mollusc density (per 0.1 m') at the 3 sam- pling locations. 1986 to 1988. Error bars = standard errors pling locations. 1986 to 1988. Errors bars = standard errors

siderably more spatial and temporal variation in num- Population structure bers occurring than could be attributed to the caging manipulation. The changes in abundance which occurred over the 'Location' accounted for up to 20 % of the variation, 2 yr period were associated with changes in popula- and 'Time' up to 33 %. Also of considerable impor- tion structure, as measured by changes in size- tance was the local-scale variation among 'Plots', frequency distributions. Increases were normally which explained up to 21 % of the variation. associated with a massive influx of individuals in the There was obviously a certain probability that we smaller size classes (loosely termed recruits). The did not detect significant effects of predators on 6 of majority of the species exhibited summer peaks in the species due to type I1 error (i.e. failure to reject a recruitment, sometime between November and false null hypothesis). To examine this possibility, we February [e.g. Umbonium guamensis (Fig. 7) and calculated the amount abundances in full cages Fragum sp. (Fig. 8)]. For the swimming gastropod, would have needed to differ from the 2 control treat- U. guamensis, some juveniles were present during ments (as a percentage of their mean) to have an most of the year, but the greatest numerical inputs 80 % probability of detecting that difference. De- were recorded in November 1986 and December partures of 10 % in Umbonium guamensis, 25 % in 1987 (Fig 7). These discrete cohorts grew rapidly Pupa nitidula and Exotica rhomboides and 35 % in until May but with substantial declines in abundance. Tellina myaformis, T obtusalis and T robusta from They persisted through July and August, but abun- their control means would have been detected with dances were lowest in late winter-spnng, before the at least 80 % probability. next recruitment period. Thus very few adults, if any, Jones et al.: Fish feeding and mollusc population dynamics 181

Solemya Urnbonium guamensis

T T North- - 3 -

2 -

1 -

NE 14- - N Shark Alley 0 l2 - a 10 - 0 8- 2 Um 6- 3 4- 2 c 2- m r" O

6] South 5

May Aug Nov Feb July Dec May May Aug Nov Feb July Dec May 86 86 86 87 87 87 88 86 86 86 87 87 87 89

Fig. 4. Solemya sp. Effects of cage treatment (H full cage, Fig. 5. Umbonium guamensis. Effects of cage treatment (M U cage control. CAopen control) on temporal changes full cage, A-A cage control, M open control) on temporal in mean mollusc density (per 0.1 m2) at the 3 sampling loca- changes in mean mollusc density (per 0.1 m') at the 3 sam- tions, 1986 to 1988. Errors bars = standard errors pling locations, 1986 to 1988. Errors bars = standard errors appear to be present at the next recruitment, sented for both the gastropod Umbonium guamensis suggesting that for the majority of the population the (Fig. 9) and the bivalve Fragum sp. (Fig. 10), the most species is annual. frequently consumed prey. Despite the massive differ- The suggestion of an annual life cycle and a period ences in these pooled size frequencies between of intense adult mortality in late winter applied to seasons, there was no obvious effect of the predator several other species, including the bivalve Fragum exclusion or the cage itself, either at Shark Alley or sp. (Fig. 8). Recruitment was clearly pulsed in North, where these 2 species were most abundant. November-December, and individuals appeared to grow rapidly until May, and persisted to July-August. Feeding pressure and effectiveness of predator After this the cohort essentially disappeared. Other exclusion species that exhibited a seasonal loss of the adult cohort were Pupa nitidula, Exotica cf. virgulata and Feeding pressure, as measured by the densities of Tellina myaformis. All appear to be annual. teleost feeding scars outside cages, varied consider- The temporal changes in size-frequency distribu- ably among locations and times (Table 2, Fig. 11). Fish tions suggested that predation may have an impact on feeding appeared to be consistently higher at Shark population on a seasonal basis. To examine this we Alley, compared to the other 2 locations. Patterns of compared size-frequency distributions for the 3 treat- temporal change in fish feeding pressure were not ments (full cage, cage control, open control) separately consistent from one location to the next (the 'Location for the summer and winter months. These are pre- X Time' interaction). 182 Mar Ecol. Prog. Ser. 80: 175-190, 1992

Fragum sp. 0'3 1May 86 n=90

O3 Aug 86 n=86

0.2 I n

South 3

2

1

0 0'3 1July 87 n=29 May AU~NOV ~eb JUIY Dec M~Y 86 86 86 87 87 87 88 0.2 SamplingPeriod

Fig. 6. Fragum sp. Effects of cage treatment (¥à full cage, AÑ cage control, 0Ñ open control) on temporal changes in mean mollusc density (per 0.1 m2]at the 3 sam- pling locations, 1986 to 1988. Errors bars = standard errors

Full cages were not totally effective in excluding predators, as the caging material was occasionally torn between sampling trips. Prior to repairing these breaches, teleost feeding bites were observed within cages (Fig. 11). However, feeding scar densities dif- fered significantly among 3 different treatments. Full cages had significantly lower feeding bite scar den- sities than the other 2 control treatments, which were not significantly different from each other (Table 2). Hence, cages certainly reduced fish feeding, and cage controls did not appear to modify fish feeding relative to open areas. Since fish feeding inside cages was 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 eliminated for ca 1 mo following each repair, cages Size (1mm intervals) were more effective in excluding fish than Fig. 11 Fig 7. Umbonium guamensis. Temporal changes in the size- suggests. The worst cage-breaching occurred at North frequency distribution of molluscs for pooled locations and between the last 2 sampling dates. However, this did treatments, 1986 to 1988. n = sample size Jones et al.: Fish feeding and mollusc population dynamics 183

not result in the breakdown of any effects of fish exclu- 0'4 1 May 86 n=104 sion (Figs. 3 to 6) except perhaps for Atys cylindricus (Fig. 2). The average time it took artificial feeding scars to disappear was similar for the 3 locations (Table 3). Therefore, bite densities were roughly proportional to bites mA2d-'. This estimate was ca 4X higher at Shark Alley than the other 2 locations. Assuming that bites 0.4 Aug 86 n=96 1 are made randomly in space (which may not be the case), the entire surface layer of the sediments at Shark Alley is being turned over by predators approximately every 300 d. Estimates are considerably longer for the other 2 sites.

Effects of cages on sediment composition

The sediments were dominated by a sand fraction of intermediate grain size (> 125, <500 pm) (Fig. 12). All locations were fairly similar in this regard, although Shark Alley had slightly coarser sediments compared with the other 2 locations. The sediment composition O3] Feb 87 n-311 was stable over the 2 yr study, as indicated by the com- parisons of samples taken at the beginning of the study (May 1986), mid-way through the study (May 1987) and at the end (May 1988). The sediment grain size- frequency distributions were almost identical for cage, cage control and open controls at all stages of the study. 0.5 0.4 ] July 87 "=l47 n DISCUSSION

The aims of this study were to describe patterns in the dynamics of mollusc populations in the sediments near the southern perimeter of One Tree lagoon, and determine the extent to which these patterns are influ- 0.4 1 Dec 87 n=541 enced by predation by large fishes. That is, we were concerned not only with detecting significant effects, but with making some assessment of their biological importance to the prey populations. We examined 10 common species, all consumed by large fishes (Jones et al. 1991), and used a quantitative, predator- exclusion approach to measure the effects of preda- 0.4 May 88 n=181 1 tion, both on overall numbers and population structure. Although the temporal pattern in abundance of each species was somewhat unique, seasonal pat- terns with summer peaks in numbers were common. These patterns occurred in the presence and absence 123 4 5 6 7 8 9 101112131415 of predation for most species at most locations. Some Size Class (1 mm intervals) evidence of predator-induced effects on dynamics were evident for 2 species only (Exoticavirgulata and Fig. 8. Frayurn sp. Temporal changes in the size-frequency distribution of molluscs for pooled locations and treatments, Solemya sp.). For these, full cages supported higher 1986 to 1988. n = sample size numbers than cage controls and open controls toward 184 Mar. Ecol. Prog. Ser. 80: 175-190, 1992

Winter

Shark Alley North 0.4 0.3 - - o.3 open control Open control n=41 0.2 - n=10 -- - 0.1 -

Full cage 0.3 j FUII cage I I - - 0.2 - -- n=13 0.1 -

0.0 , ...... , , . ,

Summer Shark Alley North

Open control - 0.2 - - - n=146 0.2 - open control - - - - n=82 0.1 - 0.1 - - ll,ll.n,n,-,n, ,-,n, . , Cage control Cage control 0.2 - - 0.1 - - n=46 0.1 - in - n, .ll.n,m.n, , ,m. ,n , Full cage Full cage 0.2 - n=92 - n=46

.n.n ,n. . .-. . . 0.0

Size Classes (1mm intervals)

Fig. 9. Umbonjurnguarnensis. Summer and winter differences in size-frequency distributions of molluscs in full cage, cage control and open control treatments at Shark Alley and North. (Note: Values were too small to plot size-frequency distributions for South.) n = sample size

the end of the experiment. Other treatment effects either of the 2 key teleost predators, Lethrinus nebu- that occurred at some times were more likely to be losus or Diagramma pjctum, in One Tree lagoon. L. due to cages rather than predators (e,g.Atys cylindri- nebulosus consumes mainly Fragum sp. and Umbo- cus and Tellina robusta). There was no general effect nium guarnensis and D. pictum prefers U.guamensis of predation on dynamics and no apparent seasonal and Telllna robusta (Jones et al. 1991). Both Exotjca change in fish feeding intensity (as measured by rhornboides and Solemya sp. are consumed, but in low feeding scars) which could account for the winter numerical proportions. Neither do the impacts corre- decline in numbers. spond to the abundance of the prey species; Exotica The species affected do not correspond in any way to vjrgulata was the most abundant mollusc and Solernya their proportional representation in the stomachs of sp. was one of the least abundant. Jones et al. Fish feeding and mollusc population dynamics 185

Winter Shark Alley North

0.3 Cage control - :. n=39 0.2 - - - 0.1 - ...... ,...... n. ,

Summer Shark Alley North 0.3 - 0.3 - Open control Open control 0.2 - - - n=198 0.2 h324 0.1 - 0.1

- Cage control 0.2 - - 7 n=170 0.1 - n,ll,n,n,n.,R,n,m,-, , Full cage n=165 0.2 0.1 0.1

0.0 123 4 5 6 7 8 9101112131415 123 4 5 6 7 8 9 101112131415

Size Classes(1 mm intervals)

Fig. 10. Fragum sp. Summer and winter differences in size-frequency distributions of molluscs in full cage, cage control and open control treatments at Shark Alley and North. (Note: Values were too small to plot size-frequency distributions for South.) n = sample size

Among the 3 locations examined, the greatest al. 1991). Therefore, it is the zone in which predators feeding intensity occurred at Shark Alley. This may are most likely to have an impact. The feeding inten- be because it is a natural corridor through which sity at Shark Alley is the highest recorded (cf. Jones large fish appear to move and was near an aggrega- et al. 1991), which would suggest that the small tion site for Diagramma pictum (Jones & Ferrell pers. effect here (2 species out of 10) is the largest that is obs.). The greater predation pressure here may likely to occur. There is a clear need for information explain the fact that this was the only location to on spatial and temporal changes in predator abund- exhibit an exclusion effect. Fish feeding is generally ance and feeding pressure, when interpreting these more intense around the perimeter zone of the experiments (Choat 1982, St. John et al. 1989, Jones lagoon where mollusc densities are higher (Jones et et al. 1991). 186 Mar. Ecol. Prog. Ser. 80: 175-190, 1992

Table 2. Analys~sof variance for the effects of exclusion treat- ments and their controls on the density of teleost feeding North scars. Variance for treatment effects (italics) is partitioned among controls and between fish exclusion treatments vs controls ('significant at 0.05 level; ''significant at 0.01 level; ns: not significant)

Factor df SS MS F

Time, A 3 21.1 7.1 3.3"' Location, B 2 36.4 18.2 12.4" Treatment, C 2 30.9 15.4 7.0' E Jan 87 July 87 Dec 87 May 88 L Among controls 1 0.3 Treatmentvs controls 1 30.6 SharkAlley Plot, D (BC) 9 13.1 1.5 9.2" A X B 6 13.0 2.2 4.3" AXC 6 9.0 1.5 3.1' Time among controls 3 4.5 Time treatment vs control 3 4.5 A X D(BC) 27 13.7 0.5 3.2- B X C 4 8.8 2.2 1.5ns AXBXC 12 5.8 0.5 1.0"' Residual 360 57.3 0.16

Jan 87 July 87 Dec 87 May 88

There are few other studies of tropical soft-sedi- South - ment invertebrate populations, in which the impor- tance of predation has been evaluated expenmen- tally. Keller (1983) found an effect of fish predators on the abundance of the urchins Tripneustes ventri- cosus and Lytechinus vanegatus at only 1 of 2 sites examined in the lagoon of Discovery Bay, Jamaica. In a previous study, we found a significant effect of fish- exclusion treatments on 3 of 9 molluscs found on the shallow sand flat of One Tree lagoon (Jones et al. Jan 87 July 87 Dec 87 May 88 1988). However, we could not exclude the possibility that disturbance and/or interactions among molluscs Fig. 11. Temporal changes in mean densities of teleost contributed to the patterns. feeding scars in full cage (H), cage control (A-A) and open control (M) treatments at North, Shark Alley and The predation effects detected in the present experi- South. Error bars = standard errors ment were clearly location- and time-specific. They were also small in magnitude, relative to the observed Table 3. Estimates of density of fish feeding scars and rate at variation in numbers in space and time. Location and which artificially made scars became unrecognisable. These time factors accounted for considerably more variation are standardised to a daily estimate of feeding scars which in than treatments (averages: 'Location', 8 %; 'Time', turn allow an estimate of the time to turn over the top 5 cm of sediment. The area of a single bite was estimated to be a 16 %; 'Treatment',

Fig 12 Sed~mentgraln s~ze-frequencydlslrlbut~ons In open control, cage control and full cage treatments (whlte, hatched and black bars respec- tlvely) at the beglnnlng of the exper~ment(May 1986),m~d-way through (July 1987) and at the end of the exper~rnent(May 1988),at the 3 locations - North, Shark Alley and South S~zecategories correspond to unlts of 1 + 188 Mar. Ecol. Prog. Ser. 80: 175-190. 1992

life cycles and the maximum feeding rates observed. There is a suite of other factors which could account At Shark Alley, we conservatively estimate that pred- for the dramatic loss of adults during winter. During ators are able to completely turn over the sediments in July 1987, many of the largest Fragum sp. and some the course of a year. If they were 100 % efficient in other species were found dead or dying on the surface extracting molluscs from the sediment, they would be of the sand, at densities of 2 to 3 per 10 m2 (Ferrell & potentially capable of removing an entire cohort. We Jones pers. obs.). These had an extreme gape and assume that the majority of molluscs do not have a would not close their valves when prodded. We also refuge in depth, as most are found in the top 5 cm observed many dead shells with tissue still inside, indi- (Jones et al. 1988). Without data on actual consumption cating death was recent and not due to fish. This rates of each species, it is difficult to say what pro- pattern of mortality may simply reflect an annual, portion of the recruits is eventually consumed by pred- semelparous life history. However, cold temperatures ators. This approach has been used to estimate the may be involved, since both high and low temper- potential impact of fish predators on soft-sediment atures are known to affect mortality rates in molluscs prey (e.g. Alheit 1981, Bennett & Branch 1990), and in (Chitramvong et al. 1981, Cranford et al. 1985, the future may assist in the interpretation of caging Vareille-More1 1985). Epibenthic predators, such as experiments. small fish and predatory gastropods, were not exam- If the intense feeding pressure does have an impor- ined. Since these have been found important in other tant effect on prey numbers, a number of factors may systems (Peterson 1979), they do need to considered in hdve contributed to our faiiure to detect this. Failure future tropicai studies. to detect a significant effect of any factor (to reject the It was hoped that the large mesh size and cage size null hypothesis of no effect) may be due to the low would reduce cage artifacts which developed over the power of an experiment caused by small sample size course of the pilot experiment (Jones et al. 1988). The or large sampling variability (Cohen 1988, Peterman effects of cages on sediment strilctijire obseived in 1990). However, in this case treatment effects were some experiments (e.g. Hulberg & Oliver 1980, Jones detected for a number of specles. One has to assume et al. 1988) did not occur in this instance. Some other there was sufficient power to detect effects of this mechanism must have accounted for the effect of magnitude for the others; indeed power analysis for cages on Atys cylindricus, Fragum sp. and Solemya the main treatment effects indicated it is unlikely sp. The problem of fish breaching the full cages was effects large enough to contribute to the major clearly a design fault. However, we had clear patterns of change in mean abundance escaped evidence that although fish did enter some of these detection. cages toward the end of a between-sampling period, The most plausible alternative explanation for the there was significantly less feeding than in both types lack of detected predation effects lies in the potential of control areas. mobility of the prey organisms. If these molluscs were In conclusion, our experiment does not support a so mobile as to move in and out of caged areas during model in which fish predation has a major effect on the normal movements, predation effects would have dynamics of mollusc populations in One Tree lagoon. been swamped and averaged over a scale that the Although some statistically significant effects were experiment could not detect (Raffaelli & Milne 1987, detected, these were small relative to the patterns Frid 1989). It has been suggested that mobility is an observed. There are a number of alternative causal important factor in structuring benthic communities explanations, such as physical factors and epibenthic (Posey 1987). Few studies have examined the move- predators, which need to be considered. In future ments of prey in conjunction with predator- reviews this study must not become a data point sup- exclusion experiments, and this is particularly difficult porting the notion that predation pressure is higher in for the non-surface-dwelling molluscs we studied the tropics. We have considerable reservations about here. Movements may be highest for gastropods such making such comparisons based solely on the frequen- as Umbonium guamensis, which can swim several cies at which significant effects are detected along a centimeters when disturbed. However, a factor sup- latitudinal gradient. In each case, the contribution of porting our conclusion that predation is unimportant different types of predators to the overall population is the cage size. The 25 m2 area is much greater than changes must be quantified. cages which have detected effects of predation or disturbance on other soft substrata (e.g. Van Blaricom 1982 [0.75 m2],Federle et al. 1983 [4 m2], Keller 1983 Acknowledgements. Special thanks to C. Hayward, L. Howitt, U. Kaly, I. Martin, J. Martin, M. Milicich, M. Norman [4 m2], Quammen 1984 m2], Raffaelli & Milne [l and G. Skllleter for the much needed f~eldassistance. Com- 1987 (4 m2], Jones et al. 1988 [l6 m2], Martin et al. ments on the manuscript by N. Andrew. R. Cole and C. Syms 1989 [l m2]). and 2 anonymous reviewers were much appreciated. The Jones et al. Fish feeding and mollusc population dynamics 189

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This article waspresented by A. J. Underwood, Sydney, Manuscript first received: April 24, 1991 Australia Revised vers~onaccepted: December 19,1991