L
Journal of Experimental Marine Biology and Ecology, 241 (1999) 15–29
Predation by fish on assemblages of intertidal epibiota:
effects of predator size and patch size
*
S.D. Connell , M.J. Anderson
Centre for Research on Ecological Impacts of Coastal Cities, Marine Ecology Laboratories A11,
University of Sydney, Sydney N.S.W. 2006, Australia
Received 24 August 1998; received in revised form 12 April 1999; accepted 28 April 1999
Abstract
We tested the hypothesis that effects of predation by fish on epibiota are independent of the size of fish and the area foraged. We used cages with different sizes of mesh to exclude fish of different sizes. Sizes of mesh were chosen following observations that there were small (,200 mm TL) and large (.200 mm TL) predatory fish at the study site. Predation by fish was intense on oysters and directly or indirectly reduced the density of the gastropod, Bembicium auratum. The cover of algae was positively affected by predation, possibly because predation on oysters created more space for algae. Predation by small fish (toadfish) was intense, but the effects of large fish were negligible. Predation was, however, independent of the sizes of experimental panels (i.e. area
foraged) over the range examined (535, 10310, 20320 cm). Our results highlight the
importance of doing experiments to test hypotheses derived from known aspects of the biology of the predators and prey being studied. 1999 Elsevier Science B.V. All rights reserved.
Keywords: Assemblage; Fouling; Patch size; Multivariate; Experiment
1. Introduction
The effect of predators on the structure of ecological assemblages has been studied in many marine habitats (reviews: Paine, 1977; Choat, 1982; Hixon, 1997). Fish are major predators, particularly for epibiota on hard substrata (reviews: Choat, 1982; Hixon, 1997). Despite this, considerable variability has been detected in the effect of fish predation on epibiota (cf. Sutherland and Karlson, 1977; Russ, 1980; Choat and Kingett,
*Corresponding author. Present address: Department of Environmental Biology, University of Adelaide, South Australia 5005, Australia. Tel.: 161-8-8303-6125; fax: 161-8-8303-5576.
E-mail address: [email protected] (S.D. Connell)
1982; Menge et al., 1985). To date, little attempt has been made to explain this variability and most work has focused on variation of predation by fish on substrata of different topographic complexity (e.g. Menge and Sutherland, 1976; Russ, 1980; Menge et al., 1985).
Assemblages of predatory fish are characterised by extreme spatial and temporal variability in composition and abundance (Williams and Hatcher, 1983; Choat and Ayling, 1987; Connell and Kingsford, 1998) and diet (Hiatt and Strasburg, 1960; Parrish, 1987; Connell, 1998a). Hence, the intensity of predation and its effects on composition of benthic assemblages may be strongly related to the types of predators present. Despite this, studies of predation by fish on invertebrates have typically not attempted to differentiate among different predators (but see Ayling, 1981; Choat and Kingett, 1982). Rather, they have been designed only to test the overall effects of fish of whatever kinds happen to be present. If the composition of predators leads to predictable changes in the structure of benthic assemblages, then such knowledge may provide a basis for predicting where, when and how predation is likely to be important.
Variation in the intensity of predation may also be explained by the response of predators to the patchiness of their prey. Many predators, including fish, actively search for their prey, so it can be predicted that predation will not be uniformly distributed among patches of varying size (Charnov, 1976). Several types of predators have been shown to respond differently to different sized patches of prey. In terrestrial habitats, birds prefer to feed from larger flowers (e.g. Brody and Mitchell, 1997). In marine habitats, birds and fish feed more intensely on the siphons of clams where the prey occur in greater densities (Whitlatch et al., 1997) and large predatory fish kill more juvenile fish that occur in larger schools (Connell, 1998b). Although it has been recognised that size of patch affects the colonisation and development of epibiotic assemblages (see review by Connell and Keough, 1985), no experiments have tested the hypothesis that the consequences of predation vary among different sized patches of epibiota.
The hypotheses tested here were that assemblages of epibiota (i) differ when exposed to different sizes of predatory fish and (ii) are more affected by predation on larger patches of habitat. These hypotheses were tested on wooden structures used for farming oysters (oyster leases) in the intertidal zone of an estuary of New South Wales, Australia where (i) it is known that the size of patches influences the early stages of development of epibiotic assemblages and (ii) observations suggest that sessile invertebrates are eaten by fish (Anderson, 1998). Oyster leases represent a major coastal habitat of New South Wales, occupying |4700 hectares of intertidal habitat in 30 major bays and estuaries.
2. Methods
2.1. Study area and experimental treatments
predatory fish were observed: (i) small elongate toadfish, Tetractenos spp. (generally
,200 mm TL; mean girth518.7 mm, range of girth 11–26 mm: n520) and (ii) large and deep-bodied fish, Monacanthus chinensis (Osbeck) and Acanthopagrus butcheri (Munro) (generally .200 mm TL, girth .50 mm). Other large predatory fish in local estuaries include the families Labridae, Scorpaenidae, Sparidae, Carangidae and Monocanthidae.
The experiments were done using intertidal wooden structures (Fig. 1: full description in Anderson and Underwood, 1997). The structures consisted of two parallel beams (5 cm32.5 cm thick and several metres long) 1 m apart. The beams were supported by several vertical posts embedded in the mud so that they were level with a tidal height of |0.5 m above Low Water Spring Tide. Panels of three different sizes (treatments) were created from 9-mm marine plywood: 5 cm35 cm (small), 10 cm310 cm (medium) and 20 cm320 cm (large). Two panels of the same size were attached to tar-covered sticks (2.5 cm32.5 cm31.8 m) with stainless-steel screws. Sticks were fastened across the beams, with surfaces of panels face down.
Fish were excluded (galvanised mesh) or allowed to feed from panels in three ‘cage’ treatments (Fig. 1): (1) open panels without cages that allowed access to all fish, (2) panels in full cages with large mesh (50 mm350 mm holes) allowing access to
Tetractenos spp. but excluding large, deep-bodied fish (.200 mm TL: see above) and (3) panels in full cages with small mesh (12.5 mm 312.5 mm holes) that prevented access to all fish except very small juveniles and families such as Blenniidae and Gobiidae, which are not normally predators on sessile epibiota. Potential artefacts due to the cages themselves were examined by comparing open panels to two ‘control’
treatments (1) panels in half cages of large mesh and (2) panels in half cages of small mesh. Partial cages were similar to full cages but the lower half of the cage was removed to allow access to any fish (Fig. 1c), while controlling for other influences on water-flow, light, sediments, etc., due to the presence of a cage. For each of the three sizes of panel there were three sticks in each treatment, yielding a total of 45 sticks and 90 panels. Sticks of different treatments were attached to the beams in a haphazard order.
After 3.5 months (1 October–15 January), each panel was collected at low tide, put into a separate plastic bag and taken to the laboratory for examination under a dissecting microscope where the abundances of benthic invertebrates were estimated. No attempt was made to identify species that could not be clearly seen at 1003 magnification or less. These included harpacticoid copepods, which were counted but lumped into this taxon, foraminifera and other microrganisms. Taxa which were not possible to count were recorded as either present or absent, including algae (except Ulvaria oxysperma
¨
(Kutzing)), foraminifera, the wood-boring bivalve Bankia australis (Calman) and the bryozoans Tubulipora pulchra (MacGillivray) and Bugula neritina (Linnaeus). Total percentage cover of algae was estimated by counting the number of times algae occurred under a set of uniformly spaced points; 25 points were used for 5 cm35 cm and 10 cm310 cm panels and 100 points for 20 cm320 cm panels.
2.2. Multivariate analyses
2
Abundance data were standardised per 100 cm (the size of medium-sized panels), to compare assemblages on panels of different sizes for all multivariate and univariate tests. Multivariate analyses were done for the 30 taxa identified. Data were fourth-root transformed and the Bray–Curtis measure (Bray and Curtis, 1957) was used to calculate dissimilarities among replicates. A new method, distance-based redundancy analysis (db-RDA) (Legendre and Anderson, 1999) was used to test for the presence of a multivariate interaction between the factors cage and panel size. This method is a non-parametric analysis of variance based on multivariate dissimilarities. It has several steps. First, principal coordinate analysis was done on the matrix of dissimilarities among replicates. This preserves, as far as possible, the Bray–Curtis dissimilarities among replicates, but places replicates into a Euclidean (additive) space so that analysis-of-variance (an additive model) can be applied. The multivariate ANOVA was done using redundancy analysis (RDA) on the principal coordinates to test particular terms in the model (i.e. the cage3panel size interaction, and cage and panel size main
[
effects). Multivariate F-ratios (symbolised by F ; Legendre and Anderson, 1999) were calculated and probabilities associated with statistical tests were obtained by permuta-tion. Residuals of the reduced model were permuted (rather than raw data) to test the interaction term and each main effect individually (ter Braak, 1992; Anderson and Legendre, 1999).
To visualise multivariate patterns, non-metric multi-dimensional scaling (nMDS) ordinations were done on the centroids (averages of the principle coordinates for each stick; n52 panels per stick). Ordinations were done using the PRIMER v4.0 computer
Anderson and P. Legendre, University of Montreal) and RDAs with appropriate permutation tests were done using CANOCOE (courtesy of C.J.F. ter Braak).
2.3. Univariate tests
Univariate tests of hypotheses for individual taxa were done using multi-factorial ANOVA (e.g. Underwood, 1997). The first analysis was a comparison of partial cages and open panels, to test for artefacts due to cages (Factor5partial cages, fixed with three levels: small mesh, large mesh, open panels). In the absence of any significant interpretable caging artefacts, a second analysis compared panels in full cages with open panels, to test for effects of exclusion of fish (Factor5cage, fixed with three levels: small mesh, large mesh, open panels). For each of these sets of analyses, the caging factor was crossed with the factor of panel size (three levels: 5 cm35 cm, 10 cm310 cm and 20 cm320 cm). The design was balanced: for each combination of treatments there were three sticks (Factor5sticks, nested in cage3panel size) and n52 replicate panels per stick. Univariate ANOVAs and Cochran’s tests were done using GMAV5
(courtesy of A.J. Underwood and M.G. Chapman).
3. Results
3.1. Composition of assemblages
Assemblages on panels were composed primarily of juvenile oysters (Saccostrea
commercialis (Iredale & Roughley) and Crassostrea gigas (Thunberg)), bryozoans
(Watersipora arcuata (Banta), Bugula neritina and Tubulipora pulchra), barnacles (Hexaminius sp., Elminius covertus Foster, and Balanus spp.), calcareous tubeworms (Spirorbis sp. and Galeolaria caespitosa (Savigny)), recently settled gastropods
(Nodilit-torina acutispira Smith and Bembicium auratum (Quoy and Gaimard)), and ephemeral
¨ species of algae (Oscillatoria sp., Rhizoclonium sp., Enteromorpha prolifera (Muller),
Ulvaria oxysperma and Caloglossa leprieurii (Montagne)).
3.2. Artefacts due to cages
Analyses did not detect any artefacts due to cages. Although assemblages differed [
among open panels and panels under partial cages (F2, 4551.580; P,0.05), pairwise comparisons did not reveal consistent significant differences among the three treatments (P.0.05). Similarly, preliminary univariate analyses did not detect significant effects of partial cages for any taxon (P.0.05) except oysters. Densities of oysters differed among open panels and cage controls (P,0.05), but SNK tests did not reveal consistent significant differences among the three treatments. The density of oysters was smaller on open panels than on panels inside partial cages made of small mesh (SNK test,
Fig. 2. Two-factor nMDS plot (Clarke, 1993) comparing centroids of assemblages on panels open to predation (symbols not circled) to those protected from predation with small mesh (symbols inside circles) for each patch size: 5 cm35 cm (5), 10 cm310 cm (10) and 20 cm320 cm (20). The values for each centroid (mean of
n52 panels per stick) were calculated from principle coordinates of Bray–Curtis dissimilarities.
partial cages made of small or large mesh. Importantly, the effect of small cages was greater than the effect of small partial cages (Fig. 2). Assuming partial cages provide an adequate test of artefacts of cages we conclude that cage artefacts were minimal and that the effects of excluding fish could be interpreted.
3.3. Effect of cages
Prior to the experiment, we predicted that prey on smaller panels would be less affected by predation than prey on larger panels. The two-factor nMDS plot of centroids for each stick (calculated from the principal coordinates of Bray–Curtis dissimilarities) indicated that multivariate differences in the structure of assemblages between panels open to predation (open panels) and panels most protected from predation (cages with small mesh) were similar in magnitude and direction for each size of panel (Fig. 2). That is, centroids representing assemblages on panels inside cages (circles) are generally located in the bottom region of the nMDS plot and their separation from centroids representing assemblages on panels open to predation (not circled) is similar across the range of panel sizes. Importantly, no multivariate interaction was detected between the factors cage and panel size (Table 1a).
The effect of predation was restricted to small predatory fish. Assemblages on panels open to predation by all fish (open panels) differed from those inside cages with small mesh (no predation by small or large fish), but not from cages with large mesh (predation by small fish only, Table 1a and b).
Table 1
2
(a) Two-factor distance-based redundancy analysis (db-RDA) on multivariate data (standardised per 100 cm unit area) examining effects of cage treatments (large mesh vs. small mesh vs. open panels) and panel size (5 cm35 cm vs. 10 cm310 cm vs. 20 cm320 cm) on assemblages of epibenthic organisms for full cages. See
[ [
text for explanation of MS and F . (b) Pairwise comparisons of main effects among sizes of mesh and panel.
[ [
The multivariate pair-wise statistic t 5œF
[ [
df MS F P
(a) Source of variation
Cage 2 0.059 1.86 0.001*
Panel size 2 0.158 4.99 0.001*
Cage3panel size 4 0.070 1.10 0.157
Residual 45 0.713
Total 53 1.000
[
(b) Pairwise comparisons t P
Cage Large mesh vs. small mesh 1.345 0.006*
Large mesh vs. open panel 1.073 0.209
Small mesh vs. open panel 1.771 0.001*
Panel size 5 cm35 cm vs. 10 cm310 cm 2.081 0.001*
5 cm35 cm vs. 20 cm320 cm 2.944 0.001*
10 cm310 cm vs. 20 cm320 cm 2.312 0.001*
unaffected by cages, except oysters, algae and a herbivorous gastropod, Bembicium
auratum (Table 2). Oysters were significantly more dense on panels inside cages with
small mesh than on other panels (Fig. 3a, Table 2a). No differences in densities of oysters were detected between panels open to predation and panels protected by cages with large mesh. The density of Bembicium auratum was greater on panels inside cages than on open panels, but did not differ between panels inside cages made from small or large mesh (Fig. 3b, Table 2a). Percentage cover of algae was greatest on open panels, significantly less extensive on panels protected by large mesh and the least extensive on panels protected by small mesh (Fig. 3c, Table 2a). The only other possible effect of predators was on the barnacle Hexaminius sp., which occurred with greater frequency on panels inside cages with small mesh than on panels in cages with large mesh (Table 3:
2
x 510.5, df52, P,0.05) but this species did not recruit in great abundance during this experiment. As found in multivariate analyses, the magnitude of cage effects did not vary among panels of different size; the cage3panel size interaction was not statistically significant for any univariate taxon (P.0.05, Table 2).
We identified the species which primarily contributed to multivariate differences among the caging treatments. This was done by successively omitting taxa shown by univariate analyses to be most affected by cages (Table 2a) and repeating the multivariate analysis until no significant multivariate differences were detected among caging treatments. Oysters were most affected by cages (Table 2a; ANOVA: F2, 185
23.45, P,0.001) but after oysters were omitted from the multivariate analysis, [
significant multivariate differences remained (RDA: F2, 4551.244, P,0.05). Cages had a much smaller effect on the percentage cover of algae (Table 2a; ANOVA:
Table 2
Summary of univariate analyses of variance and a posteriori SNK tests for effects of mesh size (large mesh vs. small mesh vs. open panels) and panel size (5 cm35 cm vs. 10 cm310 cm vs. 20 cm320 cm) on
2 a
assemblages of epibenthic organisms for full cages (standardised per 100 cm unit area)
b Cages Panel size C3P Sticks SNK results
(a) Taxa affected by cages
Bivalves Oysters 23.45*** 0.78ns 1.31ns 1.10ns O5L,S c,d,e
Gastropods Bembicium auratum 5.04* 6.37* 0.30ns 1.52ns O,L5S 20,10 f
Algae Total % cover 6.22** 0.67ns 1.20ns 1.92ns O.L.S
(b) Taxa unaffected by cages
Bivalve Lasaea australis 0.89ns 2.42ns 0.99ns 6.34*** c
Gastropod Nodilittorina acutispira 1.67ns 0.85ns 0.77ns 2.59* c,d
Polychaetes Spirorbis sp. 0.44ns 0.02ns 0.47ns 2.34ns c,d,e
Galeolaria caespitosa 0.29ns 18.49** 1.61ns 2.26ns 20.10 Alga Ulvaria oxysperma 2.05ns 9.75** 0.50ns 0.99ns 20.10.5 Other taxa Copepods 1.58ns 1.73ns 0.92ns 2.46*
d
Insect larvae 0.01ns 16.67*** 0.60ns 1.64ns 20,1055 Total no. of taxa 1.17ns 61.58*** 1.43ns 1.30ns 20.10.5
a
For each analysis, there were n52 panels on each of three sticks in each combination of (333) treatments. ns5P.0.05; *P,0.05; **P,0.01; ***P,0.001.
b
555 cm35 cm, 10510 cm310 cm, 20520 cm320 cm; S, small mesh; L, large mesh; O, open panels; inequalities indicate significant differences with P,0.05, equalities indicate differences are not significant with P.0.05.
c
For these variables, patches measuring 5 cm35 cm were not included in the analysis, due to lack of numbers on these sizes of panels.
d
Variable was transformed to y9 5log ( ye 11).
e
Variances were heterogeneous. Non-significant results are interpretable. Some caution should be used in interpreting significant results.
f 21
Variable was transformed to y9 5sin (œy).
P,0.05). A significant multivariate effect remained after percentage cover of algae and [
oysters were removed from the analysis (RDA: F2, 4551.243, P,0.05), but not after[ the removal of B. auratum, percentage cover of algae and oysters (RDA: F2, 4551.203,
P.0.05). These three variables were, thus, responsible for causing multivariate differences in assemblages among caging treatments; cages did not affect the com-position or relative abundances of other species in the assemblage. A two-factor nMDS plot of the remaining taxa, after removing these three variables, also showed that multivariate effects of cages were no longer apparent (Fig. 4, symbols representing panels inside cages (circled) are well-mixed with those representing open panels (not circled)).
3.4. Effect of sizes of panels
2
Fig. 3. Mean abundance (per 100 cm6S.E.) versus treatments of fish predation (S, full cage, small mesh; L, full cage, large mesh; PS, partial cage, small mesh; PL, partial cage, large mesh; O, open) and for three different sizes of panel.
Fig. 4. Two-factor nMDS plot comparing centroids of assemblages on panels open to predation (symbols not circled) and protected from predation (symbols inside circles) after abundances of oysters, total percentage cover of algae and abundances of the gastropod Bembicium auratum were removed from analyses. See the legend of Fig. 2 for explanation of symbols.
a positive effect on the densities of the alga Ulvaria oxysperma and the tubeworm
Galeolaria caespitosa, but a negative effect on the densities of insect larvae and Bembicium auratum (Table 2).
Table 3
Summary of frequencies of occurrence of taxa across (a) three panel sizes and (b) five treatments testing the effects of predation: S, L, O, PS, PL (as described in Fig. 3)
a b
Taxa (a) Patch size (b) Cage treatments
535 10310 20320 S L O PS PL
Bivalves Bankia australis 0 1 12 2 0 4 3 4
Xenostrobus sp. 0 0 6 1 1 1 3 0
Bryozoa Watersipora arcuata 0 8 20 7 5 4 6 6
Bugula neritina 4 7 23 5 6 5 9 9
Tubulipora pulchra 7 6 23 8 5 7 10 6
Barnacles Hexaminius sp. 5 2 10 9 1 3 4 0
Elminius covertus 2 0 4 2 1 1 2 0
Balanus spp. 3 3 8 3 3 2 3 3
Algae Rhizoclonium sp. 30 30 30 18 18 18 18 18
Oscillatoria sp. 26 29 30 17 16 18 17 17
Enteromorpha prolifera 24 30 30 18 16 17 17 16
Caloglossa leprieurii 20 25 30 15 16 15 12 17
Other taxa foraminifera 1 14 9 4 4 7 4 5
mites 7 7 12 5 7 2 5 7
a
Frequencies out of 30 possible patches (5 treatments32 panels33 sticks).
b
4. Discussion
4.1. Effect of size of fish
The first result of this experiment was that predation on panels varied according to the type of fish accessing panels. Small elongate fish (essentially toadfish) rather than large deep-bodied fish caused changes in the structure of epibiotic assemblages. Their effect was largely on oysters. There is substantial evidence demonstrating the effects of toadfish on the mortality and abundance of oysters in these experiments. In particular, where an oyster had been removed due to predation by fish, the lower valve of the animal was still left attached to the panel, so that mortality could be estimated as a direct effect (Anderson and Connell, in press). Such direct effects of predation were not possible to observe for the percentage cover of algae and the abundances of the gastropod Bembicium auratum. As found in previous work (Anderson and Underwood, 1997) the cover of algae was negatively correlated with the abundance of oysters (r5 20.32, t525 22.44, P,0.01, one-tailed test) and the abundance of B. auratum was positively correlated with the abundance of oysters (r50.50, t5254.13, P,0.001, one-tailed test). It is, therefore, likely that removal of oysters by fish indirectly caused decreases in recruitment of Bembicium and increases in the growth of algae. Further manipulative experiments would be required to test for such indirect effects; fish could have preyed on gastropods.
Assemblages on patches protected from predation by toadfish (cages with small mesh) differed from those on patches primarily accessible to toadfish (cages with large mesh) and all fish including toadfish (open patches). The lack of difference between patches open to predation by all fish and patches open to predation only by toadfish indicated that large deep-bodied fish made little difference. Oysters are found in the guts of toadfish (D. Booth, unpublished data) and Tetractenos spp. is the only fish in estuaries in New South Wales that would be able to remove large oysters from panels inside cages with large mesh.
Because one type of predator was primarily responsible for alterations to assemblages, the design of future experiments and predictions of where predation is likely to be important can be improved. The specific types of fish that were manipulated were based on observations of the sizes of predators at the study site (see Section 2). Two previous studies have tested experimentally the influences of specific types of fish on epibiota (Ayling, 1981; Choat and Kingett, 1982). Particular predators were excluded by a horizontal shield, which prevented predation by fish that orientate vertically to feed. These simple but ingenious experiments were based on information of the feeding behaviour of the fish and highlight the importance of doing experiments to test hypotheses derived from known aspects of the biology of the predators and prey being studied.
important predators of epibiota. Most studies that have detected predation by fish have used one size of mesh which excludes both small and large predatory fish alike (range of mesh sizes57.5–18.0 mm, average¯11 mm; Foster, 1975; Russ, 1980; Keough, 1984; Menge et al., 1985, Breitberg, 1985; Sala, 1997). Without information on the relative impacts of small versus large predatory fish, previous studies may have undervalued the importance of small predatory fish and overvalued that of large predatory fish.
4.2. Artefacts as alternative explanations of caging effects
We did not detect consistent artefacts when comparing open panels with cage controls, but the adequacy of partial cages in detecting artefacts can be problematic (Wilson, 1991; Connell, 1997) and some discussion of potential artefacts is needed (Peterson and Black, 1994). We are confident that small predatory fish (toadfish) are responsible for differences in the structure of assemblages of epibiota (particularly oysters) among caging treatments. If cages and not predators enhanced the abundance of oysters, we would not have observed equal densities of oysters between open panels and panels inside cages with large mesh. Moreover, there is substantial evidence demonstrating that toadfish cause heavy mortality and alter subsequent abundances of oysters in these experiments (Anderson and Connell, in press).
The only other taxa affected by cages were algae, the snail Bembicium auratum and possibly Hexaminius sp. Shading by cages was unlikely to have reduced the cover of algae inside cages; patches were already shaded in their face down position. The abundance of B. auratum, a mobile and herbivorous gastropod, was negatively correlated with algal cover. Hence, artefacts associated with food availability were unlikely. Demonstrable artefacts due to cages tend to cause barnacles to occur in fewer numbers inside cages (Marshall et al., 1980; Schmidt and Warner, 1984), opposite to the results we obtained for Hexaminius sp. In addition, the partial cages in our experimental design would have controlled for such artefacts as shading and the presence of mesh near panels. Yet, none of the analyses designed to detect caging artefacts, through the use of partial cages, gave any significant results. It is, therefore, reasonable to conclude that artefacts of cages were minimal.
4.3. Effect of size of patch
It has long been recognised that predators are unlikely to respond in a similar way to different sized patches of food (e.g. Charnov, 1976; Hodges, 1985). There has been recent recognition that predatory fish are highly likely to respond differently to changes in prey availability (Werner et al., 1983; Kingsford, 1992; Wildhaber and Crowder, 1995). Moreover, prey that occur in larger aggregations have been shown to suffer greater rates of fish predation (Connell, 1998b) suggesting that smaller aggregations of prey and patches of habitat may offer a refuge from predation (e.g. Keough, 1984).
size alone had a large effect on assemblage structure; such effects have been well documented in this (Anderson, 1998) and other assemblages of epibiota (see review in Connell and Keough, 1985). Note, however, that densities of the primary prey (oysters) did not differ on different-sized panels (Table 2a). Investigation of the cause for differences in assemblages on different patches has primarily concerned the processes of colonisation and competition (Connell and Keough, 1985) rather than predation. Consistent with the results obtained here and the suggestion that predators are more likely to respond to prey in larger numbers, we predict that predation would be greater on prey in greater densities (i.e. density-dependent predation) but not on larger patches of prey whose density is similar to smaller patches (as generally the case in this study). Further experimental studies are required to test this prediction.
5. Conclusion
In conclusion, small (toadfish) rather than large fish were the main predators of assemblages of epibiota. Despite recent suggestions that fish are more likely to respond to larger numbers of prey, we rejected the hypothesis that predation on assemblages of intertidal epibiota is greater in larger patches. A new multivariate procedure allowed us to test this hypothesis, a test which generally has not been possible in previous studies of potential multivariate interactions. The experimental structures (oyster leases) would have almost certainly have attracted fish and enhanced rates of predation, possibly by orders of magnitude above that on barren mudflats. Hence, it is worth noting that the intensity of predation reported here may have little generality to other intertidal habitats within estuaries. Finally, the formulation of hypotheses and insights gained from this experiment were dependent on preliminary information gathered on the type and sizes of the predators. We suggest, therefore, that preliminary information on the biology of the predators can and should assist in planning and interpretation of more meaningful experiments on effects of predation.
Acknowledgements
This study was supported by a University of Sydney U2000 post-doctoral fellowship to M.J. Anderson and funds from the Centre for Research on Ecological Impacts of Coastal Cities. We gratefully acknowledge assistance in the field from T. Glasby, some construction of cages by M. Haddon, use of a seine net from B. Gillanders and logistic support from G. Housefield, T. Davies and S. Heislers. This paper benefited from discussions with M. Beck, M. Lincoln-Smith and A.J. Underwood.
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