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.D. Connell, M.J. Anderson J. Exp. Mar. Biol. Ecol. 241 1999 15 –29
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 The study was done from 1 October 1997 to 15 January 1998 spring–summer in
Salamander Bay in the Port Stephens estuary, New South Wales, Australia 328 429 S, 1528 009 E. Fish present at the study location were sampled by seine netting 20 3 2 m,
4 mm mesh and underwater observation using snorkels. Two broad categories of
S .D. Connell, M.J. Anderson J. Exp. Mar. Biol. Ecol. 241 1999 15 –29
17
predatory fish were observed: i small elongate toadfish, Tetractenos spp. generally , 200 mm TL; mean girth 5 18.7 mm, range of girth 11–26 mm: n 5 20 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
cm 3 2.5 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 cm 3 5 cm small, 10 cm 3 10 cm medium and
20 cm 3 20 cm large. Two panels of the same size were attached to tar-covered sticks 2.5 cm 3 2.5 cm 3 1.8 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 mm 3 50 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 3 12.5 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’
Fig. 1. Drawing of the structure used for the experiment, showing three treatments. a Panels on a stick open panels, b panels on a stick inside a full cylindrical cage, and c panels in a partial cage control for cage
artefacts which had the bottom half of the cage removed.
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.D. Connell, M.J. Anderson J. Exp. Mar. Biol. Ecol. 241 1999 15 –29
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 100 3 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 cm 3 5 cm and 10 cm 3 10 cm panels and 100 points for 20 cm 3 20 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 cage 3 panel 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; n 5 2 panels per stick. Ordinations were done using the
PRIMER
v4.0 computer program courtesy of M.R. Carr and K.R. Clarke, Plymouth Marine Laboratory, UK.
Principal coordinates were obtained using the computer program DistPCoA M.J.
S .D. Connell, M.J. Anderson J. Exp. Mar. Biol. Ecol. 241 1999 15 –29
19
Anderson and P. Legendre, University of Montreal and RDAs with appropriate permutation tests were done using
CANOCO
E 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 Factor 5 partial 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 Factor 5 cage, 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 cm 3 5 cm, 10 cm 3 10
cm and 20 cm 3 20 cm. The design was balanced: for each combination of treatments there were three sticks Factor 5 sticks, nested in cage 3 panel size and n 5 2 replicate
panels per stick. Univariate ANOVAs and Cochran’s tests were done using
GMAV
5 courtesy of A.J. Underwood and M.G. Chapman.
3. Results
