Journal of Animal Ecology 2008, 77, 515

Blackwell Publishing Ltd

doi: 10.1111/j.1365-2656.2007.01316.x

Condition-specic competition allows coexistence of competitively superior exotic oysters with native oysters

Frederick R. Krassoi1,2, Kenneth R. Brown1, Melanie J. Bishop1*, Brendan P Kelaher1 and . 1 Stephen Summerhayes
Institute for Water & Environmental Resource Management & Department of Environmental Sciences, University of Technology Sydney, Broadway NSW 2007 Australia; and 2Ecotox Services Australasia Pty Ltd, 27/2 Chaplin Drive, Lane Cove, NSW 2066, Australia
1

Summary 1. Trade-offs between competitive ability and tolerance of abiotic stress are widespread in the literature. Thus, condition-specic competition may explain spatial variability in the success of some biological invaders and why, in environments where there is small-scale environmental variability, competitively inferior and superior species can coexist. 2. We tested the hypothesis that differences in abiotic stress alter the outcome of competitive interactions between the native Sydney rock oysters Saccostrea glomerata and exotic Pacic oysters Crassostrea gigas by experimentally testing patterns of intra- and interspecic competition across a tidal elevation gradient of abiotic stress at three sites on the east coast of Australia. 3. At low and mid-intertidal heights, exotic C. gigas were able to rapidly overgrow and smother native S. glomerata, which grew at c. 60% of the exotics rate. In high intertidal areas, where C. gigas displayed about 80% mortality but similar growth rates to S. glomerata, the native oyster was not affected by the presence of the exotic species. 4. Asymmetrical effects of the exotic species on the native could not be replicated by manipulating densities of conspecics, conrming that effects at low and mid-intertidal heights were due to interspecic competition. 5. Our results suggest that the more rapid growth of C. gigas than S. glomerata comes at the cost of higher mortality under conditions of abiotic stress. Thus, although C. gigas may rapidly overgrow S. glomerata at low and mid tidal heights, the native oyster will not be competitively excluded by the exotic due to release from competition at high intertidal elevations. 6. The success of trade-offs in explaining spatial variation in the outcome of competitive interactions between C. gigas and S. glomerata strengthen the claim that these may be a useful tool in the quest to produce general predictive models of invasion success. Key-words: interspecic competition, intraspecic competition, invasion, life-history trade-off, tidal elevation.

Introduction
Ecologists have long sought to identify species or ecosystem characteristics that consistently predict patterns of invasion (e.g. Ehrlich 1989; Lodge 1993; Williamson & Fitter 1996). Following this approach, some life-history traits have been successfully used to explain some invasions (Williamson & Fitter 1996) and disturbance has been identied as a consistently good predictor of ecosystem invasibility (Lozon & MacIsaac

*Correspondence author. E-mail: Melanie.Bishop-1@uts.edu.au

1997). In general, however, life-history traits of successful invaders and characteristics of invaded environments display great variability throughout the world (Sakai et al. 2001). Consequently, a denitive list of species traits and ecosystem characteristics that predict invasion has not emerged despite much research in this area. The failure of studies to identify species or ecosystem characteristics that consistently predict patterns of invasion may be explained by the dependence of invasion on a match between a species and environment rather than intrinsic properties of either one (Facon et al. 2006). Because species must partition limited resource among maintenance (which

2007 The Authors. Journal compilation 2007 British Ecological Society

F. R. Krassoi et al. Observational evidence exists for competition between the Sydney rock oyster Saccostrea glomerata Gould 1980, native to Australia and New Zealand, and the Pacic oyster, Crassostrea gigas Thunberg 1973, native to Japan and rst introduced to Australasia for aquaculture (Dinamani 1991). Following the rst observation of C. gigas in Mahurangi Harbour, New Zealand in 1971, the ratio of oyster recruits rapidly changed from 1000 S. glomerata to every C. gigas in 1972, to four exotic oyster recruits to every native recruit in 1978 (Dinamani 1991). Yet although C. gigas, grows at up to twice the rate of the native oyster (e.g. Nell 1993; Honkoop & Bayne 2002) and produces 50100 million eggs annually compared with the 20 million eggs of the native oyster (Krassoi 2001), interspecic competition between the two species has never been experimentally tested. Further, although each species appears to be able to survive for at least short periods from the high intertidal to the subtidal (Krassoi 2001), the potential for differential abiotic tolerance of the two species to modify the outcome of interspecic interactions has not been considered. Saccostrea glomerata is well known among shellsh growers to survive longer out of water (23 weeks at 815 C) than C. gigas (1 week at 4 C; Nell 2001) and it is common practice for shellsh growers to remove unwanted C. gigas from common substrate by holding them out of water for a sufciently long time (Pollard & Hutchings 1990). Any competitive superiority of the exotic species may be at the expense of tolerance to harsh abiotic conditions, such that the native oyster is able to persist at high intertidal elevations despite being outcompeted by the exotic further down on the shore. Here, we use an experimental approach to examine intraand interspecic competition among native S. glomerata, and exotic C. gigas across a tidal elevation gradient. In determining whether faster growing C. gigas can outcompete slower growing S. glomerata across all tidal elevations, we provide one of the rst rigorous experimental assessments of how the competitive ability of resident biota might interact with abiotic suitability to determine invasion success. By not only assessing mortality of oysters under differing density treatments, but also changes in size and shape, our experiments suggest likely implications of competitive interactions on the habitat provision by these ecosystem engineers. As modiers of habitat quantity and quality (Crooks 2002; Newell 2004), oysters can have large impacts when introduced into ecosystems, yet to date their introduction has received little experimental scrutiny (Ruesink et al. 2005).

affects survival), growth (which affects age/size at maturity and future fecundity) and reproduction, the benets of performing one ecological task often come at the cost of performing another function (ecological trade-offs: Stearns 1992). Thus, a set of traits that confer success in invading and proliferating in an area with one set of biotic and abiotic conditions may provide little benet in another. Tradeoffs, such as those between competition and colonization, and competition and antipredator defence, have been well documented (reviewed by Kneitel & Chase 2004). Traditional studies of competition utilizing native species have shown that the outcome of interspecic competition is often contingent on features of the physical environment, as competitive dominance often comes at the expense of thermal or desiccation tolerance (e.g. Connell 1961; Bestelmeyer 2000; Juliano et al. 2002; Liancourt, Callaway & Michalet 2005). Thus, exotic species that invade by outcompeting native species (see Petren & Case 1996; Holway 1999; Byers 2000) may only be successful under environmentally benign conditions, leading to regional variability in their invasion success (Blackburn & Duncan 2001) and their coexistence with native analogues in places where abiotic variability occurs over small spatial scales (see Chesson 1986). Yet, despite the potential importance of condition-specic competition to patterns of invasion success, there remain relatively few experimental studies on this topic (see Holway, Suarez & Case 2002). Because it is often argued that invaders are successful for the very reason that they are able to exploit a wide range of abiotic conditions (Lodge 1993) and invaders may not be subject to the same trade-offs as native species (see Adler 1999), explicit empirical tests of the importance of the competitionenvironmental tolerance trade-off to the success and scale of exotic species invasions are urgently required. Among aquatic organisms, oysters are one of the most globally translocated taxa (Shatkin, Shumway & Hawes 1997; Ruesink et al. 2005). Exotic oysters have been introduced with permanent establishment in at least 24 countries outside of their native ranges and introduced without successful establishment in a further 55 (Ruesink et al. 2005). Because native oysters are almost always present within environments to which exotic oysters are introduced, the nature of competitive interactions between native and exotic oysters may be critical to the outcome of translocation. Although in many instances where the two species occupy different habitats, little competition would be expected, where there is signicant range overlap it would be expected that introduced oysters might outgrow native species because they are usually selected for introduction based on their high yield (NRC 2004). Although a number of studies have attributed successful oyster invasions to the ability of the exotic to outcompete the native oyster, these are supported by observational rather than experimental evidence (reviewed by Ruesink et al. 2005). Thus, until experimental tests of competition between native and exotic oysters that involve comparisons of growth and mortality between monocultures and mixed cultures are attempted, alternative explanations such as differential susceptibility to disease cannot be ruled out.

Methods
SAMPLING DESIGN

We conducted our assessment of intra- and interspecific competition among native Sydney rock oysters, S. glomerata, and exotic Pacific oysters, C. gigas, at three oyster farms in Port Stephens, New South Wales, Australia (3243 S, 1529 E). Port Stephens, approximately 150 km to the north of Sydney, is a large (125 km2) natural harbour, which extends from the Pacific Ocean to the mouth of the Karuah River, 24 km to the west. At the time of this study, this estuary, a

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Condition-specic competition among oysters 7

focal point for Sydney rock oyster cultivation since 1878, served as the source of 75% of the NSW Sydney rock oyster industrys annual spat requirements (Anon 1986). Although C. gigas is considered a noxious pest throughout the rest of New South Wales, commercial culture of the exotic, believed to have been deliberately introduced to the area in 1984 from southern Australia, has also legally occurred in the estuary since 1991, at which time it was declared too prolific to eradicate. The three farms at Salamander Bay, Uptons Island (Tilligerry Creek) and Wirrung Island were selected due to their ideal conditions for cultivation of S. glomerata and because a survey conducted shortly before this experiment indicated the presence of C. gigas in adjacent mangrove forests (Krassoi 2001). Sites were characterized by a muddy sand substrate, shallow depths of less than 2 m, average salinities of 25 28 psu and tidal ranges of c.13 m. We utilized the stick and beam structure of the oyster farms (see Anderson 1999 for a full description) to deploy oysters at three tidal heights: Indian Spring Low Water (ISLW) +06 m (low), ISLW +10 m (mid) and ISLW +12 m (high). These three tidal elevations were chosen to encompass most of the intertidal range of S. glomerata in Port Stephens, which extends from the subtidal up to 14 m above ISLW, with our low tidal height corresponding to the optimal height for S. glomerata settlement (Krassoi 2001). Although C. gigas is generally more abundant at the low and mid tidal heights, an estuary-wide survey in June 1990 indicated that it can also occur at the high intertidal height on rocky shores, where it may account for up to 43% of oysters (Krassoi 2001). To ascertain the strength of intra- and interspecific competition among oysters across this environmental gradient of exposure, at each tidal height we deployed roughened 03 03 m polycarbonate (Perspex) plates to which 10, 20 or 30 oysters representing one or both species were attached inside of a 005 m buffer (Table 1). These densities were well within the natural range displayed by S. glomerata on adjacent substrata (Krassoi 2001). This experimental design, based on that developed by Underwood (1978), uses treatments with 10 oysters as controls against which to compare the growth and mortality of animals in treatments with enhanced density, achieved either through the addition of conspecifics or the alternate species. This type of asymmetrical design, which enables the simultaneous and unconfounded consideration of the effects of both intra- and interspecific competition does not suffer from the limitations of many designs used to assess competition (Underwood 1986, 1997). Although we chose to conduct our experiment on an artificial substrate, we suspect that oysters on the fixed horizontal polycarbonate plates would interact in similar ways to oysters on horizontal rocky shores because: (1) movement and orientation of substrata are frequently more important than surface material in determining the development of fouling communities (Glasby 2000; Holloway & Connell 2002), and (2) S. glomerata and C. gigas densities differ little between artificial and natural substrates (Chapman 2006), suggesting similarity of ecological processes between the two types of surface. The oysters were 6-month-old hatchery-reared spat obtained from the Taylors Beach Brackish Water Fish Culture Research Station. S. glomerata had a length (distance from the umbo to the furthest margin) of 45 70 mm and a width (maximum transverse distance) of 35 65 mm. The dimensions of the faster-growing C. gigas were 50 75 mm by 45 70 mm. We attached spat to the Perspex plates using two-part marine epoxy resin. The left valve of each oyster was glued to the plate, with care taken to ensure that the two valves were not glued shut. A pilot study conducted over 4 months indicated that the epoxy resin successfully held the spat in place until the oyster cemented itself to the plate with its normal growth and that it was not toxic to the organism. To ensure even spacing of oysters, we glued individuals at intersection points of a standardized grid marked on each plate. Where the experimental treatment consisted of both oyster species, oysters were arranged on the plates such that each oyster had at least one neighbour of the other species. In May 1989, we deployed 81 replicate Perspex plates at each site using 3 1 m hardwood trays. Each tray held one replicate of each of the nine treatments (Table 1) in a randomly determined spatial arrangement. At each site, three trays were deployed (n = 3). The trays were covered with a 15 15 mm plastic mesh to exclude predatory fish and were fixed to horizontal beams of the commercial leases using galvanized wire. Experimental trays were cleaned of silt, debris, algae and the upper valves of dead experimental oysters every 2 months. This involved transporting trays to the Research Station by boat, where the upper plastic mesh was removed and the tray and plastic mesh were washed with a high-pressure hose. Growth and mortality of oysters was not determined at these intermediate times because it was often impossible to distinguish between the two species without destructive sampling, especially in instances where overgrowth had occurred. Nevertheless, qualitative observations suggested negligible mortality of S. glomerata prior to overgrowth with C. gigas, although sizeable mortality of C. gigas did occur prior to interaction between the two species, particularly at the high intertidal height. Intra- and interspecific competition among oysters were examined in November 1990, 18 months following deployment. Deterioration of hardwood trays due to marine borers, and high rates of mudworm and flatworm infestation among oysters, prevented subsequent sampling. Nevertheless, significant overgrowth by C. gigas of S. glomerata at low and mid tidal heights at this time suggested that 18 months was a sufficient experimental duration for assessment of competition. Trays were transported to the laboratory, where the oysters were removed from the Perspex plates. For each plate, we determined the proportionate mortality of each species of oyster and, using callipers, the length and width (to the nearest millimetre) of five randomly selected live oysters of each species. This number of oysters was selected for analysis based on the minimum number still alive on plates. Because the asymmetrical nature of analyses required partitioning of variances, it was important to maintain a balanced design and for this reason additional oysters were not measured on plates with higher survivorship. Whole oyster weights were not measured at the termination of the experiment because pilot studies indicated weight to be significantly correlated with size (length width; S. glomerata: r2 = 0477, P < 0001, n = 75, C. gigas: r2 = 0614, P < 0001, n = 75).

Table 1. Nine experimental treatments used for simultaneous examination of intra- and interspecic competition among Sydney rock oysters (SRO) Saccostrea glomerata, and Pacic oysters (PO) Crassostrea gigas Experimental densities of oysters (no. per 025 m2) 10 (control) 10 SRO 10 PO 20 20 SRO 20 PO 10 SRO + 10 PO 30 30 SRO 30 PO 10 SRO + 20 PO 10 PO + 20 SRO

ANALYSIS OF DATA

In order to simultaneously examine the effects of intra- and interspecific competition, we utilized asymmetrical analyses of variance

2007 The Authors. Journal compilation 2007 British Ecological Society, Journal of Animal Ecology, 77, 515

F. R. Krassoi et al.
mortality data for S. glomerata and C. gigas using Perspex plates as replicates. A second analysis was then run for each species on the same set of data but with the control treatment excluded. These second analyses had four factors: site (three levels, random), height (three levels: high, mid, low), density (two levels: 20, 30) and species contributing to increases in oyster density [two levels: S. glomerata (SRO), C. gigas (PO)]. By subtracting the sums of squares for variation attributable to subsets (density, species, density species) from the sums of squares for variation among all treatments, we could then calculate a sums of squares for control vs. other treatments and perform corresponding F-tests for this main effect and interactions (Table 2) described by Underwood (1978).

of the type described by Underwood (1978). These analyses, which involve partitioning components of variation through a number of subanalyses (see also Winer 1971), allow the comparison of treatments in which the density of oysters is increased, either via the addition of conspecifics or the alternate species, against the single set of replicates of the control treatment (10 oysters of a single species). Specifically, to test hypotheses regarding effects of competition on oyster mortality, separate three-way analyses of variance (anova) with the factors, site (three levels, random), height (three levels: high, mid, low) and treatment [five levels: 10 of species 1 (control), 20 of species 1, 30 of species 1, 10 of species 1 + 10 of species 2, 10 of species 1 + 20 of species 2] were first run on arcsine-transformed proportional

Table 2. Analyses of variance examining variation in the proportional mortality of Saccostrea glomerata and Crassostrea gigas among treatments [ve levels: 10 of species 1 (control), 20 of species 1, 30 of species 1, 10 of species 1 + 10 of species 2, 10 of species 1 + 20 of species 2, where species 1 is the oyster for which mortality is being examined and species 2 is the potential competitor], sites [three levels: random; Salamander Bay (S1), Uptons Island (S2), Wirrung Island (S3)] and tidal heights [three levels: low (L), mid (M), high (H)]. Terms signicant at = 005 are highlighted in bold. All data were arcsine transformed prior to analysis. n = 3 Saccostrea glomerata d.f. Among all treatments Controls vs. others Among others Density Species Density species Site Height Site height Site all treatments Site control vs. others Site among others Site density Site species Site density species Height all treatments Height controls vs. others Height among others Height density Height species Height density species Height site all treatments Height site controls vs. others Height site among others Height site density Height site species Height site density species Residual 4 1 3 1 1 1 2 2 4 8 2 6 2 2 2 8 2 6 2 2 2 16 4 12 4 4 4 90 MS 6500 7191 6269 263 18 521 25 1020 1670 439 160 252 130 94 251 45 863 455 999 131 2654 212 176 112 197 102 249 239 151 F P Crassostrea gigas MS 150 5 199 215 380 2 3004 4417 2655 327 437 290 10 686 173 147 491 32 80 1 15 219 106 257 299 340 132 224 F P

448 16 1156 02 68 38 29 17 06 17 03 26 07 151 12 07 07 17 16

< 0001 0236 < 0001 0704 0002 0119 0026 0194 0538 0195 0743 0106 0490 < 0001 0324 0566 0608 0167 0185

00 07 12 00 134 17 119 20 00 31 08 22 04 00 01 05 13 15 06

0900 0441 0312 0946 < 0001 0298 < 0001 0148 0958 0052 0465 0139 0699 0996 0934 0756 0264 0203 0672

Cochrans test SNK tests Site height Height species

Saccostrea glomerata C = 023 (P < 001) S1: L = M = H S2: L = M = H S3: L = M > H SRO: L = M = H PO: L = M > H L: SRO < PO M: SRO < PO H: SRO = PO

Crassostrea gigas C = 013 (P > 005) S1: L = M = H S2: L = M < H S3: M < L = H

SRO, increase in density due to addition of Sydney rock oysters; PO, increase in density due to addition of Pacic oysters. 2007 The Authors. Journal compilation 2007 British Ecological Society, Journal of Animal Ecology, 77, 515

Condition-specic competition among oysters 9

Fig. 1. Mean ( 1 SE) mortality of Sydney rock oysters Saccostrea glomerata, and Pacic oysters Crassostrea gigas, 18 months after manipulation of total oyster density through the addition of Sydney rock oysters (SRO) and/or Pacic oysters (PO) to Perspex plates. Replicates were pooled within sites (n = 3).

Similar analyses were performed on untransformed oyster sizes (width length) and oyster shapes (width to length ratio) transformed by a ln(x + 1) function. Because oyster morphology is intrinsically variable and the number of remaining oysters was variable among treatments, treatment means for each combination of tidal height and site were used as replicates in these analyses. The full analyses of oyster sizes and shapes consequently had two factors, height and treatment, with the three sites serving as replicates. The subanalyses had three factors (height, density, species). We regard pooling across sites as a valid approach because pilot analyses using individual oysters as replicates within a site did not reveal significant site height treatment or site treatment effects for either species (anova: P > 025). Treatment means were generally considered statistically significant at = 005. Where Cochrans test indicated heterogeneity in variances even after transformation, the more conservative = 001 was employed to minimize the probability of Type I error. In the case of statistically significant effects, appropriate means were compared using StudentNewmanKeuls (SNK) tests (Underwood 1997).

Results
PROPORTIONAL MORTALITY

Both the tidal height at which oyster density was manipulated and the identity of the species added affected proportional mortality of S. glomerata (anova: height species added, P < 005; Table 2, Fig. 1). Whereas proportional mortality on monospecic plates was comparable (0203) not only among tidal heights but also among S. glomerata densities of

10, 20 and 30, on the mixed-species plates, mortality at the low and mid tidal heights was enhanced by the addition of even a small number of C. gigas. At these two lowest tidal heights, overgrowth of S. glomerata by C. gigas was observed on mixedspecies plates resulting in S. glomerata mortality that was four times greater than on plates with 10 S. glomerata alone (SNK contrasts, Table 2). Despite the effect of C. gigas on S. glomerata mortality, proportional mortality of S. glomerata on plates with C. gigas remained about 08, irrespective of whether 1020 C. gigas were added to the 10 S glomerata (anova: increased density, P > 005; Table 2, Fig. 1). At the high intertidal height, where overgrowth of S. glomerata by C. gigas was rare, neither the addition of S. glomerata nor C. gigas to plates with 10 S. glomerata had any effect on S. glomerata mortality (SNK contrasts, Table 2). Although, across all treatments, some differences among the three sites were evident in patterns of proportional mortality of S. glomerata across tidal heights (anova: site height, P < 005, Table 2, Fig. 2), these were mainly due to reduced mortality of S. glomerata in the high intertidal zone at one site (SNK contrasts, Table 2). Consequently, the differences in response to tidal elevation among sites did not inuence the response of S. glomerata mortality to the interaction of oyster density, the identity of added oysters and height (anova: height site all treatments, P > 005, Table 2). Whereas mortality of S. glomerata was strongly inuenced by the presence of C. gigas, mortality of C. gigas was not affected by an increase in the total oyster density to 20 or 30, whether this was through the addition of conspecics or

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F. R. Krassoi et al. S. glomerata (Table 2, Fig. 1). Across all treatments, however, C. gigas mortality was strongly inuenced by site and tidal height (anova: site height, P < 005, Table 2, Fig. 2). At two of the three sites, Uptons Island and Wirrung Island, greater proportional mortality (c.08) of C. gigas was evident at high tidal than at the mid tidal elevations (SNK contrasts, Table 2). At Uptons Island, mortality in the upper intertidal was also greater than in the low intertidal.

SIZE AND SHAPE OF OYSTERS

Fig. 2. Mean ( 1 SE) mortality of Sydney rock oysters Saccostrea glomerata, and Pacic oysters Crassostrea gigas, at Salamander Bay (S1), Uptons Island (S2) and Wirrung Island (S3) over the 18-month experiment. n = 5 treatments.

The relative growth performance of S. glomerata and C. gigas was highly dependent on tidal elevation. At low intertidal heights, C. gigas attained approximately twice the size of S. glomerata (PO 4434 360 vs. SRO 2075 199 mm2), at mid tidal heights C. gigas was about 50% larger (PO, 2990 162 vs. SRO, 2021 160 mm2) and at high tidal heights there was no appreciable difference in the size attained by the two species (PO, 1987 201 vs. SRO, 2051 108 mm2; Fig. 3). Tidal elevation had little effect on the size obtained by S. glomerata (anova: height, P > 005; Table 3, Fig. 3), but C. gigas attained greatest size when grown at a low intertidal height and remained smallest when grown in the high intertidal (SNK contrasts, Table 3, Fig. 3). Within each tidal height, the size attained by S. glomerata was smaller at total oyster densities of 20 or 30 than at densities of 10 per plate (anova: controls vs. others, P < 005, Table 3), although the magnitude

Fig. 3. Mean ( 1 SE) size (length width) of Sydney rock oysters Saccostrea glomerata, and Pacic oysters Crassostrea gigas, 18 months after manipulation of total oyster density through the addition of Sydney rock oysters (SRO) and/or Pacic oysters (PO) to Perspex plates. Replicates were pooled within sites (n = 3). 2007 The Authors. Journal compilation 2007 British Ecological Society, Journal of Animal Ecology, 77, 515

Condition-specic competition among oysters 11

Table 3. Analyses of variance examining variation in the size (length width) of Saccostrea glomerata and Crassostrea gigas among treatments, sites and tidal heights. Levels of factors are as outlined in Table 2. Terms signicant at = 005 are highlighted in bold. Data were analysed untransformed. n = 3 Saccostrea glomerata d.f. Among all treatments Controls vs. others Among others Density Species Density species Height Height all treatments Height controls vs. others Height among others Height density Height species Height density species Residual 4 1 3 1 1 1 2 8 2 6 2 2 2 30 MS 2 636 637 4 762 582 1 927 989 2 921 220 1 782 376 1 080 371 11 015 177 919 274 938 145 579 199 390 220 030 17 318 139 763 F P Crassostrea gigas MS 811 502 2 975 623 90 128 345 85 311 184 729 2 699 070 550 872 382 684 606 935 1 483 616 238 931 98 258 1 120 545 Crassostrea gigas C = 018 (P > 005) Height L>M>H F P

341 209 128 77 01 17 14 16 01

< 0001 < 0001 0001 0009 0924 0157 0256 0224 0884

27 00 01 02 203 03 13 02 01

0114 0986 0784 0687 < 0001 0713 0281 0809 0916

Cochrans test SNK tests

Saccostrea glomerata C = 030 (P > 005) Density species SRO: 10 > 20 PO: 10 = 20 10: SRO > PO 20: SRO = PO

of the density effect depended on the species of oyster added to plates (anova: density species, P < 005, Table 3). At total oyster densities of 20 per plate, S. glomerata were larger on plates with only S. glomerata than on plates with 10 S. glomerata and 10 C. gigas, but at oyster densities of 30 per plate the decreased size of S. glomerata was independent of the species composition of the additional oysters (SNK contrasts, Table 3, Fig. 3). By contrast, little change in the size of C. gigas size was evident across treatments of differing density, irrespective of whether density was increased through addition of C. gigas or S. glomerata (Table 3, Fig. 3). In contrast to oyster size, oyster shape differed little between the three tidal heights examined or between the two species of oyster (Table 4, Fig. 4). An effect of increasing oyster density on the shape of S. glomerata that was dependent on the identity of oysters contributing to density was, nevertheless, evident (anova: density species, P < 005, Table 4, Fig. 4). Whereas increasing the total density of S. glomerata from 20 to 30 oysters per plate resulted in S. glomerata with greater width to length ratios, there was no difference in the shape of S. glomerata between plates that held 10 or 20 C. gigas in addition to the 10 S. glomerata (SNK contrasts, Table 4, Fig. 4). At mid and high intertidal heights, there was a slight trend for C. gigas of greater width to length ratio on plates with 20 or 30 oysters than on plates with 10, a pattern that was evident irrespective of whether the additional density was attributed to C. gigas or S. glomerata. This pattern was not,

however, statistically signicant (anova: height control vs. others, P > 005, Table 4, Fig. 4).

Discussion
By affecting tness of individuals, competitive interactions can have large effects on the composition and structure of ecological communities (Dayton 1971; Connell 1975; Huston 1979), especially where one or more of the species involved is an ecosystem engineer (Crooks 2002). Yet, despite the possibility that exotic bivalves introduced for aquaculture may, through the displacement of native counterparts, have large effects on benthic community structure, competitive interactions between native and exotic species of oysters had not previously been examined experimentally (see Ruesink et al. 2005). In considering the relative strength of intra- vs. interspecic interactions, our study determined competitive interactions between the native Sydney rock oyster, S. glomerata, and the exotic Pacic oyster, C. gigas, at a range of tidal heights on the east coast of Australia. In generating strong evidence for competitive dominance of the exotic species at low and mid tidal heights, our results suggest that over time the native species may be displaced from certain habitats by the exotic species. It is unlikely, however, that this competition would lead to extinction, as the native S. glomerata held its own at high tidal elevations. At low and mid tidal heights, addition of 6-month-old C. gigas to plates containing similar-aged S. glomerata resulted in fourfold increases in mortality of the native species. This

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F. R. Krassoi et al.

Table 4. Analyses of variance examining variation in the shape (width/length) of Saccostrea glomerata and Crassostrea gigas among Treatments, Sites and tidal Heights. Levels of factors are as outlined in Table 2. Terms signicant at = 005 are highlighted in bold. All data were ln(x + 1) transformed prior to analysis. n = 3 Saccostrea glomerata d.f. Among all treatments Controls vs. others Among others Density Species Density species Height Height all treatments Height controls vs. others Height among others Height density Height species Height density species Residual 4 1 3 1 1 1 2 8 2 6 2 2 2 30 MS 00017 00001 00022 00028 00016 00022 00004 00002 00004 00002 00003 00001 00001 00004 F P Crassostrea gigas MS 00010 00031 00003 00000 00008 00002 00009 00006 00012 00004 00000 00012 00000 00008 F P

02 59 34 46 08 08 06 02 01

0649 0021 0076 0039 0473 0439 0538 0811 0900

41 00 11 03 12 16 00 15 00

0052 1000 0312 0611 0313 0221 1000 0235 1000

Cochrans test SNK tests

Saccostrea glomerata C = 033 (P > 005) Density species SRO: 10 < 20 PO: 10 = 20 10: SRO = PO 20: SRO > PO

Crassostrea gigas C = 030 (P > 005)

Fig. 4. Mean ( 1 SE) shape (width/length) of Sydney rock oysters Saccostrea glomerata, and Pacic oysters Crassostrea gigas, 18 months after manipulation of total oyster density through the addition of Sydney rock oysters (SRO) and/or Pacic oysters (PO) to Perspex plates. Replicates were pooled within sites (n = 3). 2007 The Authors. Journal compilation 2007 British Ecological Society, Journal of Animal Ecology, 77, 515

Condition-specic competition among oysters 13 pattern, evident irrespective of the density of C. gigas added, was not replicated by increases in the density of S. glomerata on monospecic panels, and coupled with our observation that mortality of S. glomerata was negligible prior to overgrowth by C. gigas, provides strong evidence for interspecic competition. By contrast, addition of S. glomerata to C. gigas panels had no effect on mortality of the exotic species across the examined range of densities. Thus, interspecic competition between the two species was asymmetrical, with the exotic oyster being the dominant species. Despite the large negative effects of C. gigas on S. glomerata at the lower elevations, in the upper intertidal, competition was absent. Each of the two species of oyster displayed similar rates of mortality among the three densities examined, irrespective of species composition, although this was less for S. glomerata. The mechanism by which abiotic stress prevented competitive dominance of C. gigas was the enhanced mortality and decreased growth of the exotic species at high tidal elevations. Whereas at low and mid intertidal heights C. gigas were much larger than S. glomerata, at high tidal heights there was no appreciable difference in the size attained by the two species and, in some instances, C. gigas was slightly smaller. The reduced growth of C. gigas at high tidal elevations was coupled with greater rates of mortality, up to double those of mid and low tidal heights, which reduced nominal densities of C. gigas by 50 90%. Thus, at high intertidal heights the exotics slower rate of growth and low abundance prevented overgrowth and smothering of S. glomerata. These observations agree with the model provided by Connell (1961, 1972, 1975) and Menge & Sutherland (1987) that competition is a major determinant of community structure in the lower limits of distribution, but is reduced in the upper intertidal zone as harsh physical conditions effectively reduce densities eliminating the potential for density-dependent interactions. This study did not attempt to determine the mechanism underlying the trade-off of abiotic tolerance for interspecic competitive ability. Indeed, despite the increasingly common observation of this relationship across many taxonomic groups (e.g. Bestelmeyer 2000; Juliano et al. 2002; Liancourt et al. 2005), to our knowledge there have been no direct tests of the mechanism responsible in any system. Potential mechanisms may involve the investment of energy in rapid rates of growth reducing resources available for maintenance during times out of water when the oysters cannot feed or the resources available for synthesis of heat shock proteins under conditions of stress. Alternatively, rapid rates of growth may require respiration rates that cannot be sustained during periods of prolonged emersion. In using S. glomerata and C. gigas of identical age, our study assumed similar timing of colonization between the two species. This is not an unreasonable assumption given that spawning and larval settlement of S. glomerata in Port Stephens extends from November to May/June (McOrrie 1990, 1995) and peak C. gigas settlement occurs from November through May (Holliday et al. 1993). Nevertheless, because the two species exhibit slightly different salinity and temperature optima for spawning, larval development and settlement (Baradach, Ryther & McLarney 1972; Nell & Gibbs 1986; Nell & Holliday 1988), the relative timing of settlement by the two species will vary from year to year according to climatic conditions. In years where settlement of C. gigas precedes that of S. glomerata, the asymmetry of competitive interactions between the two species may be exacerbated at low elevations, because the exotic species receives an even greater size advantage and may also pre-empt space otherwise available to the native oyster. Although in years where S. glomerata settles earlier, the intensity of competition may initially be weakened by pre-emption of space, the exotic species, which can settle on other oysters, would, nevertheless, be expected to eventually outcompete the native oyster because its growth rate and capacity for smothering is so much greater. Our nding that S. glomerata can persist at high intertidal heights, despite being outcompeted by the exotic species at lower tidal elevations is consistent with observations of the natural distribution of the two oyster species in NSW (D. Reid, unpublished data; K.R. Brown and F.R. Krassoi, unpublished data; C.P.J. Farmer, unpublished data). Whereas S. glomerata can attain high densities (of over 100 m 2) at aerial exposures of 077% of the tidal cycle, C. gigas is generally not found above aerial exposures of 40%, and is most abundant where the substrate is exposed for 030% of the tidal cycle (K.R. Brown and F.R. Krassoi, unpublished data; C.P.J. Farmer, unpublished data). Despite oysters ranking among the most translocated of marine taxa (see Shatkin et al. 1997; Ruesink et al. 2005) and the large implications this may have on the functioning of benthic systems (Crooks 2002; Newell 2004), our study represents the rst experimental consideration of competitive interactions between native and exotic oysters. Given that the mechanism by which C. gigas outcompeted S. glomerata at low and mid tidal elevations was overgrowth, and most exotic oysters are selected for introduction based on their rapid rate of growth, similar dominance of exotic oysters over native counterparts under at least some environmental conditions may be expected elsewhere. Although native and exotic oysters are likely to provide similar ecosystem goods and services, partial or complete substitution of one species for another may, nevertheless, produce signicant ecological impacts. For example, because C. gigas are generally much larger than S. glomerata, they provide habitat of different complexity to the native species and may consequently support different oral and faunal assemblages (see Wells 1961). Similarly, benthicpelagic coupling and trophic transfer may differ between native and exotic oysters as a result of differences in their physiology (Bayne 2002) and morphology (Bishop & Peterson 2006). Even where native oysters persist among exotic oysters, their provision of ecosystem services may be altered because the presence of C. gigas signicantly changed the shape (as indicated by width to length ratios) of S. glomerata, altering the physical structure of the habitat it provides. Our study provides an experimental demonstration of how the post-establishment invasion success of a competitively dominant invader hinges upon variation in the physical environment. The condition-specic nature of the competition between C. gigas and S. glomerata resembles that observed in

2007 The Authors. Journal compilation 2007 British Ecological Society, Journal of Animal Ecology, 77, 515

14

F. R. Krassoi et al.
(eds M.C. Greer & J.C. Lefer), pp. 912. Maryland Sea Grant Collegial Program, College Park, MD. Ehrlich, P.R. (1989) The attributes of invaders and the invading processes: vertebrates. Biological Invasions: a Global Perspective (eds J.A. Drake, H.A. Mooney, F. di Castri, R.H. Groves, F.J. Kruger, M. Rejmnek & M. Williamson), pp. 315328. John Wiley and Sons, New York. Facon, B., Genton, B.J., Shykoff, J., Jarne, P., Estoup, A. & David, P. (2006) A general eco-evolutionary framework for understanding bioinvasions. Trends in Ecology and Evolution, 21, 130135. Glasby, T.M. (2000) Surface composition and orientation interact to affect subtidal epibiota. Journal of Experimental Marine Biology and Ecology, 248, 177190. Holliday, J.E., Allan, G.L., Frances, J. & Diver, L.P. (1993) Evaluation of commercially used collectors for Sydney rock oysters, Saccostrea commercialis, and Pacic oysters, Crassostrea gigas. Aquacultural Engineering, 12, 63 79. Holloway, M.G. & Connell, S.D. (2002) Why do oating structures create novel habitats for subtidal epibiota? Marine Ecology Progress Series, 235, 4352. Holway, D.A. (1999) The competitive displacement of native ants by the invasive Argentine ant: mechanisms of exploitation and interference competition. Ecology, 80, 238251. Holway, D.A., Suarez, A.V. & Case, T.J. (2002) Role of abiotic factors in governing susceptibility to invasion: a test with Argentine ants. Ecology, 83, 16101619. Honkoop, P.J.C. & Bayne, B.L. (2002) Stocking density and growth of the Pacic oyster (Crassostrea gigas) and the Sydney rock oyster (Saccostrea glomerata) in Port Stephens, Australia. Aquaculture, 213, 171186. Huston, M.A. (1979) A general hypothesis of species diversity. American Naturalist, 113, 81101. Juliano, S.A., OMeara, G.F., Morrill, J.R. & Cutwa, M.M. (2002) Desiccation and thermal tolerance of eggs and the coexistence of competing mosquitoes. Oecologia, 130, 458469. Kneitel, J.M. & Chase, J.M. (2004) Trade-offs in community ecology: linking spatial scales and species coexistence. Ecology Letters, 7, 6980. Krassoi, F.R. (2001) Population ecology of the Sydney rock oyster Saccostrea commercialis and the Pacic oyster Crassostrea gigas in a New South Wales Estuary. PhD Thesis, University of Technology, Sydney, Australia. Liancourt, P., Callaway, R.M. & Michalet, R. (2005) Stress tolerance and competitive-response ability determine the outcome of biotic interactions. Ecology, 86, 16111618. Lodge, D.M. (1993) Biological invasions: lessons from ecology. Trends in Ecology and Evolution, 8, 133136. Lozon, J.D. & MacIsaac, H.J. (1997) Biological invasions: are they dependent on disturbance? Environmental Review, 5, 131144. McOrrie, S. (1990) Oyster settlement in Port Stephens 198990. Proceedings, Open Day, Brackish Water Fish Culture Research Station, NSW Agriculture and Fisheries, pp. 4145. NSW Agriculture and Fisheries, Australia. McOrrie, S. (1995) Oyster Settlement and Recruitment Study. Project 88/104, Final report. Fisheries Research and Development Corporation. Australia. Menge, B.A. & Sutherland, J.P. (1987) Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. American Naturalist, 130, 730757. National Research Council (2004) Study on Exotic Oysters in the Chesapeake Bay. National Academies Press, Washington, DC, USA. Nell, J.A. (1993) Farming the Sydney rock oyster (Saccostrea commercialis) in Australia. Reviews in Fisheries Science, 1, 97120. Nell, J.A. (2001) The history of oyster farming in Australia. Marine Fisheries Review, 63, 1425. Nell, J.A. & Gibbs, P.J. (1986) Salinity tolerance and absorption of 1-methionine by some Australian bivalve molluscs. Australian Journal of Marine and Freshwater Research, 37, 721727. Nell, J.A. & Holliday, J.E. (1988) Effects of salinity on the growth and survival of Sydney rock oyster (Saccostrea commercialis) and Pacic oyster (Crassostrea gigas) larvae and spat. Aquaculture, 68, 3944. Newell, R.I.E. (2004) Ecosystem inuences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. Journal of Shellsh Research, 23, 5161. Petren, K. & Case, T.J. (1996) An experimental demonstration of exploitation competition in an ongoing invasion. Ecology, 77, 118132. Pollard, D. & Hutchings, P. (1990) A review of exotic marine organisms introduced to the Australian region. II. Invertebrates and algae. Asian Fisheries Science, 3, 223250. Ruesink, J.L., Lenihan, H.S., Trimble, A.C., Heiman, K.W., Micheli, F., Byers, J.E. & Kay, M.C. (2005) Introduction of exotic oysters: ecosystem effects and restoration implications. Annual Review of Ecology and Systematics, 36, 643689.

other animal communities in which differences exist with respect to competitive ability and tolerance of extreme physical conditions (Connell 1961; Juliano et al. 2002). Thus, the results of this study strengthen the claim by Holway (1999) that competitive trade-offs may prove a useful tool in the quest to produce general predictive models of invasion success. Whereas consideration of only competitive ability may have led to the false conclusion that S. glomerata, will over time, be excluded by exotic C. gigas, consideration of the trade-off between competitive ability and abiotic tolerance suggests coexistence will be possible in a heterogeneous environment where the competitively inferior native oyster can persist in areas of greater abiotic stress.

Acknowledgements
We wish to thank J. Nell, S. Hunter and W. OConnor of NSW Fisheries for assistance with the rearing of oysters at the Port Stephens Research Centre. I. Anderson, M. Conlon, L. McClusky, P. Jones and B. Parsons helped in the eld. This research was funded by an Australian Research Council Linkage Grant (to B. Kelaher and M. Bishop) and a UTS Chancellors Postdoctoral Fellowship supported M. Bishop during the preparation of this manuscript. The suggestions of two anonymous reviewers improved the quality of this manuscript.

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