Blackwell Publishing Ltd Condition-Specific Competition Allows Coexistence of Competitively Superior Exotic Oysters With Native Oysters

8/3/2019 Blackwell Publishing Ltd Condition-Specific Competition Allows Coexistence of Competitively Superior Exotic Oysters With Native Oysters

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Journal of Animal Ecology 2008, 77, 515 doi: 10.1111/j.1365-2656.2007.01316.x

2007 The Authors. Journal compilation 2007 British Ecological Society

BlackwellPublishingLtd

Condition-specific competition allows coexistence of

competitively superior exotic oysters with native oysters

Frederick R. Krassoi1,2, Kenneth R. Brown

1

, Melanie J. Bishop

1

*, Brendan P. Kelaher

1

and

Stephen Summerhayes

1

1

Institute for Water & Environmental Resource Management & Department of Environmental Sciences, University of

Technology Sydney, Broadway NSW 2007 Australia; and2

Ecotox Services Australasia Pty Ltd, 27/2 Chaplin Drive, Lane

Cove, NSW 2066, Australia

Summary

1.

Trade-offs between competitive ability and tolerance of abiotic stress are widespread in the

literature. Thus, condition-specific 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 oystersSaccostrea glomerata

and exotic Pacific oysters

Crassostrea gigas

by experimentally testing patterns of intra- and interspecific 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 conspecifics, confirming that effects at low and mid-intertidal heights were due to

interspecific competition.

5.

Our results suggest that the more rapid growth ofC. gigas

than S. glomerata

comes at the cost

of higher mortality under conditions of abiotic stress. Thus, althoughC. 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:

interspecific competition, intraspecific 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 identified as a consistently

good predictor of ecosystem invasibility (Lozon & MacIsaac

1997). In general, however, life-history traits of successfulinvaders and characteristics of invaded environments display

great variability throughout the world (Sakai et al

. 2001).

Consequently, a definitive 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

*Correspondence author. E-mail: [email protected]


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F. R. Krassoi

et al.

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

, 77

, 515

affects survival), growth (which affects age/size at maturity

and future fecundity) and reproduction, the benefits 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 benefit in another. Trade-

offs, such as those between competition and colonization,

and competition and antipredator defence, have been welldocumented (reviewed by Kneitel & Chase 2004).

Traditional studies of competition utilizing native species

have shown that the outcome of interspecific 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-specific 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 mostglobally 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 com-

petition would be expected, where there is significant range

overlap it would be expected that introduced oysters mightoutgrow 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 experi-

mental 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.

Observational evidence exists for competition between

the Sydney rock oyster Saccostrea glomerata

Gould 1980,

native to Australia and New Zealand, and the Pacific oyster,

Crassostrea gigas

Thunberg 1973, native to Japan and first

introduced to Australasia for aquaculture (Dinamani 1991).

Following the first 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 in1978 (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), interspecific 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 interspecific interactions has not

been considered. Saccostrea glomerata

is well known among

shellfish 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 shellfish growers to remove unwanted

C. gigas

from common substrate by holding them out of water

for a sufficiently 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 intra-

and interspecific competition among nativeS. glomerata

, and

exotic C. gigas

across a tidal elevation gradient. In determining

whether faster growing C. gigas

can outcompete slowergrowing S. glomerata

across all tidal elevations, we provide

one of the first 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 treat-

ments, but also changes in size and shape, our experiments

suggest likely implications of competitive interactions on the

habitat provision by these ecosystem engineers. As modifiers

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).

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 (32

43

S, 152

9

E). Port Stephens, approximately

150 km to the north of Sydney, is a large (125 km

2

) 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-specific competition among oysters

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

, 77

, 515

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 ofS. glomerata

and because a surveyconducted 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 2528 psu and tidal ranges ofc.

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 ofS. 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 4570 mm and a width (maximum transverse distance)

of 3565 mm. The dimensions of the faster-growing C. gigas

were

5075 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 werenot 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 ofS. glomerata

prior to overgrowth with C. gigas

,

although sizeable mortality ofC. gigas

did occur prior to interaction

between the two species, particularly at the high intertidal height.

Intra- and interspecific competition among oysters were examinedin 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

: r

2

=

0477, P

005; Table 2, Fig. 1). At the high

intertidal height, where overgrowth ofS. glomerata byC. gigas

was rare, neither the addition ofS. 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 ofS. glomerata across

tidal heights (anova

: site height, P< 005, Table 2, Fig. 2),these were mainly due to reduced mortality ofS. 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 influence 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 ofS. glomerata was strongly influenced

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 conspecifics or

Fig. 1. Mean ( 1 SE) mortality of Sydney rock oysters Saccostrea glomerata, and Pacific oysters Crassostrea gigas, 18 months after

manipulation of total oyster density through the addition of Sydney rock oysters (SRO) and/or Pacific oysters (PO) to Perspex plates. Replicates

were pooled within sites (n= 3).


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10 F. R. Krassoiet al.

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

S. glomerata (Table 2, Fig. 1). Across all treatments, however,

C. gigas mortality was strongly influenced 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) ofC. 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 SHAPEOF OYSTERS

The relative growth performance ofS. 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 Pacific oysters Crassostrea gigas, 18 months after



Fig. 2. Mean ( 1 SE) mortality of Sydney rock oysters Saccostrea

glomerata, and Pacific oysters Crassostrea gigas, at Salamander Bay

(S1), Uptons Island (S2) and Wirrung Island (S3) over the 18-month

experiment. n= 5 treatments.


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Condition-specific competition among oysters 11


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 perplate 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 ofC. gigas size was evident across treatments of differ-

ing 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 ofS. 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 significant (anova: height control vs.

others, P> 005, Table 4, Fig. 4).

DiscussionBy affecting fitness 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 con-

sidering the relative strength of intra- vs. interspecific inter-

actions, our study determined competitive interactions betweenthe native Sydney rock oyster, S. glomerata, and the exotic

Pacific 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

Table 3. Analyses of variance examining variation in the size (length width) ofSaccostrea glomerata and Crassostrea gigas among treatments,

sites and tidal heights. Levels of factors are as outlined in Table 2. Terms significant at = 005 are highlighted in bold. Data were analysed

untransformed. n= 3

d.f.

Saccostrea glomerata Crassostrea gigas

MS F P MS F P

Among all treatments 4 2 636 637 811 502

Controls vs. others 1 4 762 582 341


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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 significant at = 005 are highlighted in bold. All data

were ln(x+ 1) transformed prior to analysis. n= 3

d.f.


MS F P MS F P

Among all treatments 4 00017 00010

Controls vs. others 1 00001 02 0649 00031 41 0052

Among others 3 00022 00003

Density 1 00028 59 0021 00000 00 1000

Species 1 00016 34 0076 00008 11 0312

Density species 1 00022 46 0039 00002 03 0611

Height 2 00004 08 0473 00009 12 0313

Height all treatments 8 00002 00006

Height controls vs. others 2 00004 08 0439 00012 16 0221

Height among others 6 00002 00004

Height density 2 00003 06 0538 00000 00 1000

Height species 2 00001 02 0811 00012 15 0235

Height density species 2 00001 01 0900 00000 00 1000

Residual 30 00004 00008


C= 033 (P > 005) C= 030 (P > 005)

Cochrans test Density species

SNK tests SRO: 10 < 20

PO: 10 = 20

10: SRO = PO

20: SRO > PO

Fig. 4. Mean ( 1 SE) shape (width/length) of Sydney rock oysters Saccostrea glomerata, and Pacific oysters Crassostrea gigas, 18 months after




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pattern, evident irrespective of the density ofC. gigas added,

was not replicated by increases in the density ofS. glomerata

on monospecific panels, and coupled with our observation

that mortality of S. glomerata was negligible prior to over-

growth by C. gigas, provides strong evidence for interspecific

competition. By contrast, addition ofS. glomerata to C. gigas

panels had no effect on mortality of the exotic species across

the examined range of densities. Thus, interspecific competition

between the two species was asymmetrical, with the exoticoyster being the dominant species.

Despite the large negative effects ofC. 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 ofC. 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 5090%. Thus, at high intertidal heights the

exotics slower rate of growth and low abundance prevented

overgrowth and smothering ofS. 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 interspecific

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 mayrequire 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 ofS. 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 ofC. gigasprecedes that ofS. 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 intensityof 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 finding 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 m2) 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 rep-

resents the first 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 rateof 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 significant 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

floral and faunal assemblages (see Wells 1961). Similarly,

benthicpelagic coupling and trophic transfer may differ

between native and exotic oysters as a result of differences intheir 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 ofC. gigas significantly changed

the shape (as indicated by width to length ratios) ofS. 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-specific nature of the competition

between C. gigas and S. glomerata resembles that observed in


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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-offbetween 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 field.

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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Received 22 May 2007; accepted 19 August 2007

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