Differences in dispersal of an intertidal gastropod in two habitats: the need for and design of repeated experimental transplantation

Journal of Experimental Marine Biology and Ecology, 237 (1999) 31–60

L

Differences in dispersal of an intertidal gastropod in two habitats: the need for and design of repeated experimental transplantation Tasman P. Crowe a , *, A.J. Underwood b a

b

Institute of Marine Ecology, University of Sydney, Sydney, NSW 2006, Australia Centre for Research into Ecological Impacts of Coastal Cities, Marine Ecology Laboratories A11, University of Sydney, Sydney, NSW 2006, Australia

Received 17 March 1998; received in revised form 5 November 1998; accepted 23 November 1998

Abstract Applying general ecological models to new habitats is made difficult where ecological processes vary from one habitat to another. To improve the generality of such models and the precision of predictions made from them, it is necessary to understand the processes that prevent generalizations. The behaviour of intertidal gastropods (Bembicium auratum) varies from rocky shores to mangrove forests near Sydney (Australia) and creates a barrier to generalization of models from one habitat to the other. Differences in behaviour could result from intrinsic differences in the populations of Bembicium occupying the different habitats or from responses to extrinsic cues that vary from habitat to habitat or from a combination of these factors. To test hypotheses from these three models, Bembicium were reciprocally transplanted between the habitats and their subsequent behaviour was compared to that of controls. Outcomes of the experiment varied considerably in space and time, but there was no evidence of intrinsic differences between populations of snails in the two habitats. Some results suggested that a combination of intrinsic and extrinsic factors causes the observed differences in behaviour. Most results were consistent with the model that differences in behaviour of snails on rocky shores and from that shown in mangrove forests are caused by differences between the two habitats and not the snails. The behaviour of individual Bembicium was extremely plastic and changed rapidly on arrival in a new habitat. Experiments of this type are an effective tool for investigating variation in behavioural processes. The study demonstrated that behavioural plasticity can act as a barrier to generalizations from some ecological models.  1999 Elsevier Science B.V. All rights reserved. Keywords: Gastropod; Dispersal; Transplantation; Behavioural plasticity; Repeated experimentation; Generality *Corresponding author. Present address: School of Biological Science, University of Southampton, Bassett Crescent East, Southampton SO16 7PX, UK. Tel.: 1 44-1703-594384; fax: 1 44-1703-594269. E-mail address: [email protected] (Tasman P. Crowe) 0022-0981 / 99 / $ – see front matter  1999 Elsevier Science B.V. All rights reserved. PII: S0022-0981( 98 )00211-1

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1. Introduction General ecological models are necessary if we are to avoid confronting an endless succession of unique situations (e.g. Underwood and Denley, 1984; Levin, 1989; Tilman, 1989; Peters, 1991; Weiner, 1995), rendering it impossible to make any predictions in novel and often threatened habitats (Simberloff, 1988). Unfortunately, however, there is abundant evidence that ecological systems vary substantially in space and time and that these variations can act as a barrier to the construction of generally applicable models (Caswell, 1976; Underwood and Denley, 1984; Foster, 1990; Steele, 1991; Underwood and Petraitis, 1993). For example, several authors have found that processes in one habitat cannot be used to predict processes in other, related habitats (Martinez and Fuentes, 1993; Haukioja et al., 1994). This suggests that ecological theories that might be used to predict processes in novel habitats will often fail. It is therefore important to understand the sorts of processes that prevent generalizations from one habitat to another (see also, Martinez and Fuentes, 1993; Haukioja et al., 1994). It would then be possible to modify predictions to take account of such processes. This paper deals with a specific example of this approach. There are significant differences between the behaviour of intertidal gastropods (Bembicium auratum Quoy and Gaimard) in mangrove forests near Sydney (Australia) and those inhabiting rocky shores. Specifically, the proportion of Bembicium dispersing from plots of microhabitat (oysters) in mangrove forests after 2 days was smaller and the displaced distances shorter than those of Bembicium dispersing from plots of oysters on rocky shores (Crowe, 1996a; Observation A, Table 1). Also, the dispersal of Bembicium in mangrove forests was never affected by the structure of surrounding microhabitat (Crowe, 1996a,b). On rocky shores, however, the proportion of snails dispersing from plots of oysters was sometimes reduced when plots were isolated from surrounding oysters compared to when plots were continuous with surrounding oysters. Displaced distances were also occasionally affected by the structure of surrounding microhabitat, but were usually greater from isolated plots than from plots continuous with surrounding oysters (Crowe, 1996a; Observation B, Table 1). It is not therefore possible to generalize from simple models developed on rocky shores to predict behaviour of Bembicium in mangrove forests. In the broadest sense, three models could explain the observed differences between behaviour of Bembicium in mangrove forests and on rocky shores. The first is that there are intrinsic (e.g. genetic or learned) differences in the snails that occupy the two habitats, causing them to behave differently. The second is that there are no intrinsic differences in the snails, but that they respond to a different set of cues in each habitat and therefore behave differently. The final model is that some combination of intrinsic and habitat-related factors acts to produce the observed patterns of behaviour. Various methods could be used to identify genetic differences between populations in different habitats (see, for example, Knight and Ward, 1987; Gosling and McGrath, 1990; Brown, 1991), and such work has been done for Bembicium vittatum (Johnson and Black, 1991). Of course, such analyses could never demonstrate whether any differences found were related to the behaviour of the snails. Here, hypotheses were proposed about the behaviour of snails taken from one habitat to the other, relative to controls in each

Observations

Explanatory models

Hypotheses relating to observation A

Hypotheses relating to observation B

(A) Rates of dispersal of snails in mangroves are different from those on rocky shores.

(1) Intrinsic factors: intrinsic differences between populations of Bembicium on rocky shores and in mangrove forests cause them to behave differently.

(B.1) Transplanted snails will respond to structure of surrounding habitat (i) differently from controls in the habitat to which they are taken and (ii) similarly to controls in their habitat of origin.

(B) Responses to structure of microhabitat are different in the two habitats.

(2) Extrinsic factors: different cues in each habitat elicit different behaviour from the individuals that live in them.

(A.1) (from model 1): transplanted snails will retain behaviour characteristic of their habitat of origin and will disperse (i) differently from controls in their new habitat and (ii) similarly to controls in their habitat of origin (A.2) (from model 2): transplanted snails will alter their behaviour in response to cues in the new habitat and will disperse (i) similarly to controls in their new habitat and (ii) differently from controls in their habitat of origin. (A.3) (from model 3): Either, snails transplanted from one of the habitats will behave as predicted in hypothesis A.1 and snails transplanted from the other habitat will behave as predicted in hypothesis A.2; Or, behaviour of transplanted snails will become intermediate between the behaviours in the habitat of origin and that to which they were taken.

(3) Interaction of intrinsic and extrinsic factors: differences in behaviour in the two habitats are caused by an interaction or combination of intrinsic differences in the snails and differences in environmental cues.

(B.2) Transplanted snails will respond to differences in the structure of surrounding microhabitat (i) similarly to controls in their new habitat and (ii) differently from controls in their habitat of origin. (B3) Interactions: it is not possible to articulate a hypothesis to distinguish model 3 from models 1 and 2; see text for details.

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Table 1 Summary of logical structure of experimental transplantations (see text for details)

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habitat. Those hypotheses were tested using reciprocal experimental transplantation. A similar approach has been used to test the heritability of differences in growth rates, morphology and behaviour of littorinids from different geographic locations (BehrensYamada, 1987; Parsons, 1997a,b) and from different phenotypic morphs at a single location (Janson, 1983) (although these studies lacked controls). McKillup (1982) used the technique to compare behavioural responses of littorinids to local and geographically remote predators and Hobday (1995) used it to test hypotheses about differences in the behaviour of limpets living on sheltered and exposed shores. If there are intrinsic differences between Bembicium in the two habitats (Model 1, Table 1), snails transplanted from one habitat to the other should retain behaviour characteristic of their habitat of origin regardless of cues in the new habitat (Hypothesis A.1, Table 1). Under an alternative model that there are no intrinsic differences between populations of Bembicium inhabiting mangroves and rocky shores, transplanted snails should alter their behaviour in response to extrinsic cues in the new habitat (Hypothesis A.2, Table 1). If an interaction of these factors is responsible for the observed differences, the outcomes would either vary from habitat to habitat or the behaviour of transplanted snails would become intermediate between that typical of snails in their new habitat and that of snails in their habitat of origin (Hypothesis A.3, Table 1). These hypotheses are straightforward with respect to the patterns of difference in proportions of Bembicium dispersing, which were consistent in space and time (Crowe, 1996a,b; see Table 1), but are more complex in relation to responses to surrounding microhabitat. Because the previous observations were that snails on rocky shores sometimes responded to the structure of surrounding microhabitat, it is not possible to make unequivocal predictions of the behaviour of transplanted snails in relation to surrounding microhabitat for any single experiment. Essentially, the only relevant results are those in which differences in response to different levels of surrounding microhabitat do arise, particularly in transplanted snails. For example, if snails transplanted to rocky shores from mangrove forests do not respond to the structure of surrounding microhabitat, it may be because they are intrinsically different from snails from rocky shores. Alternatively, they may be responding to cues on rocky shores, but, on that occasion and on those plots, the appropriate response was to disperse at equal rates from both types of plot. On the other hand, if snails transplanted from mangroves to rocky shores do respond to the structure of surrounding microhabitat, then they must be responding to cues on rocky shores and cannot be considered to be behaving as mangrove inhabitants. Under these circumstances, it is not possible to articulate a sensible hypothesis that would distinguish model 3 from models 1 and 2. In order to use responses to structure of surrounding microhabitat to distinguish between the alternative models, it would be necessary to phrase hypotheses in terms of the frequency of outcomes of the different types described above and then do a large series of experiments to accumulate the necessary volume of results. Although rarely articulated in this way, this situation is not unusual in ecology. Processes often vary through space and time, and there have long been calls for greater repetition of experiments to enable accurate interpretation against a background of variability (Connell and Sousa, 1983; Elner and Vadas, 1990; Underwood, 1997; and see Underwood and Chapman, 1992 for a specific example).

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An experiment to distinguish among the alternative hypotheses was done which required manipulations at two sites on rocky shores and two sites in mangrove forests. Each of these sites provided a result that could be individually assessed against the hypotheses. The experiment was run on two occasions in order to accumulate eight sets of experimental results, so that the overall interpretation could take account of spatial and temporal variations in the outcome.

2. Methods A reciprocal experimental transplantation was done in which snails were transplanted from two sites on estuarine rocky shores to plots at two sites in mangrove forests and vice versa (Transplantation TP, see Fig. 1 and Table 2). The sites were rocky shores, Port Hacking (PH) and Broken Bay (BB); mangrove forests, Woolooware Bay (WW) and Patonga (PT). The sites from the different habitats are geographically interspersed along the coast of central New South Wales (Australia) and were described in Crowe (1996a). In order to distinguish between the effect of the new habitat on the behaviour of the snails and the effect of simply being moved to a new site, it was also necessary to translocate snails to the other sites within the habitats of origin (Chapman, 1986; Underwood, 1986, 1988; Translocation 1 TL, see, Fig. 1 and Table 2). A comparison of these two treatments provides a direct test of the hypotheses. The results of such a comparison would, however, only relate to animals that had been moved over great distances and placed in unfamiliar surroundings. To be able to interpret the results in terms of the behaviour of natural populations of unmanipulated snails, it was necessary to incorporate controls to identify any artifacts of these manipulations. The primary requirement is to compare behaviour of manipulated snails with that of members of the unmanipulated population. To measure the behaviour of unmanipulated animals, an ‘undisturbed’ treatment was done (Undisturbed U, Table 2, details given below). Any differences between experimental and undisturbed snails could be attributable to several aspects of the experimental manipulation (Chapman, 1986; Underwood, 1986, 1988; Crowe, 1996a). First, behaviour could be altered by the fact that snails have been relocated to an unfamiliar site where large-scale behavioural cues (e.g. tidal regime, water chemistry, etc.) could have been different. To control for this, a treatment was included in which snails were translocated to plots at the site in which they were originally found (Translocation 2 TL2, see Table 2), where, as predicted by some hypotheses, large-scale cues would not be changed. The animals to be transplanted (TP) and translocated (TL and TL2) were collected on one day and had to be held for 36 h in the laboratory for marking before being taken to plots at appropriate sites (Table 3). It was therefore necessary to test the null hypothesis that there was no effect of storing the snails in the laboratory overnight. To achieve this, dispersal of snails that had been stored overnight and subsequently placed on plots at the same site at which they had been collected was compared with the dispersal of snails that were not taken to the laboratory overnight, but were instead collected on the day of the experiment (Day 3,

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Fig. 1. Schematic diagram to show treatments involving transport of snails from one location to another (i.e. Transplantation and Translocation 1). For the other treatments (TL2, TL3 and U), snails were placed on plots at the location at which they were collected (see Table 2). Dark hatching, rocky shore; light hatching, mangrove forest; TP, transplantation; TL, translocation; PH, Port Hacking; BB, Broken Bay; WW, Woolooware; PT, Patonga. * Note: half of the snails taken to each location originated from each of the two locations in the other habitat. For example, five snails from Port Hacking and five snails from Broken Bay were taken to each plot assigned to the transplantation treatment at each of Woolooware and Patonga.

Table 3), marked in the field and translocated to plots at the site at which they had been collected (Translocation 3, TL3, see Table 2). Inclusion of one final control would have enabled the evaluation of the effect on the snails’ behaviour of disturbance caused by experimental handling, as distinct from the effect of being moved over short distances to areas of unfamiliar microhabitat or being kept in the laboratory. This ‘disturbance’ control involves picking up snails, marking them and replacing them on the plot from which they had been removed (Chapman, 1986; Underwood, 1986, 1988; Crowe, 1996a). There were insufficient plots available for this treatment to be done during this experiment. Previous experiments in which this

Table 2 Manipulations for each treatment, using the rocky shore at Port Hacking (PH) as an example (see text for further explanation) Snails taken from PH go to:

Transplantation Translocation 1 Translocation 2 Translocation 3 Undisturbed

TP TL TL2 TL3 U

Woolooware / Patonga Broken Bay Port Hacking Port Hacking Port Hacking

a

Snails moved to PH come from: Woolooware / Patonga Broken Bay Port Hacking Port Hacking Port Hacking

b

Held overnight in laboratory? Yes Yes Yes No No

a

Half of the snails collected from Port Hacking for transplantation were taken to plots at Woolooware Bay and the other half were taken to plots at Patonga (see Fig. 3). b Conversely, snails arriving at plots assigned to the transplantation treatment were a mixture of animals from each of the two locations in the other habitat.

Table 3 Schedule of manipulations for the different treatments Treatment

Day 1

Day 2

Day 3

Day 5

TP TL TL2 TL3 U

N snails collected N snails collected N snails collected No manipulations done on that day kN snails collected, marked, released on plots

Marked in laboratory Marked in laboratory Marked in laboratory No manipulations done on that day No manipulations done on that day

Released on plots Released on plots Released on plots N snails collected, marked, released Marked snails cleared from surrounding area. Those on plots left untouched

Recaptured Recaptured Recaptured Recaptured Recaptured

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Treatment

N, ten adult snails; k (constant) 5 three for rocky shores and two for mangrove forests.

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control had been included found no effect of this manipulation (Crowe, 1996a,b). Although this does not strictly justify the omission of the treatment, it was impossible to include in the present experiments. It was assumed that previous results were a good guide to there being no confounding influences relative to those aspects of the manipulation. Experimental plots were 15 3 15 cm patches of oysters. In order to test hypotheses B.1 and B.2, the plots used in the experiment were of two types: ‘continuous’ and ‘isolated’. Continuous plots were in contact with surrounding oysters and isolated plots were separated from surrounding oysters by a halo of primary substratum (rock on rocky shores and mud / pneumatophores in mangrove forests) (see, Crowe (1996a) for further details). Three continuous and three isolated plots were randomly assigned to each treatment at each of the four sites (a total of 15 plots at each site). Ten snails $ 10 mm in diameter were placed on each plot for the treatments TP, TL, TL2 and TL3. This represents the average density of Bembicium in mangrove forests and somewhat less than the average density on rocky shores (Crowe, 1996a). The undisturbed control is usually done by painting snails in situ without picking them up (Chapman, 1986). In this case, however, the fact that the snails live cryptically among the folds of oysters made it impossible to paint individuals in situ. It was therefore necessary to use a variant on that theme. The Chapman (1992) data suggested that littorinids have only a short-lived reaction to disturbance and return to their natural patterns of behaviour within two days. Based on this evidence, it was assumed for the purpose of this experiment that snails that had been painted two days previously would be effectively ‘undisturbed’ on the day of the experiment. An excess of snails was therefore painted on Day 1 and placed on each plot assigned to this treatment (see Table 3). The aim was to place appropriate numbers of snails on the plots, such that densities similar to those used on experimental plots would still be there on Day 3. On Day 3, those that had dispersed were cleared from the surrounding area. That number subtracted from the original number placed was used to estimate the number of snails still on the plot. The snails remaining on the plots were left untouched (Table 3). Limitations of this method are discussed in Crowe (1996a). The snails placed on plots assigned to the transplantation treatment were of mixed origin: half from each of the sites in the other habitat. For example, of the ten transplanted snails arriving at each plot in Port Hacking, five were from Woolooware Bay and five were from Patonga Creek. Ideally, separate sets of plots would have been used at each site to determine any differences between the two sites in the other habitat. There were, however, insufficient plots to do this. Mixing the snails together was considered to be the best way to ensure that transplanted snails were generally representative of the other habitat rather than of a specific site within that habitat. In addition, this design ensured that they could be said to arrive in the other habitat rather than at a specific site in that habitat. The alternative would have been, for example, to transplant snails from Broken Bay to Patonga, snails from Port Hacking to Woolooware and vice versa. In this case, alterations to the behaviour of the snails could have been the result of interactions among cues specific to the sites rather than to the habitats as a whole. The experiment would then have been more difficult to interpret. Procedures for collecting and marking the snails and for collecting data were exactly

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as described in Crowe (1996a). Snails marked in the laboratory were taken to the field in sealed labelled plastic bags, one bag per plot. Manipulations were done simultaneously (during the same period of low-water) at four sites separated by up to 110 km (by road and sea). Two people did the manipulations at Patonga and Broken Bay (to the north of Sydney) and two others worked at Port Hacking and Woolooware Bay (to the south). Plots were emersed for only 5–6 h during a single low tide, so work had to be completed within | 2 h, leaving an hour to travel between sites. This was done three times (Days 1, 3 and 5; see Table 3). The limited time available made it necessary to reduce the volume of data collected: the percentage of snails that had dispersed from each plot was recorded, but displaced distances were only measured for snails from two of the three plots for each treatment at each site. The experiment was done twice: in January 1994 and in February 1995. There was substantial mortality of snails during the first run of the experiment, so the procedure was modified for the second run. The marked snails were transported from the laboratory to the field in moist calico bags (one bag per plot) and kept in a cool-box until they were deployed. Once placed on the plots they were sprayed with sea-water to moisten them and stimulate them to become active for long enough to attach firmly to the substratum.

3. Results

3.1. Analysis In order to distinguish between the alternative hypotheses, it was necessary to do two types of analyses, by ‘destination’ and by ‘origin’. To distinguish hypothesis A.1(i) from hypothesis A.2(i) and hypothesis B.1(i) from B.2(i), the behaviour of snails transplanted to a site was compared with the behaviour of those translocated to and within it (analysis by destination). In addition, to distinguish hypothesis A.1(ii) from hypothesis A.2(ii) and hypothesis B.1(ii) from B.2(ii), the behaviour of transplanted snails originating in a site was compared with that of those translocated from and within it (analysis by origin). Results are presented and analysed in each of these ways for each of the variables ‘percentage dispersal’ and ‘displaced distance’, i.e. the distance to where the snail was finally found (see Underwood and Chapman, 1992; Crowe, 1996a). Data from treatments TL2, TL3 and U are the same in each of the two graphs / analyses. Because snails from two sites were transplanted together to each of two sites in the other habitat, it is not possible to distinguish the site of origin of any individual transplanted snail. The transplanted snails moved to the two sites in a habitat were in part derived from each of the sites in the other habitat. Thus, in graphs comparing behaviour by origin, data for transplanted snails arriving in each of the sites in the other habitat are shown. It was, however, not possible to do one overall analysis of these data in this way because the data from the transplanted plots would have been used more than once in the same analysis (for example the data for transplanted snails arriving at Port Hacking would appear among the treatments originating from Woolooware and those from Patonga; see Fig. 7a, Fig. 8a, Fig. 9a). Two separate analyses were therefore done: one for the snails

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originating from Port Hacking and Woolooware and one for snails originating from Broken Bay and Patonga. Analyses of displaced distances were similar to those for percentage dispersal, but the additional factor ‘plot’ was incorporated. Displaced distances were measured for two of the three plots assigned to each treatment. In the event, from six to ten snails were recaptured from each plot. In order to simplify the analyses, the design was balanced with n set to seven individual measurements per plot. For plots with more than seven replicate measurements, excess data were randomly rejected. For the three plots with only six replicate measurements, the mean of the available data was used as an additional replicate to make up the shortfall and the appropriate number of degrees of freedom was then subtracted from the residual (Winer et al., 1991). The use of a subset of all available measurements could conceivably affect the outcome of the analysis, particularly if some of the means estimated by the subset were very different from the means estimated by all the available data. To examine this, a regression was done of the mean values from the randomly-chosen subset and the mean values from all the data (Fig. 2). 97% of variation in the estimates using subsets of data was accounted for by estimates using all available data and there were no obvious outliers (Fig. 2). In some cases, only one or two snails remained on ‘undisturbed’ plots on Day 3 (particularly at Port Hacking), rendering it meaningless to measure ‘percentage dispersal’ on Day 5. In other cases, shortage of time prevented the completion of all three replicates or made it impossible to search thoroughly for snails on Day 3. Data

Fig. 2. Verification of the validity of randomly selecting a subset of displaced distance data. Regression of mean displaced distance as estimated by a randomly selected subset of data (n 5 7) against the mean displaced distance for the same plot as estimated using all available data (n varied from 6 to 10). y 5 2 0.32 1 1.03x, n 5 64, r 2 5 0.97.

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from these plots were therefore either unavailable or unreliable. The number of replicate plots in the ‘undisturbed’ treatment thus varied from zero to three and the numbers of individuals for which displaced distances were measured were as small as one or two per plot. Balancing designs for analyses to compare the behaviour of undisturbed snails with that of snails in other treatments would have required the loss of too much data and thus no formal analysis of this sort was done. Available data from undisturbed plots are nevertheless presented on all figures for visual comparison with the other treatments.

3.2. Interpretation of results Model 1 predicts that transplanted snails should retain behaviour typical of snails in their habitat of origin and unlike that of animals in the habitat to which they have been taken. Snails transplanted to a rocky shore from mangrove forests (TP) will disperse in smaller proportions and over smaller distances than controls translocated from a different rocky shore (TL) or from areas of the same rocky shore (TL2, TL3; Fig. 3a), i.e. they will continue to behave like snails in the mangrove habitat from which they came. There may be some difference according to whether the surrounding microhabitat was continuous or isolated for snails originating on rocky shores (TL, TL2, TL3 and U), but no effect on snails that originated in mangrove forests (TP; Fig. 3a). Conversely, snails transplanted from a rocky shore to mangrove forests (TP) will disperse in the same proportions and over the same distances as controls translocated from that rocky shore to another shore (TL) or to plots on the same shore (TL2, TL3; Fig. 3b). Transplanted snails (TP) should also respond to structure of microhabitat in mangrove forests in the same way as do controls that remain on rocky shores (TL, TL2, TL3, U; Fig. 3b). The obverse pattern would be predicted for a mangrove forest site. There should be differences among treatments (or significant interactions involving the term ‘treatment’) in analyses of dispersal of snails taken to a site (analyses by destination) and no differences among treatments (or interactions involving ‘treatment’) in analyses of dispersal of animals taken from a site (analyses by origin). Model 2 predicts that behaviour of transplanted animals should change rapidly to become like that of controls in the habitat to which they are taken (Fig. 4a). Their behaviour should change to be different from that of animals translocated within their habitat of origin (a rocky shore in the example illustrated in Fig. 4b). Snails transplanted to a rocky shore from mangrove forests (TP) will disperse in the same proportions and over the same distances as controls translocated from a different rocky shore (TL) or from areas of the same rocky shore (TL2, TL3; Fig. 4a). In addition, there may be the same effect of structure of microhabitat on snails taken to rocky shores from mangrove forests (TP) as for snails originating on rocky shores (TL, TL2, TL3 and U; Fig. 4a). Conversely, snails transplanted from a rocky shore to mangrove forests (TP) will disperse in smaller proportions and over smaller distances than controls translocated from that rocky shore to another rocky shore (TL) or to plots on the same shore (TL2, TL3; Fig. 4b). In contrast to snails remaining on rocky shores (TL, TL2, TL3 and U), there should never be any difference due to structure of surrounding microhabitat for snails transplanted to mangrove forests (TP; Fig. 4b). Again, the obverse pattern would be predicted for a mangrove forest site. There should be no differences among

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Fig. 3. Hypothetical outcome predicted by model 1 (intrinsic differences) for a rocky shore. Note: in previous experiments, snails in mangrove forests dispersed less than those on rocky shores and snails on rocky shores sometimes dispersed less from isolated than from continuous plots. (a) Treatments in which snails are taken to plots on that shore from: mangrove forests (TP), another rocky shore (TL) and other areas on the same shore (TL2, TL3, U); (b) Treatments in which snails are taken from that shore to mangrove forests (TP), another rocky shore (TL) and to plots on the same shore (TL2, TL3, U). Treatments are explained fully in text (see Section 2); shading is used only for consistency with later figures.

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Fig. 4. Hypothetical outcome predicted by model 2 (extrinsic differences) for a rocky shore. Note: in previous experiments, snails in mangrove forests dispersed less than those on rocky shores and snails on rocky shores sometimes dispersed less from isolated than from continuous plots. (a) Treatments in which snails are taken to plots on that shore from: mangrove forests (TP), another rocky shore (TL) and other areas on the same shore (TL2, TL3, U); (b) Treatments in which snails are taken from that shore to mangrove forests (TP), another rocky shore (TL) and to plots on the same shore (TL2, TL3, U). Treatments are explained fully in text (see Section 2); shading is used only for consistency with later figures.

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treatments (or interactions involving the term ‘treatment’) in analyses by destination and clear differences among treatments (or interactions involving ‘treatment’) in analyses by origin.

3.2.1. Summary of outcomes supporting each model None of the experimental results supported model 1: ‘intrinsic differences’ (Table 4). The largest number of outcomes was in favour of model 2: ‘extrinsic differences’, but results from Port Hacking and from isolated plots at the other sites in 1995 were consistent with those predicted by model 3: ‘interaction between intrinsic and extrinsic factors’ (Table 4). There were also four separate instances of responses to structure of surrounding microhabitat that were consistent with predictions from model 2 and none in support of model 1 (Section 3.2.5). Individual outcomes in support of each model are described in detail below. There were significant differences among plots in several analyses of displaced distances (Table 5b, Table 6b). Multiple comparisons were not done for this factor. Data for plots at Patonga and Broken Bay in 1994 were extremely patchy, because of the death or disappearance of many experimental snails. No graphs or analyses are therefore presented for these sites. Data for plots in Port Hacking and Woolooware were successfully collected and the graphs showing behaviour of snails in those sites are complete. Some snails originating in those sites were, however, transplanted or translocated to Patonga and Broken Bay and many died or disappeared. Therefore, it was not possible to do complete analyses of the behaviour of snails originating in Woolooware and Port Hacking. Analyses of the subset of treatments that were available were done, but interpretations of artifacts were equivocal because of the missing data. For the transplanted and translocated plots at Patonga and Broken Bay, an estimate of dispersive behaviour was obtained by calculating the percentage dispersal of the combined survivors from all three plots. This percentage is plotted on the appropriate graphs, allowing visual comparisons to be made. 3.2.2. Evidence consistent with model 1: intrinsic factors This model was not supported by data from any site during either of the two runs of the experiment (Table 4). Table 4 Summary of the outcomes of reciprocal transplantation experiments in terms of the models supported Result provides support for: Intrinsic

Extrinsic

Interaction

PH 1994 Continuous PH 1994 Isolated WW 1994 Continuous WW 1994 Isolated WW 1995 Continuous PT 1995 Continuous

PH 1995 Continuous PH 1995 Isolated BB 1995 Isolated PT 1995 Isolated WW 1995 Isolated

PH, Port Hacking; BB, Broken Bay; WW, Woolooware; PT, Patonga. Continuous and Isolated are the two types of structure.

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Table 5 Analyses by destination: (a) analyses of percentage dispersal of Bembicium, and (b) analyses of displaced distances of Bembicium placed on plots at (i) Port Hacking and Woolooware in 1994, (ii) all locations in 1995 a (i) Source of variation (a) Site (S) Isolation (I) Treatment (T) S3I S3T I3T S3I3T Residual

(b) Site (S) Isolation (I) Treatment (T) Plot [P(S 3 I 3 T)] S3I S3T I3T S3I3T Residual

(ii) df

MS

F

1 1 3 1 3 3 3 32

14 352.08 2552.08 546.53 1302.08 1385.42 318.75 68.75 254.17

56.47*** 1.96 0.39 5.12* 5.45** 4.64 0.27

1 1 3 16 1 3 3 3 189 c

257.12 0.21 7.48 1.46 0.16 6.44 4.50 0.72 1.66

176.55*** 1.35 1.16 0.89 0.11 3.87* b 6.24 0.50

Source of variation Habitat (H) Site (S(H)) Isolation (I) Treatment (T) H3I H3T S(H) 3 I S(H) 3 T I3T H3I3T S(H) 3 I 3 T Residual Habitat (H) Site (S(H)) Isolation (I) Treatment (T) Plot [P(H 3 S 3 I 3 T)] H3I H3T S(H) 3 I S(H) 3 T I3T H3I3T S(H) 3 I 3 T Residual

df

MS

F

1 2 1 3 1 3 2 6 3 3 6 64

11 484.37 1855.21 3037.50 2678.82 1204.17 734.37 1687.50 249.65 1140.28 640.28 168.06 392.19

6.19 4.73* 1.80 10.73** 0.71 2.94 4.30* 0.64 6.79* 1.65 0.43

1 2 1 3 32 1 3 2 6 3 3 6 381 c

133.17 9.62 10.48 31.35 3.28 25.64 3.01 23.95 2.70 6.62 10.96 6.14 1.90

13.85 2.93 0.44 11.61** 1.72* 1.07 1.12 7.30** 0.82 1.08 1.78 1.87

a Dispersal of transplanted (TP) and translocated (TL) snails moved to each site is compared with dispersal of snails translocated within that site (TL2 and TL3). In analysis (i), data were only available for Wooloware and Port Hacking due to mortality of snails at Patonga and Broken Bay. (a) n 5 3 plots; data are untransformed; Cochran’s test: ns. (b) n 5 7 individuals; data are transformed, X9 5 Log e (X 1 1); Cochran’s test: ns. b Tested over residual after elimination of P(L 3 I 3 T) which was ns, p . 0.25. c Residual df reduced by three to compensate for missing data. * Denotes significance at p , 0.05; ** denotes significance at p , 0.01; *** denotes significance at p , 0.001.

3.2.3. Evidence consistent with model 2: extrinsic factors Clear support for this model was provided by results in 1994 from Port Hacking and from Woolooware and again from Woolooware in 1995 and isolated plots at Patonga in 1995 (Table 4). In 1994, snails taken to rocky habitat at Port Hacking from mangrove forests dispersed at rates similar to or greater than those of snails that had been translocated from other rocky areas in Broken Bay or within Port Hacking (Fig. 5a,b; Table 5a(i), S 3 T**; TP 5 TL 5 TL2 5 TL3 at PH, SNK test, p . 0.05; Table 5b(i), S 3 T*; TP . TL 5 TL2 5 TL3 at PH, SNK test, p , 0.05). Percentage dispersal was 80–100%

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Table 6 Analyses by origin: (a) analyses of percentage dispersal of Bembicium and (b) analyses of displaced distances of Bembicium originating from, (i) Port Hacking and Woolooware in 1994, (ii) Port Hacking and Woolooware in 1995, and (iii) Broken Bay and Patonga in 1995 a Source of variation

(i) df

(ii) MS

F

1 1 2 1 2 2 2 24

336.11 1225.00 602.78 469.44 8019.44 325.00 252.78 280.56

1.20 2.61 0.08 1.67 28.58*** 1.29 0.90

1 1 4 1 4 4 4 40

(b) Site (S) 1 Isolation (I) 1 Treatment (T) 2 Plot [P(S 3 I 3 T)] 12 S3I 1 S3T 2 I3T 2 S3I3T 2 Residual 144

18.26 0.88 9.22 1.78 0.25 117.96 3.17 0.62 1.66

10.28** 3.46 0.08 1.07 0.14 66.43*** 5.11 0.35

1 1 4 20 1 4 4 4 237 b

(a) Site (S) Isolation (I) Treatment (T) S3I S3T I3T S3I3T Residual

df

(iii) MS 2160.00 2160.00 1844.17 0.00 2989.17 830.83 145.83 358.33 6.58 17.55 16.65 3.58 0.16 25.04 14.62 1.81 2.02

F

df 6.03* 0.00 0.62 0.00 8.34*** 5.70 0.41

1.84 109.21 0.67 1.77* 0.04 6.99** 8.06* 0.51

1 1 4 1 4 4 4 40 1 1 4 20 1 4 4 4 237 b

MS

F

240.00 375.00 1514.17 1041.67 1919.17 1308.33 633.33 390.83

0.61 0.36 0.79 2.67 4.91** 2.07 1.62

11.19 0.18 19.23 3.39 22.93 25.17 14.00 13.13 1.92

3.30 0.01 0.76 1.77* 6.76* 7.42*** 1.07 3.87*

a

Dispersal of snails that were transplanted (TP) from a location is compared with dispersal of snails translocated within that location (TL2 and TL3). In analysis (i), only one transplantation (as opposed to two in analyses (ii) and (iii)) and no translocation (TL) treatments were analysed due to mortality of snails at Broken Bay and Patonga. See text for further details. (a) n 5 3 plots; data are untransformed; Cochran’s test: ns. (b) n 5 7 individuals; data are transformed, X9 5 Log e (X 1 1); Cochran’s test: ns. b Residual df reduced by three to compensate for missing data. * Denotes significance at p , 0.05; ** denotes significance at p , 0.01; *** denotes significance at p , 0.001.

over the two days. Conversely, snails from rocky shores in Port Hacking that had been transplanted to mangrove forests exhibited reduced dispersal (both in terms of percentage dispersal and displaced distances) compared to those that were translocated within Port Hacking (Fig. 5c,d; 5a(i), S 3 T***; TP , TL2 5 TL3, SNK test, p , 0.05; Table 6b(i), S 3 T***; TP , TL2 5 TL3 at PH, SNK test, p , 0.05) and also, apparently, compared to those translocated to Broken Bay (Fig. 5c). Thus, snails transplanted to or from Port Hacking had changed their behaviour to match that of snails already in the habitat to which they were taken. This suggests that any intrinsic differences between snails in the two habitats are quickly over-ridden by responses to environmental cues in whichever habitat the snails are placed. In 1994, snails taken to Woolooware from rocky shores dispersed at the same slow rate ( ¯ 50% on average over two days) as did snails translocated to Patonga or within Woolooware (Fig. 6a; Table 5a(i), S 3 T*; TP 5 TL 5 TL2 5 TL3 at WW, SNK test, p , 0.05). Similarly, snails were generally less than 20 cm from plots at Woolooware for

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Fig. 5. (a) Percentage dispersal, and (b) displaced distances of Bembicium in rocky habitat at Port Hacking, January 1994. Snails originated from the sites indicated and were moved to or within Port Hacking. Transplanted snails were of mixed origin; from mangroves at Woolooware and Patonga (see text). (c) Percentage dispersal and (d) displaced distances of snails originating from Port Hacking, January 1994. Snails originated in Port Hacking and were moved to the sites indicated. Dark hatching, TP; grey hatching, TL; cross hatching, TL2; light hatching, TL3; clear, U. PH, Port Hacking; BB, Broken Bay; WW, Woolooware; PT, Patonga. For (a) and (b), mean percentages dispersed after 2 days (1S.E.) are shown. Initial density was ten per plot except for U, where initial density was variable. n 5 3 plots, except where indicated by numbers above S.E. bars. a–d Snails transplanted to mangroves at Patonga and translocated to rocky habitat at Broken Bay suffered great mortality (see text). The data presented are the percentages of the total number of survivors that had dispersed and are for visual comparison only. Total numbers of survivors were 9, 14, 17 and 12, respectively. For (c) and (d), mean displaced distance after 2 days (1S.E). for each of two plots per treatment are shown. Initial density was 10 per plot except for U, where initial density was variable. n 5 7 snails.

all treatments including transplanted snails brought from rocky shores (Fig. 6b, Table 5b(i), S 3 T*; TP 5 TL 5 TL2 5 TL3 at WW, SNK test, p . 0.05). Displaced distances of transplantees placed on plots isolated from surrounding oysters appeared to be greater than those of snails in the other treatments (Fig. 6b), but this trend was not significant (Table 5b(i)) and distances moved by these snails were considerably smaller than those recorded at Port Hacking (where snails dispersed further than 25 cm on average: Fig. 5b). Snails that were transplanted from Woolooware to Port Hacking dispersed at greater rates and travelled greater distances than those that were translocated within Wooloo-

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Fig. 6. (a) Percentage dispersal and (b) displaced distances of Bembicium in mangroves at Woolooware, January 1994. Snails originated from the sites indicated and were moved to or within Woolooware. Transplanted snails were of mixed origin; from rocky habitat at Port Hacking and Broken Bay (see text). (c) Percentage dispersal and (d) displaced distances of snails originating from Woolooware, January 1994. Snails originated in Woolooware and were moved to the sites indicated. Dark hatching, TP; grey hatching, TL; cross hatching, TL2; light hatching, TL3; clear, U. PH, Port Hacking; BB, Broken Bay; WW, Woolooware; PT, Patonga. NA, data unavailable (see text). For (a) and (c), mean percentages dispersed after 2 days (1S.E.) are shown. Initial density was 10 per plot except for U, where initial density was variable. n 5 3 plots, except where indicated by numbers above S.E. bars. a–c Snails transplanted to rocky habitat at Broken Bay and translocated to mangroves at Patonga suffered great mortality (see text). The data presented are the percentages of the total number of survivors that had dispersed and are for visual comparison only. Total numbers of survivors were 5, 12, and 8, respectively. For (b) and (d), mean displaced distances after 2 days (1S.E.) for each of 2 plots per treatment are shown. n 5 7 snails.

ware (Fig. 6c,d; Table 6a(i), S 3 T***; TP . TL3 . TL3 at WW, SNK test, p , 0.01; Table 6b(i), S 3 T***; TP . TL2 5 TL3 at WW, SNK test, p , 0.01). In 1995, the pattern on continuous plots in mangrove habitat at Woolooware was very much the same as that seen in 1994. The percentage dispersal of snails taken to Woolooware from rocky shores (TP) was indistinguishable from that of snails translocated from Patonga (TL) or within Woolooware (TL2 and TL3; Fig. 7a; Table 5a(ii), I 3 T*; but TP 5 TL 5 TL2 5 TL3 for continuous plots, SNK test, p . 0.05). The displaced distances of transplanted snails moved to continuous plots at Woolooware also appeared to be very similar to those of translocated snails (Fig. 7b). They were considerably smaller than those observed on rocky shores (Fig. 9b. Fig. 10b), again consistent with the predictions of model 2. Analysis of variance failed, however, to detect a significant S(H) 3 I 3 T interaction (Table 6b(ii)) and there was an overall difference between transplanted snails and those in other treatments (Table 6b(i), T*;

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Fig. 7. (a) Percentage dispersal, and (b) displaced distances of Bembicium in mangroves at Woolooware, February 1995. Snails originated from the sites indicated and were moved to or within Woolooware. Transplanted snails were of mixed origin; from rocky habitat at Port Hacking and Broken Bay (see text). (c) Percentage dispersal, and (d) displaced distances of snails originating from Woolooware, February 1995. Snails originated in Woolooware and were moved to the sites indicated. Dark hatching, TP; grey hatching, TL; cross hatching, TL2; light hatching, TL3; clear, U. PH, Port Hacking; BB, Broken Bay; WW, Woolooware; PT, Patonga. For (a) and (c), mean percentages dispersed after 2 days (1S.E.) are shown. Initial density was 10 per plot except for U, where initial density was variable. n 5 3 plots, except where indicated by numbers above S.E. bars. For (b) and (d), mean displaced distances after 2 days (1S.E.) for each of two plots per treatment are shown. Initial density was 10 per plot except for U, where initial density was variable. n 5 7 snails.

TP . TL 5 TL2 5 TL3, SNK test, p , 0.05). The trend should therefore be interpreted with caution. Snails transplanted from Woolooware to rocky shores showed increased dispersal relative to snails translocated to other mangrove habitat in Patonga or within Woolooware (Fig. 7c,d; Table 6a(ii), S 3 T*; TP1 5 TP2 . TL 5 TL2 5 TL3 at WW, SNK test, p , 0.01; Table 6b(ii), S 3 T**; TP1 5 TP2 . TL 5 TL2 5 TL3 at WW, SNK test, p , 0.05). There was no significant difference in percentage dispersal of transplanted snails arriving on continuous plots in Patonga (1995) compared to snails translocated from Woolooware or within Patonga (Fig. 8a; Table 5a(ii), I 3 T*; TP 5 TL 5 TL2 5 TL3, SNK test, p . 0.05). As described above, in the analysis of displaced distances, the S(H) 3 I 3 T interaction was not significant (Table 5b(i)) and there was an overall difference between transplanted snails and those in other treatments (Table 6b(ii), T*; TP . TL 5 TL2 5 TL3, p , 0.05) indicating that transplanted snails finished up displaced by consistently greater distances than those in other treatments. Nevertheless, the displaced distances of transplanted snails moved to continuous plots at Patonga are clearly as small as those of snails that originated in mangrove forests (Fig. 8b). This

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Fig. 8. (a) Percentage dispersal, and (b) displaced distances of Bembicium in mangroves at Patonga, February 1995. Snails originated from the sites indicated and were moved to or within Patonga. Transplanted snails were of mixed origin; from Port Hacking and Broken Bay (see text). (c) Percentage dispersal, and (d) displaced distances of snails originating from Patonga, February 1995. Snails originated in Patonga and were moved to the sites indicated. Dark hatching, TP; grey hatching, TL; cross hatching, TL2; light hatching, TL3; clear, U. PH, Port Hacking; BB, Broken Bay; WW, Woolooware; PT, Patonga. For (a) and (c), mean percentages dispersed after 2 days (1S.E.) are shown. Initial density was 10 per plot except for U, where initial density was variable. n 5 3 plots, except where indicated by numbers above S.E. bars. For (b) and (d), mean displaced distances after 2 days (1S.E.) for each of two plots per treatment are shown. Initial density was 10 per plot except for U, where initial density was variable. n 5 7 snails.

aspect of behaviour thus appears to have been changed in response to cues at Patonga. In addition, snails transplanted from Patonga to rocky shores subsequently dispersed more than those that were translocated to Woolooware or within Patonga, presumably in response to cues at the sites on rocky shores (Fig. 8c,d; Table 5a(iii), S 3 T*; TP1 5 TP2 . TL 5 TL2 5 TL3 at PT, SNK test, p , 0.05; Table 6b(iii), S 3 I 3 T*; TP1 5 TP2 . TL 5 TL2 5 TL3 for continuous plots at PT, SNK test, p , 0.05).

3.2.4. Evidence consistent with model 3: interaction of intrinsic and extrinsic factors Several outcomes supported this model in the sense that snails taken to rocky shores from mangrove forests exhibited increased dispersal, but the reverse was not true. Snails transplanted to mangrove forests continued to disperse at rates similar to those of snails translocated within the rocky shore habitat and greater than those of snails translocated between and within sites in mangrove forests. This suggests that something intrinsic to snails inhabiting rocky shores causes them to disperse at great rates regardless of the habitat they are in. Mangrove snails, in contrast, respond to cues that prompt them to

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51

disperse greatly on rocky shores and little in mangrove forests. This pattern was observed in 1995 at Port Hacking (both continuous and isolated plots) and for continuous plots at Patonga and Broken Bay (Table 4). Snails transplanted to Port Hacking from mangrove forests in 1995 dispersed at rates either equivalent to or greater than those of snails translocated from Broken Bay or within Port Hacking (Fig. 9a,b; Table 5a(ii) TP 5 TL 5 TL2 5 TL3 for continuous plots, SNK test, p . 0.05, TP . TL 5 TL2 5 TL3 for isolated plots, SNK test, p . 0.05; Table 5b(ii), T**; TP . TL 5 TL2 5 TL3, SNK test, p . 0.05). Snails transplanted from Port Hacking to mangrove forests, on the other hand, did not change their behaviour relative to controls moved within the rocky shore habitat. They continued to disperse in relatively large numbers, 70% (approx.) on average (Fig. 9c; Table 6a(ii), S 3 T***; TP1 5 TP2 5 TL 5 TL2 5 TL3 at PH, SNK test, p , 0.05). They also moved over distances similar to the approximately 25 cm displaced by snails translocated within the

Fig. 9. (a) Percentage dispersal, and (b) displaced distances of Bembicium in rocky habitat at Port Hacking, February 1995. Snails originated from the sites indicated and were moved to or within Port Hacking. Transplanted snails were of mixed origin; from mangroves at Woolooware and Patonga (see text). (c) Percentage dispersal, and (d) displaced distances of snails originating from Port Hacking, January 1994. Snails originated in Port Hacking and were moved to the sites indicated. Dark hatching, TP; grey hatching, TL; cross hatching, TL2; light hatching, TL3; clear, U. PH, Port Hacking; BB, Broken Bay; WW, Woolooware; PT, Patonga. NA, data unavailable (see text). For (a) and (c), mean percentages dispersed after 2 days (1S.E.) are shown. Initial density was 10 per plot except for U, where initial density was variable. n 5 3 plots, except where indicated by numbers above S.E. bars. For (b) and (d), mean displaced distances after 2 days (1S.E.) for each of two plots per treatment are shown. Initial density was 10 per plot except for U, where initial density was variable. n 5 7 snails.

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rocky shore habitat (Fig. 9d; Table 6b(ii), S 3 T**; TP1 5 TP2 5 TL 5 TL2 5 TL3 at PH, SNK test, p , 0.05) rather than the 15 cm displaced by snails translocated within mangrove forests (Fig. 7d; Fig. 8d; Table 5b(ii), T**; TP . TL 5 TL2 5 TL3, SNK test, p , 0.05). Snails from mangrove forests put on isolated plots in rocky habitat at Broken Bay dispersed in greater numbers and over greater distances than snails translocated from other rocky areas in Port Hacking or within Broken Bay (Fig. 10a,b; Table 5a(ii), I 3 T*; TP . TL 5 TL2 5 TL3 for isolated plots, SNK test, p , 0.05). Dispersal of snails transplanted from Broken Bay to isolated plots in mangrove forests was, however, not significantly reduced in comparison to dispersal of snails translocated to isolated plots within the rocky shore habitat (Fig. 10c,d; Table 6a(iii), S 3 T*; TP1 5 TP2 5 TL 5 TL2 5 TL3 at BB, SNK test, p . 0.05; Table 6b(iii), S 3 I 3 T*; but TP1 5 TP2 5 TL 5 TL2 5 TL3 for isolated plots at BB, SNK test, p . 0.05). The pattern of behaviour of snails dispersing from isolated plots at Patonga was

Fig. 10. (a) Percentage dispersal, and (b) displaced distances of Bembicium in rocky habitat at Broken Bay, February 1995. Snails originated from the sites indicated and were moved to or within Broken Bay. Transplanted snails were of mixed origin; from mangroves at Woolooware and Patonga (see text). (c) Percentage dispersal, and (d) displaced distances of snails originating from Broken Bay, January 1994. Snails from Broken Bay were moved to the sites indicated. Dark hatching, TP; grey hatching, TL; cross hatching, TL2; light hatching, TL3; clear, U. PH, Port Hacking; BB, Broken Bay; WW, Woolooware; PT, Patonga. For (a) and (c), mean percentages dispersed after 2 days (1S.E.) are shown. Initial density was 10 per plot except for U, where initial density was variable. n 5 3 plots, except where indicated by numbers above S.E. bars. For (b) and (d), mean displaced distances after 2 days (1S.E.) for each of two plots per treatment are shown. Initial density was 10 per plot except for U, where initial density was variable. n 5 7 snails.

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consistent with that described above. Snails moved to the mangrove habitat at Patonga from rocky shores (Fig. 8a,b) retained rates of dispersal as large as those observed on rocky shores (Fig. 9a,b, Fig. 10a,b) and greater than those from plots assigned to other treatments at Patonga, (Fig. 8a,b; Table 5a(ii), I 3 T*; TP . TL 5 TL2 5 TL3 for isolated plots, SNK test, p , 0.05; Table 5b(ii), T**; TP . TL 5 TL2 5 TL3, SNK test, p , 0.05). On the other hand, those transplanted from Patonga to rocky shores responded by dispersing in larger numbers and over greater distances than controls translocated between and within mangrove forests (Fig. 8c,d; Table 5a(iii), L 3 T**; TP1 5 TP2 . TL 5 TL2 5 TL3 at PT, SNK test, p , 0.05; Table 6b(iii), S 3 I 3 T*; TP1 5 TP2 . TL 5 TL2 5 TL3 for isolated plots at PT, SNK test, p , 0.01). There was also one case in which the behaviour of snails transplanted from rocky shores to a mangrove forest changed so that it was intermediate between that of animals inhabiting the two habitats. This suggests that an intrinsic tendency to behave in one way was partially, but not completely, over-ridden by responses to extrinsic cues encountered in the new habitat. Snails transplanted to isolated plots at Woolooware in 1995 dispersed in slightly greater percentages and over slightly larger distances than those translocated to isolated plots from Patonga or within Woolooware (Fig. 7a,b; Table 5a(ii), I 3 T**; TP . TL 5 TL2 5 TL3 for isolated plots, SNK test, p , 0.05; Table 5b(ii), T*; TP . TL 5 TL2 5 TL3, SNK test, p , 0.05). They had, however, dispersed in considerably smaller percentages and over considerably smaller distances than was typical of snails translocated within the rocky shore habitat. Dispersal from isolated plots on rocky shores was generally 60–70% and displaced distances averaged ¯ 25 cm, whereas only 50% of those transplanted to Woolooware dispersed and snails were displaced from plots by less than 10 cm on average. In contrast, snails transplanted from Woolooware to isolated plots on rocky shores dispersed in percentages and over distances commensurate with those typical of snails inhabiting rocky shores and much greater than those typical of snails inhabiting mangrove forests (Fig. 7c,d).

3.2.5. Anomalous data Dispersal from continuous plots at Broken Bay in 1995 was ¯ 50% on average (Fig. 10a). This is much smaller than is typical of rocky shores and almost indistinguishable from the percentage dispersal usually recorded for mangrove forests (Crowe, 1996a,b). There were, in fact, no differences in distances dispersed from continuous TL2 and TL3 plots between the rocky shore at Broken Bay and the mangrove forest at Patonga (Fig. 8d, Fig. 10d; Table 6b(iii), S 3 I 3 T*; BB 5 PT for TL2 and TL3: SNK test, p . 0.05). Thus, the pattern that the models aim to explain, the difference in dispersal of snails resident on rocky shores and those resident in mangrove forests (see Section 1), did not exist in this case. Any comparisons involving transplantations to continuous plots at Broken Bay did not therefore provide a valid test of the hypotheses and were not interpreted in this context. 3.2.6. Effect of structure of surrounding microhabitat The only results that would bear on the hypotheses relating to structure of surrounding microhabitat are significant interactions involving the terms site (or habitat) and isolation or site, isolation and treatment. Specifically, hypothesis B.1 (arising from model 1:

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intrinsic factors) predicts a significant two way interaction (H 3 I or L 3 I) in analyses by destination and a significant three-way interaction (L 3 I 3 T) in analyses by origin. Conversely, hypothesis B.2 (from model 2: extrinsic factors) predicts a significant three-way interaction (L 3 I 3 T) in analyses by origin and significant two-way interactions (H 3 I or L 3 I) in analyses by destination. In most analyses, these interactions were not significant and such results are not discussed further because they cannot be interpreted with respect to the proposed hypotheses. Significant interactions among relevant terms were found in analyses of dispersal by snails taken to the different sites during experiments in 1994 and 1995 and in the analysis comparing dispersal of snails originating at Broken Bay and Patonga in 1995. Almost without exception, the results were consistent with hypothesis B.2. Snails placed on continuous (C) plots at Port Hacking in 1995 dispersed in consistently greater proportions and over consistently greater distances than did snails placed on isolated (I) plots (Fig. 9a,b; Table 5a(ii), S(H) 3 I*; C . I at PH, SNK test, p , 0.01; Table 5b(ii), S(H) 3 I**; C . I at PH, SNK test, p , 0.05). This is consistent with predictions from model 2 (extrinsic factors). It represents a shift in behaviour of transplanted snails so that their behaviour is indistinguishable from that of snails translocated to and within that site. At Broken Bay in 1995, snails were displaced by consistently greater distances from isolated plots than from continuous plots (Fig. 10b; Table 5b(ii), S(H) 3 I**; C , I at BB, SNK test, p , 0.01). This is also consistent with predictions from model 2 and the difference is particularly pronounced in transplanted snails (Fig. 10b), suggesting that those snails have indeed adjusted their behaviour to cues present at Broken Bay. Moreover, snails transplanted from Broken Bay to mangrove forests did not disperse different distances in response to differences in surrounding microhabitat. This behaviour was typical of snails inhabiting mangrove forests. In contrast, snails translocated within Broken Bay did disperse differently in response to surrounding microhabitat: the predicted response for snails inhabiting rocky shores (Fig. 10d; Table 6b(iii), S 3 I 3 T***; C , I for TL2 and TL3 at BB, SNK tests, p , 0.01). Displaced distances of snails transplanted from Patonga to Broken Bay in 1995 were greater from isolated than from continuous plots (Fig. 8d, Table 6b(iii), S 3 I 3 T***; C , I for TP2 at PT, SNK test, p , 0.05). This behaviour is consistent with that of snails translocated within Broken Bay (see above) and different from that of snails translocated to or within Patonga (Table 6b(iii), S 3 I 3 T***; but C 5 I for TL, TL2 and TL3 at PT, SNK test, p . 0.05). This suggests that the transplanted snails adjusted their behaviour on arrival at Broken Bay and is thus consistent with model 2. Snails transplanted to mangroves in Patonga from rocky shores showed a strong tendency to disperse further from isolated plots than from continuous plots (Fig. 8b). This behaviour is similar to that seen among snails translocated within Broken Bay and as such is consistent with predictions from model 1 (intrinsic differences). The trend is not, however, statistically significant (Table 5b(ii): S(H) 3 I 3 T, ns) and cannot, therefore, be given as much weight as other differences in the final interpretation. Percentage dispersal from continuous plots at Woolooware was greater than that from isolated plots at that site in 1994 and in 1995 (Fig. 6a, Fig. 7a; Table 5a(i), S 3 I*; C . I at WW, SNK test, p , 0.01; Table 5a(ii), S(H) 3 I*; C . I at WW, SNK test, p , 0.01).

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This pattern was also present in the data for displaced distances in 1995 (Fig. 7b; Table 5b(ii), S(H) 3 I**; C . I at WW, SNK test, p , 0.01), but not in 1994 (Fig. 6b; Table 5b(i): S(H) 3 I, ns). This pattern has not been seen in any of the other experiments done in this system (Crowe, 1996a,b). Interactions (I 3 T) in which overall responses to microhabitat structure varied with treatment were occasionally significant (Table 5a(ii) Table 6b(ii)). For example, snails in the TL treatment did respond to differences in microhabitat, but snails in TL2 did not. Because they combined data from sites in different habitats, they were not relevant to the hypotheses and will not be described here.

3.2.7. Comparisons among control treatments Snails translocated from one site within a habitat to another (TL) never behaved significantly differently from snails translocated to plots within a habitat (TL2 and TL3) (Tables 5 and 6). There was only one occasion on which snails translocated within a site, but kept overnight at the laboratory, behaved differently from snails translocated within a site without being kept overnight. That was at Woolooware in 1994 and only in terms of percentage dispersal (Fig. 6c; Table 5a(i), S 3 T**; TP . TL3 . TL2, SNK test, p , 0.01). Displaced distances of snails from these two treatments were not significantly different (Fig. 6d; Table 5b(i), S 3 T*; TP . TL2 5 TL3, SNK test, p , 0.01). Although no formal analyses were done, the behaviour of undisturbed snails generally appeared similar to that of snails in the other treatments (Figs. 5–10). Analyses of other experiments involving this treatment found no evidence that undisturbed snails behaved differently from those in other treatments (Crowe, 1996a,b).

4. Discussion Clearly, the simple model must be rejected that Bembicium in mangrove forests are intrinsically different from those on rocky shores. In some cases there was evidence pointing to potential intrinsic differences, but it was never enough to explain the observed patterns of difference in behaviour. Thus, snails in the two habitats cannot be considered simply to be distinct races or sub-species for the purposes of behavioural studies. There was no evidence to support this model and abundant evidence pointing to its rejection. The model for which alternatives were most often falsified was that Bembicium living in the different habitats are not intrinsically different, but respond to cues that differ in the two habitats. This makes intuitive sense in that mangroves and rocky shores are found in close proximity, often adjacent to one another (i.e. within a few metres) in the same estuaries, so that considerable mixing (gene flow) can potentially occur during both the planktonic larval (Anderson, 1962) and benthic adult phases of the life history (see also Gooch et al., 1972; Doherty et al., 1995). Nevertheless, proximity does not necessarily predict genetic similarity. For example, Johannesson et al. (1995a) found significant genetic variation among populations of Littorina saxatilis separated by only a few metres. Similarly, there is restricted gene flow between co-occurring morphs of the rotifer Brachioni plicatilis (Gomez and Serra,

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1995). Differences in the mating behaviour of different morphs was considered to be the mechanism by which reproductive isolation was maintained in this species (Gomez and Serra, 1995) and also in Littorina saxatilis (Johannesson et al., 1995b). Bossart and Scriber (1995), on the other hand, found no genetic differences among three geographically remote populations of the butterfly Papilio glaucos using allozyme analysis. Nevertheless, there were clear intrinsic differences in feeding behaviour in the different populations, indicating that it is quite possible for behaviour to vary from place to place despite significant gene flow. There were also several outcomes of the current experiment that supported the third model (an interaction between intrinsic and extrinsic factors) in the sense that snails living on rocky shores often appeared to retain their tendency to disperse in relatively large numbers and over relatively large distances. One scenario that could possibly explain all the results is as follows. There may be an intrinsic tendency for all Bembicium to disperse in proportions and over distances commonly observed in populations inhabiting rocky shores. That tendency can, however, be overridden in response to cues in mangrove forests. In 1994, such cues were effective in reducing dispersal of Bembicium arriving in the mangrove forest at Woolooware from the rocky shore at Port Hacking. In 1995, however, this effect was less marked. It was only apparent for continuous plots at Woolooware and Patonga and the trend for displaced distances was not statistically significant. Snails taken from mangrove forests to rocky shores always exhibited increased dispersal. This also suggests that cues affecting dispersal are relatively consistent though space and time on rocky shores, but can be quite variable in mangrove forests. An alternative explanation is that the simple extrinsic model is true (rather than an interaction), but that responses of transplanted snails to cues in mangrove forests can take longer than two days to be elicited. The transplanted animals may need time to acclimate to the new habitat. Hobday (1995) transplanted limpets within and between areas of differing wave exposure. No changes in behaviour were observed at first, but after an acclimation period of five days, transplanted animals behaved similarly to controls moved within the area to which the transplanted animals had been moved. Hobday (1995) failed, however, to assess the effect of the experimental disturbance on the behaviour of the limpets, so the responses of the animals cannot be unambiguously interpreted (see Chapman, 1986; Underwood, 1986, 1988). As a further example, zebra mussels are unable to spawn immediately on being moved from fresh to brackish water, but, after 2 days of acclimation, are able to spawn successfully (Fong et al., 1995). Conversely, immediate responses to new circumstances may not be long-lasting and animals may eventually return to intrinsic patterns of behaviour. Truscott et al. (1995) observed an immediate change in behaviour of pond snails exposed to aluminium and lead, but, as the snails became acclimated, their behaviour became similar to that of controls that had never been exposed to the metals. The results of the current experiment generally support the extrinsic model. Given time to acclimate, transplanted Bembicium may, however, return to behaviour similar to that of controls in the habitat from which they originated. To distinguish between these alternatives, it would be necessary to transplant snails between habitats and leave them for a period of time to acclimate. Dispersal experiments could then be done to compare the behaviour of these snails with that of snails that had been, (a) freshly transplanted, and (b) not transplanted at all.

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There were almost no differences among the various translocation controls. It is, therefore, reasonable to conclude that any changes in behaviour of transplanted snails relative to controls were indeed in response to transplantation to a new habitat rather than an artifact induced by being held overnight and moved to a different site. In addition, it suggests that the omission of the translocation treatment (TL) from the 1994 analysis by origin does not present a problem in the interpretation of those results. No formal analyses comparing ‘undisturbed’ snails to experimentally manipulated snails were done here. It is not, therefore, possible to be entirely certain that results apply directly to natural populations because all the formal comparisons involved experimentally disturbed animals. Evidence from two runs of an experiment to test hypotheses about dispersal, however, suggests that undisturbed snails do not behave differently from experimentally manipulated ones (Crowe, 1996a,b). The incorporation of a large suite of controls has made it possible to conclude with confidence that the results of the experiment are not merely artifacts of the process of transplantation (see also Chapman, 1986; Underwood, 1986, 1988; Crowe and Underwood, 1998). Where such controls are included, this type of experiment is an effective way to distinguish between alternative models to explain behavioural differences between habitats. What is clear is that changes of behaviour can occur and that there must be some features of the habitats that elicit specific dispersive responses. This factor alone is enough to prevent prediction of behaviour of Bembicium in mangrove forests using models developed on rocky shores. An understanding of the features of the habitats that elicit the observed responses could result in the construction of a single model able to predict dispersal in the two habitats using information on a few key variables. Variables that may contribute to differences between the habitats include spatial arrangement of microhabitat, composition of the substratum, abundance of predators and availability of food (Crowe, 1996a). Dispersal at Woolooware has been consistently the smallest of any site (Crowe, 1996a,b). It has also been the site that has had the most marked effect on snails transplanted from rocky shores (see Section 3). This suggests that whichever cues cause reduced dispersal, they are more pronounced at Woolooware than at Patonga. This additional level of variation may provide clues to the identity of influential variables. Repeated experimentation remains relatively rare, despite the strength of arguments in its favour (Connell and Sousa, 1983; Elner and Vadas, 1990; Underwood, 1997). Given the variation in the outcomes of the experiment, it was clearly essential to have run it at a large number of places and to run it more than once to allow a sensible interpretation of the results (see also Underwood and Chapman, 1992; Crowe, 1999). In this case, it was also necessary in order to unravel results with respect to hypotheses about the effect of surrounding microhabitat on dispersal of Bembicium, which were based on an observation which itself varied. This experiment has provided evidence that the behaviour of individuals of this species is quite plastic and can change rapidly and significantly in response to new sets of cues. Other species for which this type of behavioural plasticity has also been documented include nudibranchs, Tritonia diameda (Brown, 1994) and blue crabs, Callinectes sapidus (Micheli, 1995). Roe deer inhabiting forests behave quite differently from members of the same species inhabiting fields or mountains (Kurt et al., 1993). Like the butterflies discussed above (Bossart and Scriber, 1995), allozyme analyses

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failed to detect genetic differences among these sub-populations (Kurt et al., 1993). This indicates that behavioural experiments are the most relevant in such investigations and suggests that, as in the current study, the different behaviours are responses to the different habitats (behavioural plasticity) rather than being evidence of distinct races or sub-species. Behavioural plasticity of this type must always be considered as a possible barrier to generalization and will potentially reduce the confidence with which predictions can be made, even from models based on a detailed knowledge of the behaviour of a species in one habitat. Under these circumstances, research to improve such predictions needs to focus on the environmental cues that elicit responses from the species in question.

Acknowledgements This research was funded by an Australian Postgraduate Research Award and University of Sydney Research Grant to TPC and an ARC Special Investigator’s Award to AJU. A large team was involved in the field work and we are extremely grateful to Gee Chapman, Sean Connell, Eric Dorfman, Nicole Gallahar, Bronwyn Gillanders, Tim Glasby, Will MacBeth, Vanessa Mathews and Guillermo Moreno for their efforts. Eric Pierce and Graham Housefield provided technical support and the Witchards kindly gave permission for the work at Patonga. We would also like to thank Gee Chapman, Michael Douglas, Todd Minchinton and two referees for valuable comments on earlier drafts of the manuscript.

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