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Journal of Animal Ecology 2004 73, 577–584

Absence of costs of foraging excursions in relation to limpet aggregation

Blackwell Publishing, Ltd.

R. A. COLEMAN, A. J. UNDERWOOD* and M. G. CHAPMAN* Marine Biology and Ecology Research Group, School of Biological Sciences, University of Plymouth, Drake Circus, Plymouth PL4 8AA, UK; and *Centre for Research on Ecological Impacts of Coastal Cities, Marine Ecology Laboratories A11, University of Sydney, NSW 2006, Australia

Summary 1. Animal aggregation has been well studied, with many proximate and ultimate models proposed. Many of the proximate models have relied on cost–benefit arguments, but frequently aspects of cost have been inferred in relation to position in group. An expected cost to an animal that rests in aggregations, but departs to forage, is that being in the centre of a group may impede foraging opportunities, in that ‘inner’ animals cannot leave to forage until outer animals have done so. 2. Experiments with a limpet Cellana tramoserica, on a rocky shore in New South Wales, Australia, showed that central limpets remain central more often than would be expected by chance. In respect of costs due to access to foraging, we show that there is no effect of position (central vs. outer) in timing of foraging excursions or of feeding-rate. We also show that an aggregated distribution of C. tramoserica at rest does not translate into an aggregated distribution of foraging animals. 3. We propose that aggregations of C. tramoserica are probably a function of how the group reassembles after foraging and is much dependent on processes happening at a small spatial scale. It is highly probable that assumptions about the effects of limpet aggregation on rocky shore ecology (i.e. in influencing patchiness of algae) may be premature. Key-words: behaviour, Cellana tramoserica, foraging, grazing, trade-offs. Journal of Animal Ecology (2004) 73, 577–584

Introduction Many animals live in groups and the reasons for this have long been the subject of debate (Hamilton 1971; Alexander 1974). There are obvious advantages. Group living may increase reproductive success, of particular importance in free-spawning sessile invertebrates which predominate in marine systems. Reduction of risk of predation through dilution, increased vigilance and associated avoidance have been addressed, especially for highly mobile prey, e.g. fish (e.g. Rangeley & Kramer 1998) and birds (e.g. Kenward 1978). Grouping may also reduce risks of stresses from the physical environment (Feare 1971; Garrity 1984). There are also potential disadvantages: groups may represent ‘better quality’ patches of prey and result in an aggregation response by predators or repeated attacks (Cummings, Schnieder & Wilkinson 1997). Intraspecific competition for resources

© 2004 British Ecological Society

Correspondence: R.A. Coleman, Marine Biology and Ecology Research Group, School of Biological Sciences, University of Plymouth, Drake Circus, Plymouth PL4 8AA, UK; Fax: + 44 (0) 1752 232970; E-mail: [email protected]

such as food and refuge may be greater among grouped individuals. Aggregated distributions of organisms will also have implications for interactions within an assemblage. This could be important when the organisms concerned are important consumers, for example limpets on rocky shores (Hawkins et al. 1992). Thus, there can be strong links between behaviour of individuals and dynamics of assemblages. Limpets, like many other gastropods, are known to form aggregations. These have been observed in Patella spp. in the NE Atlantic (Jones 1948; Hawkins & Hartnoll 1983; Coleman et al. 1999) and in Scutellastra granularis in South Africa (Bosman & Hockey 1988); R.A. Coleman unpublished data). The evidence for causes of aggregation is contradictory. In mid- and upper-shore areas, chitons, limpets and other gastropods tend to aggregate into groups, possibly in response to stresses of desiccation and wave-exposure (e.g. Feare 1971; Chelazzi, Deneubourg & Focardi 1984). Groups may also be associated with topographic features, particularly cracks and crevices, but they can also occur on very smooth rock (Lewis & Bowman 1975; Focardi, Deneubourg & Chelazzi 1985). On moderately exposed shores in the

578 R. A. Coleman, A. J. Underwood & M.G. Chapman

© 2004 British Ecological Society, Journal of Animal Ecology, 73, 577–584

NE Atlantic, limpets aggregate under clumps of fucoid algae (Southward 1964; Hartnoll & Hawkins 1985). For limpets the main benefit of living in a group is likely to be a reduction in stress or risk of mortality. For instance, limpets living in groups may be less prone to desiccation (Gallien 1985) because moisture will be retained on the rock surface between them and air-flow over the limpets will be modified reducing evaporation (Lowell 1984). Limpets in groups are probably less at risk from dislodgement by wave-action or by wave-borne objects (Shanks & Wright 1986). Grouped limpets may also be less susceptible to attack by predators. Preliminary work has shown that oystercatchers (Haematopus ostralegus) are more successful when they attack solitary as opposed to grouped limpets (Coleman et al. 1999). Another probable advantage of group living is the increased probability of fertilization, although this is very difficult to quantify (but see Feare 1971 and Levitan, Sewell & Chia 1992) for work with Nucella lapillus and sea urchins, respectively). Grouping may also have associated ‘costs’. Although some predators (e.g. oystercatchers) prefer solitary prey and attack grouped limpets less frequently, other predators such as crabs or fish, which may be less selective, could find groups of prey easier to locate. Predators foraging randomly will also be more likely to encounter groups of prey than solitary prey (Krause & Ruxton 2002). Costs and benefits may vary for animals in different positions within a group. Animals on the outside possibly have greater access to resources and more time to feed when animals move out of the group (Santini & Chelazzi 1996). In contrast, animals in the middle of groups may have to embark on foraging excursions later after surrounding animals have moved, and must return earlier to regain the central position. Conversely, the risks from environmental stress (desiccation, dislodgement) and predation while at home should be less in the middle of the group. If different positions have different ‘values’ then competition should occur for the best locations in the group. The model that being in the centre of a group incurs a cost via reduced access to foraging areas requires assumptions about the potential costs to be considered. It is not known whether the position of a limpet inside a group is a consequence of random formation of groups after the individuals forage, or because ‘central limpets’ (defined as being surrounded by members of that group) have behavioural or physiological tendencies to be central. If the former model were correct, limpets formerly in the centre of a group will be in any position in new aggregations after they have returned from feeding. In contrast, if the second model were correct, it could be hypothesized that limpets identified as central on one occasion will, after subsequent excursions, be found in central positions more often than by chance. If the second model is supported and being central is more consistent through time than expected by chance, it can be predicted that the central limpets

will have a longer time between the start of the foraging period and departure from a resting site and less time to feed (before the tide falls) than is the case for limpets that occur in outer positions in aggregations when not feeding. If the period of foraging were reduced for limpets occupying central positions, they may also be expected to compensate by feeding faster. This leads to the hypothesis that central limpets will graze faster (number of radular scrapes and/or increased duration of radular scrapes). These and related hypotheses were tested for the limpet Cellana tramoserica (Holten, 1802) on an intertidal rocky shore in New South Wales, Australia, during the austral winter of 2000. Limpets are very important in influencing assemblage dynamics on rocky shores; their grazing is a major determinant of macroalgal abundance and consequent patterns of biodiversity (Hawkins & Hartnoll 1983; Hawkins et al. 1992; Underwood 2000). On rocky shores in New South Wales, Australia, Cellana tramoserica (Mollusca: Nacellidae) is one of the most abundant limpets (Edgar 2000). It feeds during high tides (Underwood 1975; Mackay & Underwood 1977) and is inactive during emersion. Where topography is relatively uniform, C. tramoserica are not aggregated and are often more uniformly dispersed than by chance (Underwood 1976). In contrast, the limpets we examined occurred in areas where there were pits in the rock and formed aggregations around pits (R.A. Coleman personal observation).

Materials and methods This work was conducted at the Cape Banks Scientific Marine Research Area (hereafter referred to as ‘Cape Banks’) at the entrance to Botany Bay, New South Wales, Australia (34°00′ S, 151°15′ E), the general ecology of which has been described extensively elsewhere (e.g. Underwood, Denley & Moran 1983; Chapman & Underwood 1998). All the hypotheses were tested at several times and in several sites on the shore so that generality could be maximized. Sites were defined as representative areas of the shore (40–60 m2) where C. tramoserica could be found in aggregations. Sites were separated by a minimum of 10 m.

  Groups of limpets were selected haphazardly in each of three sites. In each group, the number of limpets was noted and a central limpet clearly marked using nail varnish. ‘Central’ was defined as above, so small aggregations where no central limpet could be discerned were ignored. Each group was allocated randomly to one of three time periods: 1 day, 7 days or 22 days, and there were 12 independent groups for each time period. At the end of each time period the groups were revisited and the identity of the central limpet checked. A loglikelihood test of independence with William’s correction (Sokal & Rohlf 1995) was used to test the null

579 Foraging and aggregation by a limpet

hypothesis that changes in central limpet were independent of the site chosen. If there were no tendency for the central limpet to remain constant, it would be expected that each limpet in a group would have an equal chance (1/n, where n is the number of limpets in the group) of being so. It was assumed that this probability was constant over time. From this, an expected frequency of limpets being found in the centre of a group was derived and tested against the observed number using χ2 tests.

      On each of three occasions, limpets in three sites on the shore (different sites on each occasion) were observed. During low tide, 24 groups of limpets were selected haphazardly and, from these, 12 central limpets and 12 outer limpets were selected randomly. ‘Outer’ limpets are defined as not being completely surrounded by other members of their group (Coleman & Hawkins 2000). These limpets were marked individually using coloured plastic microlabels and the location of the group indicated by marking the rock adjacent to the group with a small dot of brightly coloured nail varnish. This allowed us to see when an individual limpet left on a foraging excursion. The number of limpets sampled in each site had been previously determined as the maximal number of observations that could be made by one person during a 20-min period of observation. The sole selection criterion for the groups was that they should have clearly identifiable central and outer limpets and were at approximately the same tidal height. Limpets were described as ‘at home’ or ‘away’ from sites of aggregation every 20 min from submersion of the first group until the last group was emersed. Data were analysed by  run on WinGMAV5 (EICC, University of Sydney).

        


Grazing was assessed in situ by recording radular rasps using a hydrophone on the end of a 1·5-m pole and a portable tape-recorder (Petraitis 1992). Foraging behaviour in many species of limpets is triphasic; a mobile outward phase, a stopped or sedentary phase and a rapid return phase (Hartnoll & Wright 1977). This was borne out by observations of foraging C. tramoserica (R.A. Coleman personal observation). The hypothesis under test referred to feeding after submersion, so only the grazing of animals moving out from an aggregation was measured. On each of two dates, two sites were visited and the foraging activity of limpets recorded. During low tide, 12 groups of limpets were haphazardly selected and either an outer or a central limpet selected in each group, each being clearly and uniquely marked. Once covered by the tide and when they had moved at least 5 cm from their resting site, radular rasps were

recorded for 1 min from each of six limpets, each individual was recorded only once. Recordings were later transcribed into ‘The Observer’ behavioural software (Noldus Technologies, Wageningen, the Netherlands), with each rasp being recorded as an event (0·1 s), so that frequency of rasps and total duration of feeding could be quantified. Null hypotheses were tested by  as above.

         We tested the hypothesis that levels of aggregation differ between emersed and submerged limpets using a dispersion index. At each of three sites on two different days, aggregation was recorded at high tide (± 1 h) and at low tide (± 1 h). This was performed twice for each tide to allow for variations in foraging activity between limpets. The sequence of day, tide and site was randomized over a 6-week period. On each sampling occasion, 10 0·5 × 0·5-m quadrats were set randomly. In each quadrat, three replicate independent measures of aggregation (Pielou’s Iα; Pielou 1969) were calculated. Null hypotheses were tested by .

Results Densities of limpets ranged from 145 to 209 individuals m−2. Across all sites, groups had three to 15 limpets although five – eight were more common. The aggregations were usually associated with topographic features such as pits, which were usually large enough to hold five to eight limpets. These pits often retained surface water for longer than did the surrounding rock.

  For the 1- and 7-day periods, membership of every group could be determined. One of the 22-day groups had totally dispersed; this was counted as a change in central limpet. There was no difference among sites in the proportion in which the central limpet changed (Fig. 1a) (William’s adjusted G-test = 1·15, 4 d.f., P > 0·05). The number of limpets retaining their central position did decline over time (Fig. 1b) but was, at every time, significantly greater than would be expected under random assortment ( χ2 = 64·1, 2 d.f., P < 0·001). Some limpets appeared to move between aggregations and in other cases aggregations themselves were displaced slightly from their previous location, but still had the same central limpet. Timing of foraging In the analysis of these data, as with 2·2 and 2·3 below, the highest-order interaction [position × site (date)] was not significant and the mean square was much smaller than the residual, so this interaction was pooled with the residual (Underwood 1997). There were no differences


Duration of foraging activity There was no significant difference between central and outer limpets in the mean duration of foraging activity (Fig. 2a, Table 1). Again, there was significant variation among sites for each date (Table 1; Fig. 2b). Timing of return from foraging There was no difference between central and outer limpets in timing of return to an aggregation after foraging (Fig. 2a, Table 1). As before, there was significant variation in return-times among sites (Fig. 2b, Table 1).

 

Fig. 1. Consistency in being central. (a) The frequency of groups of limpets (out of 12) in which the central limpet changed over the three different time periods for all three sites. A different set of limpets was observed for each period. (b) The frequency of limpets retaining a central position in their group over three different time periods (pooled across sites), compared with the expected distribution based on random re-assembly of the group after foraging.

in times of departure between outer and central limpets (Table 1, Fig. 2a). The timing of departure from a resting site varied significantly from site to site for each day (Table 1, Fig. 2b).

Where recordings were decipherable, it was evident that limpets leaving aggregations were grazing. On the first day, one recording at site 1 and two recordings from site 2 were uninterpretable due to the noise of swash masking that of radulae. Replicates were removed at random to obtain a balanced data set of four replicates. For the analysis of frequency of rasps (radular scrapes min−1) the factor position × site (date) was pooled with the residual term as above. There was a significant interaction of position and date with respect to number of scrapes min−1 (Table 2) in that on day 1 the mean number of scrapes min−1 was greater for central than for outer limpets and vice versa for day 2 (Fig. 3). SNK tests could not detect significant differences on either day. There was no significant difference between central and outer C. tramoserica in the length of time spent scraping in any 1 min (Table 2; Fig. 3).

  -  -     Limpets were more aggregated at low tide (mean Iα = 1·05, n = 180, SE = 0·025) than high tide (mean Iα = 0·81, n = 180, SE = 0·028) (Table 3).

Table 1. Analyses of variance of timing aspects of foraging excursions of limpets in different position in a group (central and outer) for 12 replicate groups, at three sites on three different dates. Departure was defined as the period (in minutes) between submersion and leaving an aggregation; data were ln (x + 1) transformed. Foraging is the proportion of the time submerged spent feeding; data were arcsine transformed. Return was defined as the period between arrival an aggregation and emersion; data were ln(x + 1) transformed. Variances were homogeneous after transformation (departure: Cochran’s C = 0·12, NS; foraging excursions C = 0·12, NS; return to resting site C = 0·14, NS). In all cases, position × site (date) was not significant, so this factor was pooled with the residual (Underwood 1997), where factors have been tested against this pooled factor they are indicated by ¶. Significance is denoted by asterisks (***P < 0·001, **P < 0·01, *P < 0·05) Departure


Foraging

Return

Source

d.f.

MS

F

MS

F

MS

F

Position (i.e. central vs. outer) Date Position × date¶ Site (date)¶ Position × site (date)¶ Residual Pooled residual with P × S (D)

1 2 2 6 6 198 204

1·3 29·8 2·6 22·7 0·2 1·5 1·5

0·50 1·31 1·75 15·45*** 0·11

742·3 12 388·9 723·9 1626·9 554·6 373·6 378·9

1·03 7·62* 1·91 4·29** 1·46

0·1 46·0 5·9 15·1 1·2 2·2 2·2

0·01 3·05 2·66 6·82*** 0·56


Fig. 2. (a) The foraging patterns of C. tramoserica in relation to immersion and position in a group. (a) Central (C) and outer (O) C. tramoserica for all sites and dates; (b) activity of all limpets irrespective of position in a group for sites 1–3, representing randomly chosen patches of shore at different dates (see Table 1 for ). The open bars represent mean departure periods defined as the time from being immersed at time = 0 and departure from the resting site; these should be read against the left ordinate scale. The shaded bars represent period spent foraging (defined as time away from the resting site) as a mean of the proportion of the time available between submersion and emersion; these should be read against the right ordinate scale. The solid bars represent mean return periods (defined as the time from a limpet returning to its resting site and then being emersed), and these should be read against the left ordinate scale.

Table 2. Analyses of grazing activity measured by recordings of radular scrapes of four central limpets and four outer limpets each in different groups, at two sites on two different dates. Rate was measured as the number of radular scrapes/minute and time spent feeding was defined as the total time the radula spent in contact with the substratum as the sum of the duration of all scrapes. Variances were homogeneous (grazing rates Cochran’s C = 0·24, NS; Time spent feeding C = 0·22, NS). Significance is indicated by asterisks (*P < 0·05) Grazing rates


Time spent feeding

Source

d.f.

MS

F

MS

F

Position Date Position × date Site (date) Position × site (date) Residual Pooled residual with P × S (D)

1 1 1 2 2 24 26

13·8 22·8 247·5¶ 4·3¶ 22·7 47·9 46·0

0·06 5·32 5·39* 0·09 0·47

0·5 0·0 1·8 5·4 5·2 3·9

0·28 0·00 0·35 1·39 1·34


Fig. 3. Grazing activity of limpets from central or outer positions over two different observation days. The left-hand four bars show the grazing rate mean number of grazes min−1 (± SE) (measured as the number of radular scrapes min−1) and the right-hand four bars show the mean period spent feeding (± SE), which was the total time the radula spent in contact with the substratum as the sum of the duration of all scrapes.

Table 3. Analysis of variance of three replicate measures of aggregation of limpets by Pielou’s (1969) Iα during tide-in or tide-out at three sites on each of two occasions from 10 quadrats. There was no test for sequence. Variances were homogeneous after ln(x + 1) transformation (Cochran’s C = 0·06, NS). ¶ These factors were eliminated from the analysis because they were non-significant at P > 0·25 (Underwood 1997) Source

SS

Sequence Se Site Si Tide Ti Quadrat Qu (Se × Si × Ti) Se × Si Se × Ti Si × Ti¶ Se × Si × Ti¶ Residual

–

d.f. MS F

1 – 0·3 2 0·2 1·3 1 1·3 15·8 108 0·1 0·3 2 0·1 0·0 1 0·0 0·1 2 0·0 0·0 2 0·0 27·8 240 0·1

– 1·17 8·87 1·26 0·90 0·28 0·33 0·10

P – > 0·3 < 0·005 > 0·07 > 0·41 > 0·5 > 0·7 > 0·9

Discussion


This work used mensurative experiments (Hurlbert 1984) to test hypotheses about potential costs in relation to position in an aggregation. These costs were suggested to affect foraging, in that central animals were expected to leave resting aggregations later than the outer group members and return to resting sites earlier (Coleman & Hawkins 2000), thus reducing time available for foraging. It was proposed that because the central limpets may have reduced foraging times, they would compensate by increasing feeding rates either by grazing faster or increasing the time that the radula spent in contact with the substratum.

The hypothesis of central limpets retaining their central position in aggregations was supported and consistent across sites. It is not clear whether the tendency to be central is a property of the individual limpet, a competitive effect or simply a consequence of group reassembly after foraging. This latter possibility seems likely, because it appeared from informal observations as if C. tramoserica may have been using contact with conspecifics in the proximity of its resting site as a cue to stop. Repeat observations of reassembly of a group over long periods of time would clarify this, coupled with manipulative experiments involving selective removal of limpets in different positions within the group. Many models of grouping by animals are based on the assumption of costs and benefits (Hamilton 1971; Beecham & Farnsworth 1999). The costs are given as increased apparency to predators (Hamilton 1971) and reduced access to feeding (Beecham & Farnsworth 1999; Coleman & Hawkins 2000) by outer limpets blocking inner ones. Our results show that this simplistic assumption of reduced feeding access is not true for Cellana tramoserica at Cape Banks. The assumption of blocked foraging opportunities is based on the principle that organisms will attempt to maximize energy intake during foraging excursions and that, somehow, being in a group will physically restrict access to feed. This latter assumption is dependent on outer limpets departing aggregations before central ones. We observed that all limpets appeared to leave their resting sites almost simultaneously and that the only variations in timing aspects of foraging excursions were among sites and dates. This is consistent with limpets not conforming to an energy-maximization premise (Santini & Chelazzi 1996) and variation in foraging behaviour being related


to individual variation and physical aspects of the shore (Gray & Naylor 1996). It would appear that our observed patterns of activity are best explained by smallscale differences in topography (Chelazzi, Parpagnoli & Santini 1998) and differences in satiation related to gut-processing (Santini & Chelazzi 1996; Chelazzi et al. 1998). Manipulative experiments of food supply in relation to foraging activity are needed here. The results of our observations of use of radulae by grazing limpets are consistent with the results from foraging activity in showing no effect of position in an aggregation on feeding-rates. Little discernible difference in rock type was noted between the different sites, but given that the rock was not uniformly flat there may have been differences in hardness between areas. This would go some way to explaining differences in radular action (Hawkins et al. 1989). Experiments comparing rock type, manipulating abundance of food and noting feeding activity would clarify these uncertainties. Such data would usefully address the questions raised by modelling studies (Santini & Chelazzi 1996; Chelazzi et al. 1998) as to whether grazing by limpets can be explained by statedependent models. The role of limpets in modifying rocky-shore assemblages is understood from many studies (see Hawkins et al. 1992; Underwood 2000 for reviews). The links between aggregated distributions of limpets and the effects of grazing is, however, less well known. Our results showed that even though C. tramoserica was aggregated when emersed, grazing animals during high tide showed an almost random distribution. Although such patterns have been shown for Littorina unifasciata (Chapman 1995) this has not been demonstrated in other species of limpets; so on a site scale, aggregation of limpets at-home may not always be relevant for predicting patterns of algal escapes, and that the predictions of some modelling studies for algal escapes from grazing by Patella vulgata (Johnson et al. 1997) may not be universal. It has been suggested that there is a trophic chain of algae, limpets and avian predators (Wootton 1992), which means that predators could modify indirectly the spatial distribution of algae. This argument was used by Coleman et al. (1999) to propose that the differential predatory success of oystercatchers on aggregated and solitary limpets may have assemblagelevel consequences. Our results indicate this inference may be premature. Data from wax disks used to record of patterns of grazing (Thompson, Johnson & Hawkins 1997; Forrest, Chapman & Underwood 2001) in relation to limpets’ spatial dispersion would be needed to confirm our observations.

Acknowledgements © 2004 British Ecological Society, Journal of Animal Ecology, 73, 577–584

This work was funded by an International Exchange Study Visit Grant from The Royal Society to R.A.C. and an EICC Visiting Fellowship to R.A.C. A.J.U. and M.G.C. gratefully acknowledge the support of the Australian Research Council. We thank Emma Sheehan,

David Blockley and Sónia Monteiro, for assistance in the field. Most of all, the authors would like to thank Lisandro Benedetti-Cecchi for his perceptive comments on the design and analysis of experiments. This paper was greatly improved by comments from Dave Raffaelli, George Branch and an anonymous referee.

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