The effect of social interactions on tadpole activity and growth in the British anuran amphibians (Bufo bufo, B. calamita, and Rana temporaria)

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1 J. Zool., Lond. (1998) 245, 431±437 # 1998 The Zoological Society of London Printed in the United Kingdom The effect of social interactions on tadpole activity and growth in the British anuran amphibians (Bufo bufo,, and Rana temporaria) R. A. Grif ths 1 and J. P. Foster 1, * 1 The Durrell Institute of Conservation and Ecology, University of Kent, Canterbury, Kent CT2 7NJ, U.K. (Accepted 28 November 1997) Abstract Tadpoles of different species of frogs and toads display different tendencies to aggregate. We investigated some of the costs and bene ts of aggregating in three British species by examining their behavioural responses to the presence of conspeci cs, and by monitoring the performance of tadpoles under different levels of social interaction with other individuals. The common toad (Bufo bufo), an aggregating species, displayed higher levels of activity than the natterjack toad () and common frog (Rana temporaria), two species that form aggregations less frequently. Moreover, out of the three species, only B. bufo increased activity in the presence of conspeci cs. In all three species, increased interaction between individuals resulted in increased variation in size. However, average growth rate was affected only in B. bufo, which grew faster when raised in isolation and not interacting with other individuals. Under certain conditions intraspeci c competition therefore seems to be more important than social facilitation, but may lead to average size at metamorphosis being larger within the population. The consequences of intraspeci c competition within aggregations may therefore be different for individuals and populations. Key words: tadpoles, aggregation, competition, activity, growth INTRODUCTION In animals that display social behaviour there are both costs and bene ts to living in a group. Advantages of group-living include reduced predation risk by the effects of dilution, confusion, or increased vigilance (e.g. Hamilton, 1971; Pulliam, 1973; Foster & Treherne, 1981), but these may be offset by increased competition for food within the group (e.g. Lima & Dill, 1990; Magurran & Bendelow, 1990; Richardson, 1994). On the other hand, foraging may be enhanced within the group by socially facilitated behaviour that increases the detection, availability, or acquisition of food (e.g. Bertram, 1978; Clayton, 1978; Pulliam & Caraco, 1984). Within a group the cost of reduced predation risk and social facilitation may therefore be increased competition for food resources. Tadpoles are convenient models for studying the costs and bene ts of living in groups. Different species within the same assemblage may differ in their tendency to form aggregations (Wassersug, 1973; Grif ths & Denton, 1992; Blaustein & Walls, 1995), and such behaviour may be related to the risks associated with predation and competition. In tadpole aggregations, * Present address: Froglife, Triton House, Bram eld, Halesworth, Suffolk IP19 9AE, U.K. feeding may be facilitated by the collective stirring of detritus and micro-organisms, and this may bene t the group (Beiswenger, 1975). However, this bene t may be offset by competition between individuals for the suspended food particles. Such competition may combine both exploitative and interference mechanisms. In the latter case, large individuals may inhibit the feeding of smaller individuals by direct interactions (Savage, 1961; Wilbur, 1977), or alternatively, slow their growth indirectly by releasing inhibitory protothecan algae into the water (Beebee, 1995; Grif ths, 1995; Petranka, 1995). Although it is well known that one of the outcomes of competition between tadpoles is a reduction in mean size at metamorphosis and increased variation in growth between individuals (e.g. Wilbur & Collins, 1973; Wilbur, 1977), the mechanisms that control these responses are poorly understood. In this study, we compare the effects of behavioural interactions in the three anuran species native to Britain. These species display different tendencies to aggregate, and have different susceptibilities to predation. Common toad (Bufo bufo) tadpoles form large, dense aggregations, and may be aposematically coloured and unpalatable to many predators; natterjack toad (Bufo calamita) tadpoles form large aggregations less frequently, but are also aposematic and unpalatable; common frog (Rana temporaria) tadpoles do not

2 432 R. A. Griffiths and J. P. Foster regularly form social aggregations, and are cryptically coloured and palatable to a wide range of predators (Heusser, 1971; Cooke, 1974; Reading, 1990; Denton & Beebee, 1991). The aim of the experiments was two-fold. Firstly, we compared the activity responses of the three species in the presence and absence of a conspeci c aggregation. Secondly, we compared the performance of the three species under constant density and food supply, while manipulating the degree of intraspeci c interaction between individuals, using a similar methodology to that used by Breden & Kelly (1982). These authors found that in B. americanus (an aggregating species), increased interaction between tadpoles increased size at metamorphosis. We therefore predict that, as the degree of aggregation increases between species, the bene ts of living in a group will outweigh the costs associated with competition, and that this will be manifested as increased growth at higher levels of social interaction. MATERIALS AND METHODS Raising tadpoles Rana temporaria, Bufo calamita, and B. bufo tadpoles were collected as either spawn or hatchlings from ponds in the south of England and raised in outdoor stock tanks on a diet of rabbit pellets. The experimental groups therefore probably consisted of a mixture of kin and non-kin. All tadpoles used in the experiments were free-swimming and independently feeding, with hindlimb buds developing (Gosner, 1960: stages 26±34). When tested with conspeci cs, individuals did not differ from each other in development by more than two Gosner (1960) stages. At the end of the experiments tadpoles and metamorphs were used to restock appropriate habitats as part of wider conservation programmes. Activity responses to aggregations The responses of tadpoles to conspeci c aggregations were studied using the apparatus described by Grif ths & Denton (1992). This consisted of a plastic box ( cm deep) divided into 3 sections by 2 nylon mesh partitions. The partitions were 5 cm from each end of the box, leaving a central section of cm. The box was lled with 0.6 l of aged tap water, which gave a depth of 3 cm. The activity of individual tadpoles was monitored either alone or in the presence of 20 conspeci cs of similar size and developmental stage. In the `no aggregation' treatment, a single tadpole was introduced into the central section of the compartment and allowed to acclimate for 10±12 min. The number of seconds spent actively swimming (i.e. tail exing clearly visible) was then recorded for 5 min using a stopwatch. The same procedure was used in the `aggregation' treatment, except that a stimulus group of 20 conspeci cs was added to one of the end compartments of the test chamber at the same time that the test tadpole was introduced. The density of tadpoles used was within the range of densities observed within natural aggregations of frog or toad tadpoles. Forty individuals of each species were tested under each experimental treatment. Stimulus tadpoles were drawn randomly from a group of about 100 individuals and replaced every 2 or 3 trials. The end compartment containing the stimulus tadpoles was alternated between trials and the experimental chambers were thoroughly rinsed in tap water after each test. Experiments were carried out between 10:00 and 17:00, with treatments randomly allocated over this time period, and performed on a uniformly illuminated laboratory bench at C. Two-way ANOVA was used to test for differences in activity between the three species and between `aggregation' and `no aggregation' treatments, together with interactions between these factors. Pairwise comparisons were performed using the Student±Newman±Keuls test. Behavioural interactions The effects of different levels of intraspeci c interaction were monitored by raising tadpoles in plastic boxes ( cm) containing 0.5 l of aged tap water. The degree of social interaction was manipulated while maintaining a xed density of one tadpole per 125 ml water. Under `fully interacting' conditions, four tadpoles were allowed to interact freely. Under `partially interacting' conditions, the four tadpoles were separated from each other by an aluminium mesh partition which prevented physical contact between tadpoles but permitted free exchange of water and suspended particles between compartments. The third treatment consisted of a `no interaction' control, where a single tadpole was enclosed in one quarter of the chamber (so that tadpole density was identical to that in the other two treatments). This area was sectioned off using an acetate barrier attached rmly to the sides, so that faeces and food could not drift into unused parts of the chamber (Fig. 1). The `full interaction' and `no interaction' treatments both had a piece of aluminium attached to the side of the chamber to ensure that water quality was the same in all treatments. Each treatment was replicated 10 times, and each replicate chamber was allocated a random position on some laboratory shelves. The experiment was carried out in a laboratory subject to natural photoperiods via a window, and at a temperature of C. Tadpoles were provided with a per capita food ration, adjusted according to tadpole size and density within each treatment. The food consisted of nely ground rabbit pellets, and the ration was calculated as 0.16mean tadpole mass per tadpole per day, using a similar regime to that determined by Werner (1992). Separate rations were calculated for each treatment and

3 Behaviour and growth in tadpoles 433 (a) (b) (c) Fig. 1. Design of experimental chambers to test the effect of interaction level on tadpole performance. (a) Full interaction; (b), partial interaction; (c) no interaction. Broken lines, aluminium partitions; solid line, acetate barrier. for each species. As it was dif cult to weigh the experimental tadpoles, mass was estimated from weekly length measurements using regression equations derived from separate samples of tadpoles ( and B. bufo: ln(mass) = ln(length); : ln(mass) = ln(length). In chambers with partitions, equal amounts of food were placed in each of the 4 compartments, although food particles could wash between different compartments as a result of tadpole activity. Food and water were renewed twice weekly. Tadpole growth rate was used as a response variable for the degree of social interaction. Total length was measured to 0.5 mm precision at weekly intervals, by anaesthetizing tadpoles in benzocaine (Laird & Oswald, 1975), and measuring them on waxed graph paper. To insure independence between observations, all statistical analyses were performed on experimental chamber means. One-way ANOVA was then used to compare the mean growth rates of tadpoles between treatments. In addition, the variance in size was calculated for each chamber in the full and partial interaction treatments. Variances were cube-root transformed to ensure normality, and one-way ANOVA was then performed on the transformed data to compare the variation in size between these two treatments. Analyses were performed after 2 week's growth in B. bufo and, and after 1 week's growth in, as the latter species has a much shorter development period than the other two (metamorphosis commenced 12 days after the start of the experiment). Four experiments were carried out between March and June The rst 3 experiments investigated interactions with conspeci cs in, and B. bufo. The fourth experiment tested interspeci c interactions between and B. calamita. In this experiment, full and partial interaction treatments had two tadpoles of each species in each experimental chamber. In the partial interaction chambers, conspeci cs were placed in diametrically opposite compartments. tadpoles in one chamber suffered some mortality, which resulted in an unbalanced design. A General Linear Model three-way ANOVA was therefore performed to compare the effects of species, interaction level, and presence of conspeci cs or heterospeci cs on growth rate and variance in size. At the end of each experiment, samples of faeces were pipetted from each experimental chamber and examined under a microscope for the presence of cells of Prototheca richardsi. This cell may cause growth inhibition in tadpoles by diverting small tadpoles from high-quality food to Prototheca-laden faeces (Beebee & Wong, 1992). RESULTS Activity responses to aggregations Activity levels varied between species, with B. bufo spending about twice as much time swimming as the other two species (Fig. 2; species: F 2,234 = 52.6, P < 0.001; aggregation: F 1,234 = 7.1, P < 0.01). The aggregation6species statistical interaction term was also signi cant (F 2,234 = 4.0, P < 0.05), indicating that the three species did not respond in the same way to the presence of conspeci cs (Fig. 2). Whereas B. bufo increased swimming activity when a group of conspeci cs was present, neither nor showed any difference in activity between `aggregation' and `no aggregation' treatments (Student±Newman± Keuls tests, P > 0.05). Intraspeci c interactions Out of the three species tested, only the growth rates of B. bufo tadpoles differed signi cantly between treatments (F 2,26 = 8.96, P = 0.001; Fig. 3a). Pairwise comparisons revealed that control B. bufo tadpoles raised in isolation grew faster than fully and partially interacting tadpoles, but there was no difference in growth between the two social interaction treatments

4 434 R. A. Griffiths and J. P. Foster Activity (s) aggregation no aggregation Growth rate (mm/day) (a) 0 B. bufo Fig. 2. Effect of a conspeci c aggregation on activity in tadpoles. Bars, mean time spent actively swimming during 300 s of observation, + sd (n = 40) (b) Growth rate (mm/day) (a) Variation in growth none none none B. bufo Fig. 4. (a) The effects of interspeci c interactions on tadpole growth rate; (b) variation in size (cube root of variance) in R. temporaria and. +Rt, tadpoles raised with R. temporaria; +Bc, tadpoles raised with. Bars, mean values + sd (n = 10). 2.0 (b) Variation in growth were all higher under fully interacting conditions than under partial interaction (B. bufo: F 1,17 = 7.84, P<0.05; : F 1,18 = 16.55, P<0.001; : F 1,17 = 13.08, P<0.01; Fig. 3b). Examination of faecal smears revealed the presence of Prototheca richardsi cells in all experimental chambers. Interspeci c interactions 0.0 partial full partial (Student±Newman±Keuls tests, P>0.05). However, all three species displayed signi cant differences between the two social interaction treatments with regard to variation in tadpole size. Within-chamber variances full B. bufo Fig. 3. (a) The effects of interaction level on tadpole growth rate; (b) variation in growth (cube root of variance). Bars, mean values + sd (n = 10). As expected, the larger tadpoles grew faster than those of, but growth varied according to whether tadpoles were raised with conspeci cs or heterospeci cs (Fig. 4a). grew faster with than with conspeci cs, but this effect was not reciprocated in, which showed little difference in growth between conspeci c and heterospeci c treatments. This effect was con rmed by a signi cant species6con-/heterospeci c statistical interaction in the ANOVA (Table 1). There was a trend for the growth rates of both species to be greater under

5 Behaviour and growth in tadpoles 435 Table 1. Summary of three-way ANOVAs testing for the effects of species, social interaction (full or partial), and presence of conspeci cs or heterospeci cs, together with statistical interactions between these factors. Variables are growth rate (mm/day) and cube-root of the variance in size. ***P < 0.001, **P<0.01, *P<0.05 Growth rate Size variation Factor d.f. F F Species *** 12.6*** Conspeci cs/heterospeci cs 1 9.8** < 0.1 Social interaction *** Species6conspeci cs/heterospeci cs 1 6.2* < 0.1 Species6social interaction Conspeci cs/heterospeci cs6social interaction Species6conspeci cs/heterospeci cs6social interaction 1 < Error 71 Total 78 fully interacting conditions although this was not signi cant. Variances in growth differed between the two species, and as in the intraspeci c experiment, were higher under fully-interacting conditions (Fig. 4b, Table 1). Examination of faecal smears revealed the presence of Prototheca richardsi cells in all experimental chambers. DISCUSSION In fully interacting treatments, tadpoles were allowed to display the full range of competitive interactions, encompassing both differential exploitation of the food resources between individuals, direct interference between individuals, and indirect interference via the release of growth-inhibiting Prototheca in the faeces. In partially interacting treatments, direct interference between individuals was removed, and the main competition mechanisms were therefore exploitation competition and indirect interference via the release of growth inhibitors. As the experiments controlled for density, and food was supplied on a per capita basis, the results suggest that an increase in variation in growth with increasing direct interference between individuals is a general trend within this guild of species. This raises the question of what type of physical interactions may occur between tadpoles. In experiments performed on salamander larvae (Ambystoma opacum), Smith (1990) observed that physical interactions between larvae resulted in reduced growth independently of exploitative competition, and that larger competitors resulted in more severe growth inhibition than smaller competitors. Such growth inhibition was a result of attempted cannibalism of small larvae by large larvae. Cannibalism occurs much less frequently in anuran tadpoles, although `butting' behaviour has been observed between tadpoles of the American toad, Bufo americanus (Beiswenger, 1975; Waldman, 1982). Vigorous swimming movements by large tadpoles have been observed to prevent access to food by smaller tadpoles in both ranid and bufonid tadpoles (Savage, 1961; Wilbur, 1977). These behaviour patterns may result in smaller tadpoles feeding less ef ciently than larger tadpoles, thereby accentuating any size variation within the group. Although physical interactions result in increased variation in growth, and perhaps tness, this pattern may not necessarily be detrimental to the smaller tadpoles in the longer term. Breden & Kelly (1982) showed that increased interaction in Bufo americanus tadpoles resulted in increased variation in development time, but increased mass at metamorphosis. Variation in growth and development therefore results in asynchronous timing of metamorphosis, but as the fastest growing individuals metamorphose, the remaining smaller individuals are released from competition (Grif ths, Edgar & Wong, 1991). With less competition for resources, the smaller individuals grow faster and eventually metamorphose at the same size as, or even larger than, their earlier-metamorphosing counterparts. Interference competition may therefore result in a staggering of tadpole development, which in turn allows individuals to partition the resources within a pond on a temporal scale. In at least one of the species studied here (B. calamita), such asynchrony in development does indeed result in a larger mean size at metamorphosis for the population as a whole (Foster, 1994). There are, however, costs associated with delaying metamorphosis in this way. A longer larval period results in increased risk of predation by aquatic invertebrates (e.g. Wilbur, Morin & Harris, 1983), and as breeds in highly ephemeral ponds, there is a high risk of slowgrowing tadpoles dying as a result of pond desiccation prior to metamorphosis. In addition, ephemeral ponds may deteriorate in quality over time as nutrients are bound up in plant growth or are exported from the system by metamorphosing individuals (e.g. Seale, 1980). Thus late developing tadpoles may be more resource-limited than early developers. Increased variation in growth and development may therefore only bene t small tadpoles in wet years when ponds retain water for long enough to allow metamorphosis of both fast and slow developers, and when the threats posed by predation and resource-limitation are relatively low. Otherwise bene ts can only accrue through group

6 436 R. A. Griffiths and J. P. Foster selection, whereby small tadpoles die at the expense of large tadpoles, but their genetic relatedness insures a high degree of inclusive tness. Werner (1992) raised frog tadpoles (Rana sylvatica and R. pipiens) under fully interacting conditions but at different densities with a per capita food ration. There was little difference between treatments in terms of growth, suggesting that interference competition may be relatively unimportant in these species. In contrast, the present results suggest that behavioural interactions between individuals result in increased variation in growth. Thus interference competition in tadpoles may be independent of density and related to the nature of the interaction, rather than the frequency of interaction, between individuals. Werner's (1992) results also suggest that high activity levels are related to superior exploitative ability. Certainly, the most active species studied in the present experiments (B. bufo) is a superior competitor, at least when raised with (Banks & Beebee, 1987). Growth inhibition in tadpoles can arise as a result of resource diversion by the inhibitory alga, Prototheca richardsi. Prototheca cells are excreted in the faeces of crowded tadpoles and appear to be highly attractive to small tadpoles. Consequently small tadpoles are diverted from other higher-quality food that may be available and growth rates decrease. Large tadpoles are less attracted to Prototheca-laden faeces and are consequently less affected (Beebee & Wong, 1992). Although the relative importance of this mechanism in nature is controversial (see reviews by Beebee, 1995; Grif ths, 1995; Petranka, 1995), Prototheca cells were detected in all experimental chambers and may therefore have affected the growth patterns observed. In fully interacting treatments tadpoles were more likely to have access to the faeces produced by other individuals, and any size discrepancies within the group could therefore have been accentuated. This would have resulted in increased variation in size with increased social interaction. In only one of the three species studied, B. bufo, did interactions between individuals result in slower average growth relative to controls raised in isolation. As this was also the only species that increased activity in the presence of conspeci cs, reduced growth may be a cost of aggregating in this species. Although this result appears to contrast with the ndings of Breden & Kelly (1982), who found that B. americanus tadpoles metamorphosed at a larger size when raised under fully interacting conditions, this may have been because they used size at metamorphosis rather than tadpole growth rate as a variable. As discussed above, slower-growing tadpoles may metamorphose later, but at a larger size, than earlier-metamorphosing counterparts. It is possible, then, that the principal bene t of aggregating for B. bufo tadpoles lies in reducing predation risk rather than facilitation. Alternatively, facilitation may be related to group size, and food quality and abundance. If so, perhaps the number of tadpoles used in the present experiment, or the relatively simplistic feeding regime, did not provide conditions under which facilitation could take effect. The tadpoles of and, appear to rely on lower levels of activity and crypsis (at least in ) to minimize predation risk. These two species consequently do not form large social aggregations and are less active than B. bufo. There may be some competition between pairs of individuals but little social facilitation. The result is increased variation in growth but no decrease in average growth rate for the population. Interestingly, this mechanism seems to operate on an interspeci c as well as an intraspeci c basis in these two species, but competition is asymmetric, as observed in other anurans (Morin & Johnson, 1988; Werner, 1992). The larger tadpoles perform better in the presence of, despite lower overall food levels, than when raised with conspeci cs. Under fully interacting conditions, the improved performance of may be related to physical interactions between species, release of inhibitory Prototheca and exploitative competition. Physical interactions were prevented under partially interacting conditions and the growth of at the expense of was less marked. As there was no reciprocal reduction in growth of in the presence of, however, other interactions may also play a role. In nature, factors such as group size, variations in food quality and abundance, and predation risk, will undoubtedly in uence the relative importance of competition and facilitation in groups of tadpoles. The present experiments suggest that in small groups and under per capita food resources, competition may be more important than facilitation. This effect is manifested by increased variation in growth and development between individuals at higher levels of interaction. Faster growth of some individuals at the expense of others may reduce the risk of catastrophic population losses as a result of pond desiccation. Clearly then, the consequences of group-living and competition are quite different in individuals and populations. Further research is needed to determine whether variation in growth rates is due to inherited tness differences between individuals, or to the ampli cation of chance differences in size that arise during early development. Acknowledgements This project was funded by the Natural Environment Research Council and the European Social Fund and licenced by English Nature. Rebecca May assisted with tadpole husbandry and measuring, Professor P. Brown provided statistical advice; Lee Brady, Trevor Beebee, Tim Halliday and Richard Tinsley provided helpful comments on previous drafts of the manuscript.

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