Invest in arms: behavioural and energetic implications of multiple autotomy in starfish (Asterias rubens)

Transcription

1 Behav Ecol Sociobiol (2001) 50: DOI /s ORIGINAL ARTICLE K. Ramsay M. J. Kaiser C. A. Richardson Invest in arms: behavioural and energetic implications of multiple autotomy in starfish (Asterias rubens) Received: 17 November 2000 / Revised: 26 March 2001 / Accepted: 11 April 2001 / Published online: 23 June 2001 Springer-Verlag 2001 Abstract The autotomy of body parts as a means of escaping predation or renewing damaged tissues has evolved in a number of animal groups. Starfishes are unique in that they can autotomise >75% of their body mass and continue to survive. Presumably, multiple autotomy of tissue has energetic costs in terms of potential fitness and may affect the allocation of energy reserves accordingly. We investigated arm autotomy, predatory capabilities and subsequent regeneration in common starfish, Asterias rubens, that were induced to lose one, two or three arms. Initially, both regeneration of autotomised arms and the rate of growth of intact arms was slowest in animals that had lost the most arms (i.e. three arms missing vs two arms missing vs one arm missing). However, 8 months later, the growth of intact arms since the start of the experiment was not significantly different between groups of starfish that had autotomised different numbers of arms. However, the average dry weight per regnerating arm was significantly higher in starfish that had autotomised the most arms. Arm loss decreased the ability of starfish to open mussels and those that had autotomised two arms were significantly less likely to feed successfully on a mussel in a 24-h period than intact starfish. Our data suggest that proportionally more energy is allocated to arm regeneration in starfish that have suffered multiple arm loss and this may compensate a potential decrease in fitness that results from decreased feeding capability. Keywords Energetic costs Autotomy Arm regeneration Starfish Predation Communicated by J. Krause K. Ramsay M.J. Kaiser ( ) C.A. Richardson School of Ocean Sciences, University of Wales-Bangor, Menai Bridge, Anglesey, LL59 5EY, UK m.j.kaiser@bangor.ac.uk Fax: Present address: K. Ramsay, Countryside Council for Wales, Ffordd Penrhos, Bangor, LL57 2LQ, UK Introduction Autotomy is the deliberate shedding of body parts or appendages used as an escape response to predators or as a means of replacing infected or damaged appendages (e.g. Emson and Wilkie 1980; Punzo 1982; Dial and Fitzpatrick 1983, 1984; Robinson et al. 1991; Smith 1992). Several animal groups have evolved the ability to autotomise and subsequently regenerate body parts. Among the best known examples of animals exhibiting such behaviour are the lizards, salamanders and slowworms that can autotomise and regenerate their tail or rear portion of the body (Pratt 1946; Wake and Dresner 1967; Sheppard and Bellairs 1972). In addition, many arthropods, including crustaceans (Juanes and Smith 1995), centipedes (Lewis 1981) and arachnids (Johnson and Jakob 1999) can autotomise limbs, while echinoderms are known to autotomise and regenerate body appendages and internal organs (Emson and Wilkie 1980). The autotomy of a body part results in an energetic cost in terms of the loss of tissues from the body (although see Johnson and Jakob 1999). The loss of body parts may have implications for the animal s mechanical performance, e.g. locomotion and the ability to capture and feed on prey (Punzo 1982; Juanes and Smith 1995). In some groups, the loss of appendages that function as adornments used to attract mates or for signalling among conspecifics can have social costs (Fox and Rostker 1982). Intense intraspecific competition among salamanders and blue crabs can lead to a high incidence of limb autotomy, although the costs associated with such energy losses are not thought to lead to regulation of population size through self-thinning (Vanbuskirk and Smith 1991; Smith 1995). Autotomy is relatively common within populations of starfish and increases with the abundance of natural predators (Ramsay et al. 2000a). In addition, anthropogenic disturbances such as intense physical perturbation of the seabed by towed bottom-fishing gears has led to an increase in the incidence of starfishes that exhibit evidence of autotomy and the proportion of starfishes

2 with multiple arm autotomy (Kaiser 1996).There is also some evidence that extremely high levels of fishing disturbance can lead to population declines of starfish through fishing-associated mortality (Ramsay et al. 2000b). The consequences of arm loss for asteroid starfishes may include a reduced capacity for feeding and locomotion and may result in the diversion of energy from growth or reproduction to regeneration of the affected body part (Lawrence 1992). Presumably, the allocation of energy to regeneration will reflect the relative importance of regeneration compared to other body processes, such as reproduction, somatic growth or nutrient storage. If replacement of autotomised tissues is crucial to the survival of the animal then any available energy might be expected to be partitioned to regeneration. However, Goss (1969) paradigm states that essential structures cannot regenerate (e.g. heart and liver), whilst non-essential structures do not, which implies that structures that are regenerated improve an organism s performance and hence fitness (Lawrence et al. 1986). Studies of arm regeneration in asteroids have focussed on energy allocation between regeneration, gonadal development and development of the pyloric caeca that secrete digestive enzymes (Lawrence et al. 1986; Lawrence and Ellwood 1991; Lares and Lawrence 1994). In Echinaster paucispinus fed low levels of food, regeneration was slow and energy allocation appeared to be primarily to the existing arms (Lares and Lawrence 1994). Similar results were obtained for Luidia clathrata fed a sub-maintenance diet. In this case, nutrients appeared to be primarily allocated to growth of the pyloric caeca and gonads of intact arms and secondarily to regeneration (Lawrence et al. 1986). In contrast, when these starfish were fed high levels of food, regeneration was faster (Lawrence and Ellwood 1991). These studies imply that starfish either divert energy to existing tissues or invest in regeneration of autotomised tissues according to the availability of food. We know of no studies that have investigated the allocation of energy following multiple arm autotomy. This is particularly relevant in starfish, because multiple arm loss occurs more frequently in areas of the seabed exposed to intensive bottom-fishing activities and is additional to arm loss resulting from natural predator pressure (Kaiser 1996; Ramsay et al. 2000a). The loss of increasing numbers of appendages may adversely affect performance (e.g. predation efficiency) and hence fitness. Thus the strategy for the allocation of energy to growth, reproduction or regeneration may differ according to the potential loss of fitness associated with the loss of differing numbers of appendages. To our knowledge, no one has investigated the consequences of multiple arm loss in starfish, and rates of arm regeneration following multiple arm loss appear to be unknown. The present study examined arm regeneration rates in common starfish following the loss of one, two or three arms and compared the feeding ability of intact starfish with those that had autotomised differing numbers of arms. Methods Regeneration after multiple arm autotomy 361 Fig. 1 The position of autotomised arms (A) in relation to the madreporite (M) in starfish that were induced to autotomise one, two or three arms Three groups of 20 starfish (Asterias rubens) were induced to autotomise either one, two or three arms by applying pressure half way down the arm with a pair of pliers. The arm chosen for autotomy was always the same relative to the position of the madreporite and adjacent arms were autotomised sequentially (Fig. 1). The time taken for the starfish to autotomise the arm was recorded from the moment the pressure was applied to the arm to the moment that tissue cleavage was completed. At the beginning of the experiment, no significant differences in arm length were apparent between the different treatment groups of starfish (average arm lengths, one arm autotomised 35.3±2.1 mm, two arms autotomised 34.5±1.8 mm, three arms autotomised 35.0±2.8 mm; ANOVA: F 2,57 =0.12, P=0.89). Due to the constraints of aquarium space, starfish were maintained in pairs in each of 30 small aquaria ( cm) supplied with ambient-temperature (6 14 C) running seawater. Starfish were fed ad libitum live mussels Mytilus edulis of varying sizes (5 40 mm shell height). Each pair of starfish received the same treatment to reduce any competitive bias that might be associated with the different treatments (e.g. starfish with five intact arms might be competitively superior to starfish with three arms). The experiment was conducted between 7 October 1999 and 12 June After 26 days, each starfish was examined and the length of all intact and regenerating arms measured (from the point where the arm joins the body to the arm tip). In our data analyses, we used two records for each starfish, the average length of the intact arms and the average length of the regenerating arms. Clearly, the number of arms used to calculate average length varied among treatments. These measurements were repeated approximately fortnightly for the following 8 months. On completion of the experiment, animals were killed and all five arms were removed by cutting from the proximal end of the row of adambulacral spines on one side of the arm to the same point on the other side. The dry weight of entire individual arms was determined after drying at 60 C to a constant weight. Dry weight is a better indicator than length of the energy invested in individual starfish arms, but could only be quantified at the end of the experiment. The measurement of entire arms overlooked the possibility that the proportion of the dry weight of the internal organs (pyloric caeca and gonads) and body wall might differ among

3 362 treatments at the beginning and end of the experiment, as may the concentration or type of organic compounds that occurred in intact and regenerating arms. While it was possible to compare the increment in weight of regenerating arms from the start to the end of the experiment (the start weight was 0 g), only differences in the final weight of the intact arms could be tested. We tested for differences among treatments with respect to the increment in arm length with time using an analysis of covariance on ln-transformed data for the intact arms and on untransformed data for the regenerating arms. Feeding success The following experiment was undertaken to investigate how multiple arm autotomy may influence the feeding ability of starfish. Starfish (diameter 5 7 cm) were divided into 12 replicate groups of six, of which two animals were left intact, two were induced to autotomise a single arm and two to autotomise two arms, using the method described above. Each group of six starfish was held in one of 12 aquarium tanks (dimensions as above). Starfish were starved for 7 days to standardise hunger levels. Following the starvation period, each starfish was placed separately into an individual tank, containing a single mussel (shell length cm). Individual starfish were used only once during the experiment. No significant differences were apparent in the size of either starfish or mussels between groups (ANOVA: starfish arm length F 2,67 =0.43, P=0.65; mussel length F 2,67 =1.83, P=0.17). The tanks were left undisturbed for 24 h whilst starfish feeding activity was recorded using a video camera. Feeding was considered to start when the starfish adopted the characteristic humped feeding position over the mussel and to end when the starfish moved away from a consumed mussel. A feeding attempt was deemed to have been unsuccessful if the starfish had failed to open the mussel at the end of the 24-h feeding trial. We tested for significant differences among treatments using a χ 2 -test with the null hypothesis that 50% of starfish from each treatment would feed successfully on the mussels presented to them. Results Arm autotomy and regeneration The time taken for starfish to autotomise an arm was longest for the first arm and decreased with increasing numbers of arms autotomised [ln time (s) (±SD); first arm 3.76±1.10, second arm 3.36±0.91, third arm 3.12±0.86; ANOVA, F 2,112 =3.79, P=0.025]. An analysis of covariance of the increase in the size of the regenerating arms with time indicated that there was no effect of treatment (Fig. 2; ANCOVA, F 2,1014 =0.53, P=0.59). The increase in length (ln-transformed) of intact arms varied according to the number of arms autotomised (ANCOVA, F 2,1014 =19.01, P<0.0001) as did the rate of increment (Fig. 2). Starfish that had autotomised more than one arm increased their arm length at a significantly different rate than those that had autotomised only one arm (Fig. 2). An examination of the differences among treatments at different points during the experiment revealed that arm length was significantly different among treatments midway through the experiment whereas by the end of the experiment there was no difference in arm lengths among the different treatment groups (average lengths of intact arms after 130 days: one arm autotomised 51.7±3.2 mm, two arms autotomised 46.0±4.0 mm, Fig. 2 Average lengths of regenerating arms (a) and intact arms (b) in starfish that were induced to autotomise one, two or three arms. The slope for regenerating arms did not vary significantly among treatments (one arm vs two arms regenerating: t 1,678 = 0.69, P=0.77; one arm vs three arms: t 1,678 = 1.07, P=0.53; two versus three arms: t 1,678 = 0.37, P=0.93) In contrast, the slopes for intact arms varied significantly (ln-transformed data) among treatments (one arm vs two arms regenerating: t 1,678 = 4.45, P<0.001; one arm vs three arms: t 1,678 = 6.55, P<0.0001; two versus three arms: t 1,678 = 2.09, P=0.09, n.s.) three arms autotomised 42.6±2.8 mm; ANOVA, F 2,57 = 7.19, P=0.002; after 249 days: one arm autotomised 66.4±3.6 mm, two arms autotomised 64.1±3.4 mm, three arms autotomised 66.5±2.9 mm; ANOVA, F 2,56 =0.63, P=0.54). The change in dry weight of the arms at the end of the experiment was used as a proxy for energy allocation to growth of regenerating arms. The average dry weight of those arms in the process of regeneration was significantly higher in starfish that had lost the most arms (Table 1). The change in dry weight of intact arms could not be ascertained as this would have required destructive sampling. Hence, the dry weight of intact arms could only be determined at the end of the experiment. For intact arms, the average dry weight per arm did not vary with the number of arms lost (Table 1). Feeding success Direct observations revealed three distinct behavioural outcomes during each feeding trial: the starfish would (1) move over the mussel and not attempt to feed, (2) at-

4 363 Table 1 Mean [±95% confidence interval (CI)] dry weight per arm at the end of the 249 days of the regeneration experiment. The dry weight of the regenerating arms represents the increase in weight from 0 g, i.e. at the beginning of the experiment. Values shown with an asterisk are significantly different from each other (P<0.005) Average dry weight per arm (g) ANOVA results F df P Intact arms One arm autotomised 3.04± , Two arms autotomised 2.69±0.18 Three arms autotomised 2.79±0.24 Regenerating arms One arm autotomised 1.06±0.19* , Two arms autotomised 1.22±0.11 Three arms autotomised 1.42±0.21* Table 2 The percentage of starfish with five, four or three intact arms that consumed a mussel within 24 h Number of intact arms Percentage of starfish that χ 2 df P consumed a mussel in 24 h Five arms (n=24) Four arms (n=23) 39 Three arms (n=23) 26 Table 3 Mean (±95% CI) feeding times for starfish with five, four or three intact arms Number of intact arms Average feeding ANOVA time (h) F df P Five arms (n=18) 13.4± , Four arms (n=9) 14.7±6.2 Three arms (n=6) 12.8±3.2 tempt to subdue the prey but not succeed by the end of the 24 h trial, and (3) attempt to feed and subdue the prey within the 24-h period. Only two individuals fell into category 2, one starfish with four arms and the other with three intact arms. For the purposes of our analysis, these starfish were excluded. A greater proportion of starfish with five intact arms were able to consume a mussel within 24 h than those that had autotomised one arm and a greater proportion of these, in turn, were able to consume a mussel than starfish that had autotomised two arms (Table 2). The average time taken to consume a mussel was highly variable (from just under 5 to over 24 h). Consequently, there was no significant difference in consumption time among treatment groups, although the number of data points was relatively low for starfish that had autotomised one or two arms (Table 3). Discussion Autotomy has evolved as a mechanism of escape from predation or as a means of renewing damaged or infected body tissues. Although this may be perceived as an energetically costly mechanism of predator avoidance, the alternative may be death. Hence, it is perhaps not surprising that when exposed to repeated simulated predator attacks (the application of direct pressure to the starfish arm), starfish autotomise consecutive arms more rapidly than the first arm that was autotomised. Nevertheless, arm loss is costly in terms of potential fitness and the present study demonstrated that increasing arm loss adversely affected the likelihood that a starfish would attempt to consume prey of a standard size. Similar findings have been noted for other starfish species, such as Luidia clathrata (Slater and Lawrence 1980). In our study, A. rubens that had autotomised two arms had the lowest percentage of feeding attempts (26%) when tackling mussel prey (cf. 39% for those that had autotomised one arm and 83% for intact starfish) and often did not attempt to feed. The latter behaviour implies that starfish that had autotomised multiple arms were either incapable of tackling the prey presented or that such an attempt would have been energetically too costly. The fact that starfish passed over the mussel prey and then did not attempt to feed perhaps suggests that they can assess the vulnerability of their prey. Other studies have shown that starfish tend to select mussels of a size that maximises their rate of energy intake (McClintock and Robnett 1986; Campbell 1987; Sommer et al. 1999). Thus a starfish confronted with prey of an unsuitable size (relative to the size of the starfish) is more likely to reject these prey and continue searching for prey of an appropriate size (Sommer et al. 1999). The present study suggests that, as well as body size, the number of intact arms influences the foraging capabilities of starfish and may cause them to adjust their diet accordingly. The possibility that starfish would adjust their diet according to their physical capabilities was not addressed in this study but such a study would clearly be of great value.

5 364 Robinson et al. (1991) studied the importance of the autotomy and regeneration of caudal lamellae in damselfly larvae. These larvae suffer a high incidence of cannibalism and larvae that were able to autotomise their lamellae in response to intraspecific predation attempts were more likely to survive than those that had already lost their lamellae. However, as the caudal lamellae are involved in both swimming and respiration, their autotomy incurred costs in loss of potential fitness. Robinson et al. (1991) found that the damselfly larvae were more reluctant to display predator avoidance behaviours such as swimming when they had autotomised their lamellae. Furthermore, larvae without lamellae were found to position themselves closer to the air/water interface to enable them to acquire sufficient oxygen for respiration but at the expense of an increased risk of predation. In the present study, the time taken by a starfish to consume a mussel appeared to be highly variable and no relationship between time and the number of arms autotomised was apparent (Table 3). However, this result is a little misleading, because only 26% of starfish with three arms succeeded in overcoming mussel prey within 24 h compared with 83% of starfish with five arms. Sommer et al. (1999) reported the relationship between starfish (A. rubens) size and the preferred size range of mussels (M. edulis) consumed. Using their equations, we estimated that for the size of starfish used in our experiments, the preferred mussel size range would be mm shell length and the maximum size would be 31.8 mm. Mussels of mm shell length were offered to the starfish in the present study, and were therefore towards the upper limit of the preferred size range of prey, and this may explain the variable feeding times we observed. Lawrence and Ellwood (1991) found that the rate of growth of regenerating arms exceeded that of intact arms in L. clathrata and A. vulgaris. This was also the case in our study of A. rubens, in which the average increase in length of intact arms was 31±1 mm in 8 months, whilst the average growth of regenerating arms was 46±1 mm over the same time period. However, using increase in arm length may be unrepresentative of energy allocation and dry weight of body tissue is probably a better predictor. The relationship between length and dry weight was logarithmic and thus an increase in the length of an intact arm corresponds to a greater weight increase than the same length of a regenerating arm. Accordingly, the average increase in dry weight per arm was greater for intact arms ( g) than for regenerating arms ( g) in all three treatment groups. This suggests that, overall, more energy per arm may be allocated to growth of intact arms than to regeneration. We know of no studies that have investigated the strategies used for energy allocation following multiple autotomy. From the results of our feeding experiment, the number of intact arms appeared to be positively correlated with feeding success and, consequently, potential fitness. Arm loss may also affect locomotion, nutrient storage and reproduction (Lawrence 1992; Lawrence and Larrain 1994). One would expect that the allocation of energy to the regeneration of particular tissues would be positively correlated with the increase in fitness gained by regenerating those tissues. Therefore, starfish that had lost more arms might be expected to allocate more energy to their regeneration, as appears to be the case in the present study. During the first 2 months of the experiment, the starfish with three autotomised arms began to regenerate them but did not increase the length of their intact arms. In contrast, the starfishes that had autotomised only one arm increased the length of their intact arms by 8.5 mm. At the end of the 8-month experimental period, the average dry weight of intact arms was the same regardless of the number of arms that had been autotomised, but the average dry weights of regenerating arms were significantly different. The starfish that had the most regenerating arms had the heaviest arms in terms of dry weight. Thus the energy allocated to regeneration appears to be positively correlated with the number of arms autotomised. This may reflect the disadvantages of multiple arm loss and a pressing need to regenerate these tissues to a condition that restores the feed capabilities of the starfish. In summary, animals that had autotomised multiple arms had reduced feeding success compared with those that had autotomised only one arm. This may have led to the initially slower regeneration and growth of the intact arms observed in animals with multiple arm loss. However, after approximately 4 months, the growth rates of both regenerating and intact arms increased, such that there were no differences in the arm length of the intact or the regenerating arms of either the two-, three-, or four-armed starfish. Nevertheless, the investment of energy in terms of dry weight was greatest in regenerating arms of starfish with multiple arm loss. The observed differential growth rates in the latter part of the experiment are probably related to improved feeding capabilities or result from the diversion of energy away from another function, such as reproductive development. More energy may be allocated to regeneration in starfish that have lost more arms and this may reflect the decrease in fitness resulting from multiple arm loss. The present study demonstrates that multiple arm autotomy in starfish is energetically costly. Multiple arm autotomy in starfish occurs with the highest frequencies in areas of the seabed that are intensively fished with bottom-fishing gears. While there is some benefit to starfish populations at low to medium levels of fishing disturbance from the energy subsidies gained from discarded bycatches and other animals killed on the seabed, at the highest levels of fishing disturbance, starfish populations begin to decline (Ramsay et al. 1997; Ramsay et al. 2000b). This population decline may be explained by multiple and frequent tissue damage and loss as a result of direct interactions with fishing gears. Acknowledgements This study was funded by the Ministry of Agriculture Fisheries and Food, Fisheries Division III, project code MF0714.

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