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Foraging and antipredator decisions in the hermit crab Pagurus acadianus (Benedict)
J. Exp. Mar. Biol. Ecol., 156 (1992) 225-238 © 1992 Elsevier Science Publishers BV. All rights reserved 0022-0981/92/$05.00
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Foraging and antipredator decisions in the hermit crab Pagurus acadianus (Benedict) •
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Alison M. Scarratt and Jean-Guy J. Godin Department of Biology, Mount Allison University, Sackville, New Brunswick, Canada (Received 27 June 1991; revision received 8 November 1991; accepted 11 November 1991)
Abstract: The hermit crab Pagurus acadianus (Benedict) possesses two major defences against mobile aquatic predators, viz., fleeing and refuging in its gastropod shell. When approached by a potential predator, a crab must choose to either continue its current activity (e.g., feeding), flee or hide in its shell. If a foraging crab flees when threatened, it must secondarily decide whether to carry its food item and, if so, how far to carry it whilst escaping. Alternatively, if the crab takes refuge in its shell, it must then decide how long to remain hidden and when to resume locomotory activity following emergence from the shell. Because these behavioural alternatives have associated costs (e.g., energy expenditure, predation risk, lost foraging pportunity), the crabs' decision as to which behaviour to adopt should be sensitive to the respective cost of each. We tested specific predictions of this general economic hypothesis ofbehavioural decision making by varying the weight of food items presented to crabs ( = lost feeding opportunity cost, energetic cost of carry) and the amount of time the crabs were "handled" by a predator following "capture" (-- predation risk). Most crabs tested fled from an approaching lobster predator model. Contrary to expectation, flight initiation distance was unaffected by the mass ofthe food item available to the foraging crabs. As predicted, however, the distances fleeing crabs carried individual food items varied inversely with the food's weight. Time spent hiding in the shell and latency to resume locomotion following a predator"attack" were relatively unaffected by the size of the food item available. As expected, the crabs' decision to emerge from their shell following a threat appeared sensitive to their perceived risk of predation, as evidenced by an observed positive relationship between refuging time (in shell) and the duration of preceding handling of the crab by the predator. These findings are interpreted within the cost-benefit framework of behavioural decision making. Key words: Antipredation; Crab; Decision making; Foraging; Predation risk; Trade-off
INTRODUCTION
Animals have evolved diverse behavioural responses to predators and show considerable flexibility in these responses over their lifetime (e.g., Ydenberg & Dill, 1986; Sih, 1987; Lima & Dill, 1990). Such responses include fleeing, hiding in a physical refuge, joining a social group or mobbing when a potential predator has been detected. Although an animal may reduce its risk of predation by actively fleeing from a predator and (or) by hiding in a refuge, it may incur potential costs, such as lost foraging opportunities, in doing so (Ydenberg & Dill, 1986; Sih, 1987). Because the cost of Correspondence address: J.-G.J. Godin, Department of Biology, Mount Allison University, Sackville, New Brunswick E0A 3C0, Canada.
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foraging under predation hazard may be death (Godin & Smith, 1988), prey animals are expected to trade off foraging gains and risk of mortality from predation in choosing the behavioural alternative which maximizes fitness (reviewed by Milinski, 1986; Dill, 1987; Godin, 1990; Lima & Dill, 1990). A foraging individual should thus delay its antipredator response to an approaching predator when expected fitness benefits from continued foraging exceed the costs of delaying (Ydenberg & Dill, 1986; Dill & Ydenberg, 1987; Dill & Houtman, 1989). Moreover, the type and intensity of the antipredator response exhibited should be sensitive to its costs and to the current threat of predation, as assessed by the prey (Sih, 1987; Helfman, 1989; Lima & Dill, 1990). Here we investigate, within the framework of the above general economic (costbenefit) hypotheses, foraging and antipredator decisions in hermit crabs Pagurus acadianus (Benedict) exposed to a simulated threat of predation from a lobster model. P. acadianus typically inhabits the boreal marine sublittoral zone (Logan et al., 19,~,), where it is exposed to predators such as lobsters Homarus americanus (Logan ~t al., 1983; Elner & Campbell, 1987). Unlike most adult decapod crustaceans, the abdomen of hermit crabs is not covered by a hard carapace. Instead, they occupy empty gastropod shells, which provide protection against physical abrasion and predators (Reese, 1969; Hazlett, 1981; Lancaster, 1988); almost all known species are mobile while occupying such shells (Hazlett, 1981). Hermit crabs are in general omnivorous detdtivores (Reese, 1969). To forage effectively, the crab must extend its cephalothorax and legs out of the shell aperture. However, this also exposes it to predators. When confronted by an approaching aquatic predator, P. acadianus typically exhibits one of two antipredator responses. The crab may either rapidly move "away from an attacking predator (= flight) or remain stationary and withdraw into its shell ( = refuging), leaving only the tips of its chelae exposed (pers. obs.). However, a fleeing or refuging crab cannot forage, and thereby potentially incurs a cost of lost foraging opportunity. Because foraging and antipredator behaviours (i.e., fleeing, hiding in shell) appear to be mutually exclusive activities in hermit crabs, they are thus ideal subjects for investigating behavioural decisions (sensu Dill, 1987) made when foraging and predator avoidance (or escape) conflict. Decision making in this context has not been previously studied in hermit crabs, although other behavioural decisions have been addressed (e.g., Elwood & Stewart, 1985; Hazlett, 1987; Jackson & Elwood, 1990). In the current study, individual hermit crabs were initially given a choice between remaining stationary, and continuing to feed on a food item of standardized mass, and escape from an approaching potential predator (a lobster model) in the laboratory. We predicted that foraging crabs would delay their flight from the "attacking" predator longer to continue foraging, and thus show shorter flight initiation distances, with increasing mass ( = potential energetic value) of the food item available to them, thus reflecting a trade off between predation risk and immediate foraging gains. Secondly, we predicted that both the likelihood of a food item being carried and the distance carried would decrease with increasing mass of the food item, presumably owing to increased energetic cost of transport and predation risk (through reduced escape speed
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and increased conspicuousness). Finally, at some point along its attack path, the predator model eventually came into contact with the crab. Physical contact between predator and prey was maintained for different standardized periods of time, thereby simulating different predator "handling times" and thus different apparent risk of mortality to predation. We also predicted that, if hermit crabs are sensitive to variations in predation risk (cf. Helfman, 1989), they ought to remain hidden in their shell and delay resuming locomotion longer when predation risk is perceived to be greater, but at an increasing cost of lost opportunity to forage.
MATERIALS AND METHODS ANIMALS AND HOLDING CONDITIONS
Hermit crabs were collected subtidally by scuba diving in Passamaquoddy Bay, near the Huntsman Marine Science Centre, St Andrews, New Brunswick, Canada (45 ° 05' N, 67 ° 04'W), between May and October 1989. The crabs were transported to Mount Allison University, where they were held in plastic tanks supplied with running seawater (13.7 + 0.3 °C) and exposed to a 12 L" 12 D illumination regime. Empty gastropod shells were placed in the tanks, so that the crabs could change their shell if necessary. Crabs were fed ad libitum a mixed diet of frozen haddock Melanogrammus aeglefinus and a specialized crustacean food (Halifax Standard Reference Diet No. 84; Fisheries and Oceans Canada) thrice weekly. The experimental crabs weighed on average 1.52 g (SE = 0.04, range = 0.48-2.96, n = 159) and carried a gastropod shell weighing 3.25 g (SE -- 0.06, range -- 1.63-6.41). Crabs primarily occupied Littorina littorea (66.7 ~o)or Nucella lapillus (25.2~o) shells at the time they were tested. The particular gastropod shell species occupied by the crabs had no consistent effect on their antipredator behaviours in this study. A crab's sex could only be determined with certainty by removing it from its shell at the end of an experimental trial. Most (67.9~o) of our crabs were females. Since the behaviours recorded in this study did not differ between the sexes, the data were pooled over both sexes for analysis. HERMIT CRAB-LIVE LOBSTER INTERACTIONS
Observations were made on the behaviour of hermit crabs in the presence of a live lobster to ascertain the types of antipredator responses exhibited towards this predator, and to confirm whether these responses were qualitatively similar to those exhibited towards a realistic lobster model used in this study. Interactions between a live lobster (major chela = 9 x 5 cm; L x W), previously deprived of food for 48 h, and four to six hermit crabs in a rectangular seawater tank (90 x 60 x 28 cm) were recorded over 3 consecutive days (total = 24 h observations) using an overhead video camera under dim red light. Crabs were not provided with any food in these trials. Frequencies of lobster
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attacks, crab antipredator responses and attack success were quantified from the video tapes. HERMIT
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INTERACTIONS
Experimental tank Behavioural responses of hermit crabs toward~ a lobster model (see below) were observed in two identical Plexiglas tanks (92 x 20 x 25 cm; Fig. 1), each supplied with recirculating (,~ 1 1. rain - ~) filtered seawater maimained at 10.5 + 0.3 ° C and exposed to a 12 L ' 12 D illumination regime (fluorescent light intensity -- 100 Ix at the surface).
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The bottom and three sides of each tank were covered externally with light blue cardboard, partly to reduce external disturbance. To facilitate distance measurements, the cardboard on the back wall and bottom of each tank were demarcated at 5-cm intervals with marker lines. A shaded hide (25.5 x 20 x 25 cm) to conceal the predator model was constructed at the water inlet end of the tank by placing a styrofoam root" over the area, covering the walls with black polyethylene plastic and dropping a black plastic curtain half way down the water column at the entrance to the hide (Fig. 1). A circular clear Plexiglas cylinder (15 cm diameter), used to restrain individual crabs before the onset of an experimental trial, was placed 45 cm away from the entrance to the predator's hide (Fig. 1). The cylinder could be raised remotely with the aid of a pulley system, thereby allowing the crab to move freely within the tank. Both ~anks were located behind a blind to minimize external disturbance of the animals. Behavioural observations were made through two small horizontal windows, covered with black fibreglass netting, in the blind.
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Predator model Two identical predator models were constructed from molded plastic lobsters. The model's chelae (9 x 4.5 cm; L x W) were fully extended anteriorly and horizontally. The models were painted with acrylics to resemble a live lobster, covered with a thin coat offibreglass resin and mounted on a right-angle shaped, clear glass rod (for manual presentation). Prior to introducing a hermit crab into the experimental tank, the predator model was hidden in the darkened hide, where it remai~ecl Stationary on the bottom with the attached glass rod protruding through a slit in the hide's roof and above the observation blind (Fig. 1). This apparatus allowed an observer, located behind the blind, to manually advance the model out of cover and along the bottom towards the crab at the other end of the tank.
Experimental protocol Prior to being introduced into the experimental tank, hermit crabs were deprived of food for 48 h to standardize hunger levels. Crabs were placed individually into the restraining cylinder in the experimental tank and allowed to acclimatize for at least 2 h before being provided with a piece of haddock, of a predetermined standard weight (see below), as food. This food item was gendy dropped into the cylinder with the aid of a transparent plastic scoop attached to a glass rod. This food-provisioning procedure did not appear to disturb the crab. Four weight classes of food items were used, viz., 80-120, 180-220, 280-320 and 380-420 mg wet wt. For simplicity, these size classes will hereafter be referred to as the 100, 200, 300 and 400-mg food items. All but the smallest of these food items exceeded the amount of haddock (160 + 25 mg) a crab could consume over a relatively prolonged time period (8 h). If the test crab did not start feeding within 5 rain of food presentation, the trial was discontinued. Most crabs, however, began feeding within 1 min of food presentation. The test crab was allowed to feed for 20-25 s whilst the restraining cylinder was gently raised out of the tank. Raising the cylinder did not interrupt foraging. Over this latter period, our crabs could consume on average 2.6 + 0.5 mg of haddock, representing 1.6% of their satiation ration. We assumed that this feeding period was sufficient for the test crab to assess the size, and perhaps the potential energetic value, of the fiaod item presented without significantly altering its hunger level. After raising the restraining cylinder, the foraging crab was "attacked" by manually advancing the lobster model from the hide towards it at a standard speed of 8 + 0.5 cm s - ' We recorded: ''~ whether the crab subsequently fled or remained stationary in response to th,e approaching predator; and (ii) the distance the fleeing crab carried the food !,~em before dropping it. The distance separating predator model and crab at the instant the latter initiated flight was also recorded and is referred to as "flight initiation distance". Although most simulated attacks were initiated when the test crab was facing (0 _ 45 °) the approaching lobster model, a crab would sometimes rotate slightly just as the model began its "attack". We therefore categorized (in 45 ° sectors) _
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the orientation of the crab's shell aperture relative to the model's attack path, because the crab's orientation may determine the likelihood of visual predator detection and thus of flight initiation. In all trials, the attacking predator model eventually intercepted the fleeing or stationary crab, which immediately withdrew into its shell. Since hermit crabs are sensitive to external mechanical stimuli received through their shell (l-Iazlett, 1987), we attempted to simulate differential risk of predation by varying the amount of time the predator model "handled" the "captured" crab. "Handling" consisted of lightly, but continuously, contacting the crab with the tips of the model's chelae. Each test crab was exposed to one of four predetermined "predator handling times", viz., 0, 10, 20 or 30 s. We assumed that the longer a predator persists at handling a crab, the greater the risk of mortality the latter incurs. At the end of this handling period, the lobster model was removed from the tank. We then recorded the time the crab spent hiding in its shell, which is referred to as "hiding time" (does not include the preceding predator handling time). The latter ended when the crab's eye stalks were extended beyond the rim of the shell's aperture. The time elapsed between crab emergence from the shell and its resumption of locomotion was defined as "time to resume locomotion". The experimental design therefore consisted of four different food treatments ( = different sized food items) and four predation hazard treatments (= different predator handling times). Each combination of food and predation hazard treatments was randomly predetermined and replicated with at least 10 different crabs (except for four combinations, due to the unavailability of naive animals). No crab was used more than once in this study. CONTROLS FOR PREDATOR MODEL
Control trials were carried out to ascertain whether the observed crab antipredator responses towards the lobster model were due to the threatening nature of the model or simply to novelty or disturbance associated with its presentation. Individual crabs were exposed to the mov'ng glass rod only in one series of trials (n -- 5) and to a green sponge (area presented = 8 x 5 cm), attached to the end of the glass rod, in a second series 01 = 5). These control trials were carried out in a similar manner to the ones described above, except that the crabs were not handled by the rod or sponge here. Crab behaviours in these control trials were recorded as described above, and compared with the behaviours of crabs (n = 10) which were approached (but not handled) by the lobster model. Crabs in these trials had access to a 100-mg food item. DATA ANALYSIS
Data were normalized by log transformation prior to statistical analysis. Significance of treatment effects were tested using the two-way ANOVA and ANCOVA as appropriate. Mean scores were compared with the Tukey-Kramer test for multiple comparisons or the t test for paired comparisons as appropriate. The level of statistical
BEHAVIOURAL D E C I S I O N S IN T H R E A T E N E D H E R M I T CRABS
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significance was set at P < 0.05. All tests used are one-tailed and are described in Sokal & Rohlf (1981).
RESULTS INTERACTIONS WITH LIVE LOBSTER
A total of I 18 unambiguousattacks by the live lobster on hermit crabs were observed. Most (86.4 9o) of the attacks resulted in the crab fleeing from the approaching lobster. Flight was simply a rapid movement away from the lobster. Fleeing resulted in successful escape from the predator ,,,;-a~_,.,.! Or/oof all interactions, whereas the lobster overtook and came into physical contact with the fleeing crab on the remainder (54.9~o) of the interactions. Such "captured" (and handled) crabs immediately withdrew into their shell, and in only 10.79/0 of these captures was the shell crushed and occupant killed by the lobster. In a minority at attacks (13.69o), the crabs did not flee from the approaching lobster, but alternatively remained stationary and withdrew into their shell. On 43.79/0 of these attacks, the lobster captured the stationary crab which subsequently withdrew into its shell. Only 14.3 ~o of these crabs were killed. Therefore, hermit crabs exhibited two antipredator responses to an approaching predatory lobster, fleeing and hiding within their shell. INTERACTIONS WITH LOBSTER M O D E L
The antipredator responses exhibited by hermit crabs towards the approaching lobster model were qualitatively similar to those shown towards a live lobster (described above).
Fleeing Most test crabs (157 out of 159) fled from the approaching lobster model. Their overall mean + SE flight initiation distance was 8.8 + 0.5 cm. Since the distance at which individual crabs initiated their escape was negatively correlated (Spearman's rank correlation; rs = -0.26, t = 3.36, df = 157, P < 0.001) with the orientation of their shell's aperture relative to the predator's attack path, it was necessary to adjust fligh' initiation distance for the orientation covariate using the ANCOVA prior to testing for a treatment effect of food item size. When so adjusted, crab flight initiation distance was not significantly affected by the mass of the food item on which they were feeding ( A N C O V A ; F3.15 4 = 2.18, P > 0.05). Therefore, for a given body orientation, foraging crabs did not progressively delay their flight, and thereby exhibit shorter flight initiation distances, with increasing weight of the food item available within the range used.
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Carrying food Most (98.7 ~o) fleeing crabs carried the food item in their chelae during escape from the approaching predator model. Therefore, no relationship existed between the likelihood of a fleeing crab carrying a food item and the mass of the latter. The food item was eventually dropped by the crab at some distance along its escape path. Larger food items tended to be dropped sooner than smaller food items, as indicated by the observed (and predicted) negative relationship between the mass of the food item and the distance it was carried (linear regression; F~,~57 = 6.60, r = -0.20, P < 0.02; Fig. 2).
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Food item size (mg) Fig. 2. Relationship between mass of the food item on which individual hermit crabs were feeding when attack.d by a lobster model and mean + SE distance they carried the food item whilst fleeing. Numbers above bars denote sample size. Line-of-best-fit was obtained by least-squares linear regression.
Hiding #~ shell The time withdrawn crabs spent hiding in their shell was not affected (two-way ANOVA; F3.~43 --- 1.69, P > 0.15) by the mass of the food item it was feeding on prior to the predator's attack, but was by how long the crabs were previously handled by the p r e d a t o r (F3,14 3 -- 12.93, P < 0.001); there was no statistical interaction between these two treatments (F9,143 = 1.15, P > 0.30). However, the expected inverse relationship between crab hiding time and food item weight (i.e., expected lost foraging gains) may have been masked by the fact that smaller food items tended to be located closer to the hiding crab, and thus were perhaps less costly to retrieve, than the larger items in our study, as noted above. Even when statistically controlled for the distance the fleeing crab carried a food item before retreating in its shell, its hiding time remained unaffected by food mass (ANCOVA; F3.~54 = !.27, P > 0.25). Hiding time thus appears to have been determined mainly by the crab's cor.finu;Jus assessment of its risk of predation, which is assumed here to be positively corre!ated with predator handling time. As expected, when statistically contrglled for both the
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distance and size of the food item carried during flight, the time individual crabs spent hiding in their shell increased with increasing duration of the period they were handled by the predator model (ANCOVA; F3.1s3 = 1339, P < 0.001; Fig. 3). Therefore, the longer a crab was handled by a potential predmor, the more reluctant it was to emerge from its shell, regardless of potential foraging gains.
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Predator handlingtime (s) Fig. 3. Relationship between time crabs were "handled" by predator and mean + SE time they subsequently spent hiding in their shell. Different letters above bars denote significant differences (P < 0.05) among means (Tukey-Kramer multiple-means comparison test). Numbers above bars represent sample, size.
Resumption of locomotion after an attack Following emergence from its shell, a previously refuging crab must resume its locomotory activity if it is to locate food, but presumably at the cost of increased exposure to predators. The crabs' latency time to resume locomotion following emergence from their shell was influenced by the mass of the food item on which they h..' been feeding (two-way ANOVA; F3.~43 = 4.79, P < 0.005), but was not affected by the time they had been previously handled by the predator (Fa.143 = 1.56, P > 0.20); there was no statistical interaction between these two treatments (F9.~43 = 1.35, P > 0.20). The significant foodosize treatment effect persisted (F3.1s3 - 4.83, P < 0.005) when the latency data were subjected to an ANCOVA, which statistically controlled for both the varying distance of the food item from the emerging crab and the time it had previously been handled by the predator. However, the expected negative relationship between latency time to resume locomotion and food item mass was not apparent (Fig. 4). With the exception efthe 300-rag class, variation in the weight of the food items available had relatively little effect on the crabs' latency time to resume locomotion.
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Food item weight (mg) Fig. 4. Relationship between mass of food item on which individual hermit crabs were feeding when "attacked" by a lobster model and their subsequent mean + SE latency time to resume locomotion following emergence from their shell. Other details are as in Fig. 3.
CONTROLS FOR PREDATOR MODEL
Hermit crabs behaved differently towards the realistic lobster model than to either the glass rod only or the rod with a sponge attached. First, none of the crabs tested stopped feeding to flee from the approaching rod. In comparison, the crabs fled from both the approaching sponge and the lobster model, but their mean + SE flight initiation distance for the sponge (5.8 + 1.2 cm) was significantly shorter (t = 2.36, d f - 13, P < 0.05) than that for the lobster model (12.7 + 1.2 cm). Secovdly, the crabs did not hide in their shell when "attacked" by either the rod or the sponge, but did in response to the approaching lobster model and remained hidden for 3.1 + 1.6 s on average. Lastly, following the removal of the "attacking" object, the crabs took significantly longer on average (t = 3.55, df - 13, P < 0.01) to resume locomotion when they had just previously been "attacked" by the lobster model (12.5 + 1.3 s) compared to the sponge (1.4 + 1.5 s). They did not stop moving about in response to the approaching rod. These observations strongly indicate that the hermit crabs were able to discriminate between the three different objects presented and apparently assessed the lobster model as the most threatening. Therefore, we conclude that the behaviour of hermit crabs observed in this study were elicited specifically in response to a lobster model and not simply to the novelty or disturbance associated with the presentation of this model. DISCUSSION The hermit crab P. acadianus possesses two major defences against mobile aquatic predators, viz.: fleeing and refuging in i.ts .3hell. Because antipredator behaviours have associated costs such as lost opportunities to forage and increased energy expenditure,
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individual crabs ought to be sensitive to variations in these costs and the current risk of predation when making foraging and antipredator decisions (cf., Ydenberg & Dill, 1986; Dill, 1987; Abrahams & Dill, 1989; Hdfman, 1989; Lima & Dill, 1990). In the current study, hermit crabs responded to the simulated threat of predation from a lobster model in ways which are, for the most part, consistent with this general economic hypothesis. All hermit crabs (except two) fled in response to the approaching lobster model. However, contrary to the prediction of Ydenberg & Dill's (1986) economic model of escape from predators, crab flight initiation distance (FID) did not decrease progressively with an increase in the mass of the food item available (i.e., increasing potential cost of lost foraging opportunity due to flight). Therefore, it would appear that the timing of escape from an approaching predatory threat, and thus FID, in this hermit crab species is not sensitive to the potential lost opportunity cost of flight. In comparison, FID has previously been shown to be sensitive to variations in the costs of flight and the risk of mortality to predation in other animals (e.g., Dill & Ydenberg, 1987; Dill & Houtman, 1989; Dill, 1990). Perhaps animals which possess morphological defenses, such as shells in crabs and spines i, fishes (McLean & Godin, 1989), can afford to be relatively insensitive to varying risk of predation and lost opportunity costs of escape and thus to defer their flight until capture by a predator is imminent. Alternatively, our crabs may have assessed the different weights of food items presented as being of equal value, and thus initiated their flight at a similar distance from the predator, regardless of the mass of the food item on which they were feeding when "attacked". Animals (such as the hermit crabs in the current study) which forage on relatively large food items that cannot be consumed wholly and quickly may either: (i)escape without the food item; (ii) escape and carr~~the food item with them; or (iii) remain with the food and defend themselves when threatened by a predator (Formanowicz & Brodie, 1988). These behavioural option,~ have different benefits (expected energetic gains from the food) and costs (energetic cost of escape, risk of predation). Therefore, the forager should carry a food item whilst escaping only when the costs of carrying do not exceed the costs of interrupting feeding and lost foraging gains (Ydenberg & Dill, 1986; Formanowicz & Brodie, 1988). In the curren ~ study, all foraging hermit crabs (except two) carried the food item while fleeing from an approaching predator, regardless of the weight of the food item. Therefore, their decision to carry or abandon a food item at the instant of flight initiation was unaffected by the food item's weight (at least within the range of weights tested here). In contrast, ~orat~mg " " ..... ~-~" Procambarus clarkii (Bellman & Krasne, 1983) and fiddler crabs Uca panacea (Formanowicz & uu items Brodie, 1988) faced with a predator)' threat are: more likely to carry sm,m - - " ~t, c^^.~ than large ones when escaping. These different results may reflect differences between the studies in the relative size of food items used. On average, the weights of the food items presented to crayfish (Bellman & Krasne, 1983) and fiddler crabs (Formanowicz & Brodie, 1988) represented 30-300 and 19-128Y/o, respectively, of their live body weights, compared with 6-26°/o for hermit crabs in the current study.
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However, we further noted an inverse relationship between the weight of a food item and the distance it was carried by a fleeing hermit crab, before it was abandoned. We offer two possible explanations for this novel finding. First, hermit crabs may have assessed the relative benefits and costs of carrying or abandoning a food item during the course of their flight from the predator, but not before. Because predation risk (through decreased escape speed and increased conspicuousness) and energy expenditure likely increase in escaping crabs with increasing amount of weight carried (Formanowicz & Brodie, 1988), the costs of carrying a food item may exceed expected benefits (future foraging gains) sooner for larger food items than smaller ones. Therefore, a fleeing forager ought to carry a large food item over a shorter distance than a smaller one before dropping it, thereby trading off expected foraging gains and risk of mortality to predation. Our results are consistent with such an economic hypothesis. Alternatively, larger food items may have been more readily stripped from the fleeing crab's chela by drag forces, and consequently were carried shorter distances, than smaller items. Further experimentation is required to determine which mechanism is more plausible. Once "captured" by the lobster model, a fleeing crab typically withdrew within its shell. In doing so, the crab minimized its risk of predation but at the cost of lost energetic gains from foraging. Therefore, if hermit crabs are sensitive to variations in this cost, then their hiding time should be inversely related to the weight of the food item (i.e., expected future energetic gains) on which they were feeding prior to the predator's attack. We did not observe such a monotonic relationship, suggesting that the crabs' decision to emerge from their shell, at the cost of increased predation risk, is not based simply on their expected energetic gains from foraging in the immediate future. Greater risk taking in individuals with expectations of immediate or greater food rewards has been demonstrated in other species (e.g., Fraser & Huntingford, 1986; Godin & Smith, 1988; Godin & Sproul, 1988; Dill et al., 1990). However, since lobsters can also scavenge (cf., Elner & Campbell, 1987, pers. obs.), and may feed on any food dropped by fleeing prey, the presence nearby of a previously-dropped food item may be very uncertain to a refuging crab. This uncertainty may render the mass of such a food item an unreliable indicator of potential future r~wards and thus for basing decisions on when to emerge from hiding. Notwithstanding the potential effects of foraging opportunities, threatened hermit crabs may also have been sensitive to var.~ation in (apparent) predation risk in deciding when to emerge from their shell. As predicted, the time individual crabs spent hiding in their shell increased with increasing predator handling time, a presumed correlate of predation risk. This observed relationship suggests that this crab's shell refuging behaviour is ~hreat sensitive (sensu Helfinan, 1989). While hiding in its shell, a crab presumably cannot see its predator but may be able to smell it. Because a model predator was used in this study, predator olfactory cues were absent. Therefore, in the absence of visual and olfactory cues about the presence of the predator, a hiding hermit crab may alternatively be able to use mechanical stimuli transmitted through its shell, while being
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237
handled by the predator, to assess its current risk of predation. Our results support the notion that the crabs used the duration of the predator handling period as an indicator of the current risk of predation when deciding to emerge from their shell. Upon emerging from its shell following a threat of predation, a crab must then decide when to resume locomotory activity, perhaps in search of food. Such activity also has associated costs, in terms of energy expenditure and increased predation risk, and benefits, such as increased probability of encountering food. It would thus be prudent for the animal to delay movement if the predator is ~till nearby, which could be assessed visually or olfactorily. If it is not (as was the case in our study), then the decision to resume movement may be dependent on the crab's hunger level and (or) the expected value of a future food reward, which could be reinforced by chemical cues from the food item (cf., Hazlett, 1971). The expected inverse relationship between latency time to resume locomotion and food item mass was not observed in the current study. This could mean that the crabs do not use the assessed'quality of a resource ( = mass of a food item) to decide when to resume locomotion following a threat of predation, as they do when deciding to resume shell investigative behaviour following a startle stimulus based on the quality of another resource, the shell under investigation (Jackson & Elwood, 1990). Alternatively, as suggested above, the absence of the aforementioned expected relationship may have been due to the crabs having valued equally the different food sizes available in the current study, all of which could have exceeded a certain threshold mass above which food items are categorized similarly as high quality. Varying hunger level is unlikely to be important in our study since it was standardized among the experimental animals. In general, the results of this study support the hypothesis that hermit crabs are able to assess their current risk of predation and the costs of predator avoidance (or escape) in making a number of foraging and antipredator decisions. ..
ACKNOWLEDGEM ENTS
We gratefully acknowledge the assistance of R. W. Rangeley in the collection of crabs in the field, S. Davis in setting up the experimental apparatus, and D.J. Scarratt in providing the prepared crustacean food. The Huntsman Marine Science Centre provided diving and temporary animal holding facilities. We also thank R. Aiken, L.A. Dugatkin, R. W. Elwood, V. Gotceitas, R. W. Rangeley and two anonymous referees for their helpful comments on earlier versions of the paper. This study was supported by grants to J.-G.J. Godin from NSERC Canada and Employment & Immigration Canada's Challenge '89 summer program.
REFERENCES Abrahams, M.V. & L.M. Dill, 1989. A determination of the energetic equivalence of the risk of predation. Ecology, Voi. 70, pp. 999-1007.
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Bellman, K.L. & F.B. Krasne, 1983. Adaptive complexity of interactions between feeding and escape in crayfish. Science, Vol. 221, pp. 779-781. Dill, L. M., 1987. Animal decision making and its ecological consequences: the future of aquatic ecology and behaviour. Can. J. ZooL, Vol. 65, pp. 803-811. Dill, L.M., 1990. Distance-to-cover and the escape decisions of an African cichlid fish, Melanochromis chipokae. Environ. Biol. Fish., Vol. 27, pp. 147-152. Dill, L.M., A. H.G. Fraser & B.D. Roitberg, 1990. The economics of escape behaviour in the pea aphid, Acyrthosiphon pisum. Oecologia, Vol. 83, pp. 473-478. Dill, L.M. & R. Houtman, 1989. The influence ofdistance to refuge on flight initiation distance in the gray squirrel (Sciurus carofinensis). Can. J. Zool., Vol. 67, pp. 233-235. Dill, L.M. & R.C. Ydenberg, 1987. The group size-flight distance relationship in water striders (Gerris remigis). Can. J. Zool., Vol. 65, pp. 223-226. Elner, R.W. & A. Campbell, 1987. Natural diets of lobster Homarus americanus from barren ground and macroalgal habitats off southwestern Nova Scotia, Canada. Mar. Ecol. Prog. Ser., Vol. 37, pp. 131-140. EIwood, R.W. & A. Stewart, 1985. The timing of decisions duri" ~ shell investigation by the hermit crab, Pagurus benahardus. Anita. Behav., Voi. 33, pp. 620-627. Formanowicz, D. R., Jr. & E.D. Brodie, Jr., 1988. Predation risk and forager escape tactics. Anim. Behav., Vol. 36, pp. 1836-1838. Fraser, D.F. & F.A. Huntingford, 1986. Feeding and avoiding predation hazard: the behavioral response of the prey. Ethology, Vol. 73, pp. 56-68. Godin, J.-G. J., 1990. Diet selection under the risk of predation. In, Behavioural mechanisms offood selection, edited by R.N. Hughes, NATO ASI Ser., Vol. G20, Springer-Verlag, Berlin, pp. 739-769. Godin, J.-G.J. & S.A. Smith, 1988 A fitness cost of foraging in the guppy. Nature, Vol. 333, pp. 69-71. Godin, J.-G.J. & C.D. Sproul, 1988. Risk taking in parasitized sticklebacks under threat of predation: effects of energetic need and food availability. Can. J. Zoo'., Vol. 66, pp. 2360-2367. Hazlett: B.A., 1971. Chemical and chemotactic stimulation of feeding behavior in the hermit crab Petrochirus diogenes. Comp. Biochem. Physiol., Vol. 39A, pp. 665-670. Hazlett, B.A., 1981. The behavioral ecology of hermit crabs. Annu. Rev. Ecol. Syst., Vol. 12, pp. 1-22. Hazlett, B.A., 1987. Information transfer during shell exchange in the hermit crab Ciibanarius antiilensis. An#t, Behav., Vol. 35, pp. 218-226. Helfman, G.S., 1989. Threat-sensitive predator-avoidance in damselfish-trumpetfish interactions. Behav. Ecol. Sociobiol., Vol. 24, pp. 47-58. Jackson, N.W. & R.W. Elwood, 1990. Interrupting an assessment process to probe changes in the motivational state. Anita. Behav., Vol. 39, pp, 1068-1077. Lancaster, i., 1988. Pagurus benzhardus ( L . ) u an introduction to the natural history of hermit crabs. Field Stud,, Vol. 7, pp. 189-238. Lima° S.L. & L.M. Dill, 1990. Behavioral decisions made under the risk of predation: a review and prospectus. Cat,, J. ZooL, Vol. 68, pp. 619-640. Logan, A., A. A, Mackay & J. P. A. Noble, 1983. Sublittoral hard substrates. In, Marine and coastal systems of the Quoddy region, New Brunswick, edited by M. L. H. Thomas, Can. Spec. Publ. Fish. Aquat. Sci., Vol. 54, pp. 119-139. McLean, E.B. & J.-G.J. Godin, 1989. Distance to cover and fleeing from predators in fish with different • amounts of defensive armour. Oikos, Vol. 55, pp. 281-290. Milinski, M., 1986. Constraints placed by predators on feeding behaviour. In, The behaviour of teleostfishes, edited by T.J. Pitcher, Croom Helm~ ~ ondon, pp. 236-252. Reese, E.S., 1969. Behavioral adaptations of intertidal hermit crabs. Am. Zool., Vol. 9, pp. 343-355. Sih, A., 1987. Predators and prey lifestyles: an evolutionary and ecological overview. In, Predation: direct and indirect impacts on aquatic communities, edited by W.C. Kerfoot & A. Sih, University Press of New England, Hanover, pp. 203-224. Sokal, R.R. & F.J. Rohlf, 198l. Biometry. W.II. F~ce,',a~ & Co., New Y~z~%second ,u~uu,,~'~:':^-859 pp. Ydenberg, R.C. & L.M. Diq, 1986. The economics of fleeing from predators. Adv. Study Behav., Vol. 16, pp. 229-249.
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JEMBE 01729
Foraging and antipredator decisions in the hermit crab Pagurus acadianus (Benedict) •
~j
Alison M. Scarratt and Jean-Guy J. Godin Department of Biology, Mount Allison University, Sackville, New Brunswick, Canada (Received 27 June 1991; revision received 8 November 1991; accepted 11 November 1991)
Abstract: The hermit crab Pagurus acadianus (Benedict) possesses two major defences against mobile aquatic predators, viz., fleeing and refuging in its gastropod shell. When approached by a potential predator, a crab must choose to either continue its current activity (e.g., feeding), flee or hide in its shell. If a foraging crab flees when threatened, it must secondarily decide whether to carry its food item and, if so, how far to carry it whilst escaping. Alternatively, if the crab takes refuge in its shell, it must then decide how long to remain hidden and when to resume locomotory activity following emergence from the shell. Because these behavioural alternatives have associated costs (e.g., energy expenditure, predation risk, lost foraging pportunity), the crabs' decision as to which behaviour to adopt should be sensitive to the respective cost of each. We tested specific predictions of this general economic hypothesis ofbehavioural decision making by varying the weight of food items presented to crabs ( = lost feeding opportunity cost, energetic cost of carry) and the amount of time the crabs were "handled" by a predator following "capture" (-- predation risk). Most crabs tested fled from an approaching lobster predator model. Contrary to expectation, flight initiation distance was unaffected by the mass ofthe food item available to the foraging crabs. As predicted, however, the distances fleeing crabs carried individual food items varied inversely with the food's weight. Time spent hiding in the shell and latency to resume locomotion following a predator"attack" were relatively unaffected by the size of the food item available. As expected, the crabs' decision to emerge from their shell following a threat appeared sensitive to their perceived risk of predation, as evidenced by an observed positive relationship between refuging time (in shell) and the duration of preceding handling of the crab by the predator. These findings are interpreted within the cost-benefit framework of behavioural decision making. Key words: Antipredation; Crab; Decision making; Foraging; Predation risk; Trade-off
INTRODUCTION
Animals have evolved diverse behavioural responses to predators and show considerable flexibility in these responses over their lifetime (e.g., Ydenberg & Dill, 1986; Sih, 1987; Lima & Dill, 1990). Such responses include fleeing, hiding in a physical refuge, joining a social group or mobbing when a potential predator has been detected. Although an animal may reduce its risk of predation by actively fleeing from a predator and (or) by hiding in a refuge, it may incur potential costs, such as lost foraging opportunities, in doing so (Ydenberg & Dill, 1986; Sih, 1987). Because the cost of Correspondence address: J.-G.J. Godin, Department of Biology, Mount Allison University, Sackville, New Brunswick E0A 3C0, Canada.
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foraging under predation hazard may be death (Godin & Smith, 1988), prey animals are expected to trade off foraging gains and risk of mortality from predation in choosing the behavioural alternative which maximizes fitness (reviewed by Milinski, 1986; Dill, 1987; Godin, 1990; Lima & Dill, 1990). A foraging individual should thus delay its antipredator response to an approaching predator when expected fitness benefits from continued foraging exceed the costs of delaying (Ydenberg & Dill, 1986; Dill & Ydenberg, 1987; Dill & Houtman, 1989). Moreover, the type and intensity of the antipredator response exhibited should be sensitive to its costs and to the current threat of predation, as assessed by the prey (Sih, 1987; Helfman, 1989; Lima & Dill, 1990). Here we investigate, within the framework of the above general economic (costbenefit) hypotheses, foraging and antipredator decisions in hermit crabs Pagurus acadianus (Benedict) exposed to a simulated threat of predation from a lobster model. P. acadianus typically inhabits the boreal marine sublittoral zone (Logan et al., 19,~,), where it is exposed to predators such as lobsters Homarus americanus (Logan ~t al., 1983; Elner & Campbell, 1987). Unlike most adult decapod crustaceans, the abdomen of hermit crabs is not covered by a hard carapace. Instead, they occupy empty gastropod shells, which provide protection against physical abrasion and predators (Reese, 1969; Hazlett, 1981; Lancaster, 1988); almost all known species are mobile while occupying such shells (Hazlett, 1981). Hermit crabs are in general omnivorous detdtivores (Reese, 1969). To forage effectively, the crab must extend its cephalothorax and legs out of the shell aperture. However, this also exposes it to predators. When confronted by an approaching aquatic predator, P. acadianus typically exhibits one of two antipredator responses. The crab may either rapidly move "away from an attacking predator (= flight) or remain stationary and withdraw into its shell ( = refuging), leaving only the tips of its chelae exposed (pers. obs.). However, a fleeing or refuging crab cannot forage, and thereby potentially incurs a cost of lost foraging opportunity. Because foraging and antipredator behaviours (i.e., fleeing, hiding in shell) appear to be mutually exclusive activities in hermit crabs, they are thus ideal subjects for investigating behavioural decisions (sensu Dill, 1987) made when foraging and predator avoidance (or escape) conflict. Decision making in this context has not been previously studied in hermit crabs, although other behavioural decisions have been addressed (e.g., Elwood & Stewart, 1985; Hazlett, 1987; Jackson & Elwood, 1990). In the current study, individual hermit crabs were initially given a choice between remaining stationary, and continuing to feed on a food item of standardized mass, and escape from an approaching potential predator (a lobster model) in the laboratory. We predicted that foraging crabs would delay their flight from the "attacking" predator longer to continue foraging, and thus show shorter flight initiation distances, with increasing mass ( = potential energetic value) of the food item available to them, thus reflecting a trade off between predation risk and immediate foraging gains. Secondly, we predicted that both the likelihood of a food item being carried and the distance carried would decrease with increasing mass of the food item, presumably owing to increased energetic cost of transport and predation risk (through reduced escape speed
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and increased conspicuousness). Finally, at some point along its attack path, the predator model eventually came into contact with the crab. Physical contact between predator and prey was maintained for different standardized periods of time, thereby simulating different predator "handling times" and thus different apparent risk of mortality to predation. We also predicted that, if hermit crabs are sensitive to variations in predation risk (cf. Helfman, 1989), they ought to remain hidden in their shell and delay resuming locomotion longer when predation risk is perceived to be greater, but at an increasing cost of lost opportunity to forage.
MATERIALS AND METHODS ANIMALS AND HOLDING CONDITIONS
Hermit crabs were collected subtidally by scuba diving in Passamaquoddy Bay, near the Huntsman Marine Science Centre, St Andrews, New Brunswick, Canada (45 ° 05' N, 67 ° 04'W), between May and October 1989. The crabs were transported to Mount Allison University, where they were held in plastic tanks supplied with running seawater (13.7 + 0.3 °C) and exposed to a 12 L" 12 D illumination regime. Empty gastropod shells were placed in the tanks, so that the crabs could change their shell if necessary. Crabs were fed ad libitum a mixed diet of frozen haddock Melanogrammus aeglefinus and a specialized crustacean food (Halifax Standard Reference Diet No. 84; Fisheries and Oceans Canada) thrice weekly. The experimental crabs weighed on average 1.52 g (SE = 0.04, range = 0.48-2.96, n = 159) and carried a gastropod shell weighing 3.25 g (SE -- 0.06, range -- 1.63-6.41). Crabs primarily occupied Littorina littorea (66.7 ~o)or Nucella lapillus (25.2~o) shells at the time they were tested. The particular gastropod shell species occupied by the crabs had no consistent effect on their antipredator behaviours in this study. A crab's sex could only be determined with certainty by removing it from its shell at the end of an experimental trial. Most (67.9~o) of our crabs were females. Since the behaviours recorded in this study did not differ between the sexes, the data were pooled over both sexes for analysis. HERMIT CRAB-LIVE LOBSTER INTERACTIONS
Observations were made on the behaviour of hermit crabs in the presence of a live lobster to ascertain the types of antipredator responses exhibited towards this predator, and to confirm whether these responses were qualitatively similar to those exhibited towards a realistic lobster model used in this study. Interactions between a live lobster (major chela = 9 x 5 cm; L x W), previously deprived of food for 48 h, and four to six hermit crabs in a rectangular seawater tank (90 x 60 x 28 cm) were recorded over 3 consecutive days (total = 24 h observations) using an overhead video camera under dim red light. Crabs were not provided with any food in these trials. Frequencies of lobster
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A N D J.-G.J. G O D I N
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CRAB-LOBSTER
MODEL
INTERACTIONS
Experimental tank Behavioural responses of hermit crabs toward~ a lobster model (see below) were observed in two identical Plexiglas tanks (92 x 20 x 25 cm; Fig. 1), each supplied with recirculating (,~ 1 1. rain - ~) filtered seawater maimained at 10.5 + 0.3 ° C and exposed to a 12 L ' 12 D illumination regime (fluorescent light intensity -- 100 Ix at the surface).
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The bottom and three sides of each tank were covered externally with light blue cardboard, partly to reduce external disturbance. To facilitate distance measurements, the cardboard on the back wall and bottom of each tank were demarcated at 5-cm intervals with marker lines. A shaded hide (25.5 x 20 x 25 cm) to conceal the predator model was constructed at the water inlet end of the tank by placing a styrofoam root" over the area, covering the walls with black polyethylene plastic and dropping a black plastic curtain half way down the water column at the entrance to the hide (Fig. 1). A circular clear Plexiglas cylinder (15 cm diameter), used to restrain individual crabs before the onset of an experimental trial, was placed 45 cm away from the entrance to the predator's hide (Fig. 1). The cylinder could be raised remotely with the aid of a pulley system, thereby allowing the crab to move freely within the tank. Both ~anks were located behind a blind to minimize external disturbance of the animals. Behavioural observations were made through two small horizontal windows, covered with black fibreglass netting, in the blind.
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Predator model Two identical predator models were constructed from molded plastic lobsters. The model's chelae (9 x 4.5 cm; L x W) were fully extended anteriorly and horizontally. The models were painted with acrylics to resemble a live lobster, covered with a thin coat offibreglass resin and mounted on a right-angle shaped, clear glass rod (for manual presentation). Prior to introducing a hermit crab into the experimental tank, the predator model was hidden in the darkened hide, where it remai~ecl Stationary on the bottom with the attached glass rod protruding through a slit in the hide's roof and above the observation blind (Fig. 1). This apparatus allowed an observer, located behind the blind, to manually advance the model out of cover and along the bottom towards the crab at the other end of the tank.
Experimental protocol Prior to being introduced into the experimental tank, hermit crabs were deprived of food for 48 h to standardize hunger levels. Crabs were placed individually into the restraining cylinder in the experimental tank and allowed to acclimatize for at least 2 h before being provided with a piece of haddock, of a predetermined standard weight (see below), as food. This food item was gendy dropped into the cylinder with the aid of a transparent plastic scoop attached to a glass rod. This food-provisioning procedure did not appear to disturb the crab. Four weight classes of food items were used, viz., 80-120, 180-220, 280-320 and 380-420 mg wet wt. For simplicity, these size classes will hereafter be referred to as the 100, 200, 300 and 400-mg food items. All but the smallest of these food items exceeded the amount of haddock (160 + 25 mg) a crab could consume over a relatively prolonged time period (8 h). If the test crab did not start feeding within 5 rain of food presentation, the trial was discontinued. Most crabs, however, began feeding within 1 min of food presentation. The test crab was allowed to feed for 20-25 s whilst the restraining cylinder was gently raised out of the tank. Raising the cylinder did not interrupt foraging. Over this latter period, our crabs could consume on average 2.6 + 0.5 mg of haddock, representing 1.6% of their satiation ration. We assumed that this feeding period was sufficient for the test crab to assess the size, and perhaps the potential energetic value, of the fiaod item presented without significantly altering its hunger level. After raising the restraining cylinder, the foraging crab was "attacked" by manually advancing the lobster model from the hide towards it at a standard speed of 8 + 0.5 cm s - ' We recorded: ''~ whether the crab subsequently fled or remained stationary in response to th,e approaching predator; and (ii) the distance the fleeing crab carried the food !,~em before dropping it. The distance separating predator model and crab at the instant the latter initiated flight was also recorded and is referred to as "flight initiation distance". Although most simulated attacks were initiated when the test crab was facing (0 _ 45 °) the approaching lobster model, a crab would sometimes rotate slightly just as the model began its "attack". We therefore categorized (in 45 ° sectors) _
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A.M. SCARRATT AND J.-G.J. GODIN
the orientation of the crab's shell aperture relative to the model's attack path, because the crab's orientation may determine the likelihood of visual predator detection and thus of flight initiation. In all trials, the attacking predator model eventually intercepted the fleeing or stationary crab, which immediately withdrew into its shell. Since hermit crabs are sensitive to external mechanical stimuli received through their shell (l-Iazlett, 1987), we attempted to simulate differential risk of predation by varying the amount of time the predator model "handled" the "captured" crab. "Handling" consisted of lightly, but continuously, contacting the crab with the tips of the model's chelae. Each test crab was exposed to one of four predetermined "predator handling times", viz., 0, 10, 20 or 30 s. We assumed that the longer a predator persists at handling a crab, the greater the risk of mortality the latter incurs. At the end of this handling period, the lobster model was removed from the tank. We then recorded the time the crab spent hiding in its shell, which is referred to as "hiding time" (does not include the preceding predator handling time). The latter ended when the crab's eye stalks were extended beyond the rim of the shell's aperture. The time elapsed between crab emergence from the shell and its resumption of locomotion was defined as "time to resume locomotion". The experimental design therefore consisted of four different food treatments ( = different sized food items) and four predation hazard treatments (= different predator handling times). Each combination of food and predation hazard treatments was randomly predetermined and replicated with at least 10 different crabs (except for four combinations, due to the unavailability of naive animals). No crab was used more than once in this study. CONTROLS FOR PREDATOR MODEL
Control trials were carried out to ascertain whether the observed crab antipredator responses towards the lobster model were due to the threatening nature of the model or simply to novelty or disturbance associated with its presentation. Individual crabs were exposed to the mov'ng glass rod only in one series of trials (n -- 5) and to a green sponge (area presented = 8 x 5 cm), attached to the end of the glass rod, in a second series 01 = 5). These control trials were carried out in a similar manner to the ones described above, except that the crabs were not handled by the rod or sponge here. Crab behaviours in these control trials were recorded as described above, and compared with the behaviours of crabs (n = 10) which were approached (but not handled) by the lobster model. Crabs in these trials had access to a 100-mg food item. DATA ANALYSIS
Data were normalized by log transformation prior to statistical analysis. Significance of treatment effects were tested using the two-way ANOVA and ANCOVA as appropriate. Mean scores were compared with the Tukey-Kramer test for multiple comparisons or the t test for paired comparisons as appropriate. The level of statistical
BEHAVIOURAL D E C I S I O N S IN T H R E A T E N E D H E R M I T CRABS
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significance was set at P < 0.05. All tests used are one-tailed and are described in Sokal & Rohlf (1981).
RESULTS INTERACTIONS WITH LIVE LOBSTER
A total of I 18 unambiguousattacks by the live lobster on hermit crabs were observed. Most (86.4 9o) of the attacks resulted in the crab fleeing from the approaching lobster. Flight was simply a rapid movement away from the lobster. Fleeing resulted in successful escape from the predator ,,,;-a~_,.,.! Or/oof all interactions, whereas the lobster overtook and came into physical contact with the fleeing crab on the remainder (54.9~o) of the interactions. Such "captured" (and handled) crabs immediately withdrew into their shell, and in only 10.79/0 of these captures was the shell crushed and occupant killed by the lobster. In a minority at attacks (13.69o), the crabs did not flee from the approaching lobster, but alternatively remained stationary and withdrew into their shell. On 43.79/0 of these attacks, the lobster captured the stationary crab which subsequently withdrew into its shell. Only 14.3 ~o of these crabs were killed. Therefore, hermit crabs exhibited two antipredator responses to an approaching predatory lobster, fleeing and hiding within their shell. INTERACTIONS WITH LOBSTER M O D E L
The antipredator responses exhibited by hermit crabs towards the approaching lobster model were qualitatively similar to those shown towards a live lobster (described above).
Fleeing Most test crabs (157 out of 159) fled from the approaching lobster model. Their overall mean + SE flight initiation distance was 8.8 + 0.5 cm. Since the distance at which individual crabs initiated their escape was negatively correlated (Spearman's rank correlation; rs = -0.26, t = 3.36, df = 157, P < 0.001) with the orientation of their shell's aperture relative to the predator's attack path, it was necessary to adjust fligh' initiation distance for the orientation covariate using the ANCOVA prior to testing for a treatment effect of food item size. When so adjusted, crab flight initiation distance was not significantly affected by the mass of the food item on which they were feeding ( A N C O V A ; F3.15 4 = 2.18, P > 0.05). Therefore, for a given body orientation, foraging crabs did not progressively delay their flight, and thereby exhibit shorter flight initiation distances, with increasing weight of the food item available within the range used.
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Carrying food Most (98.7 ~o) fleeing crabs carried the food item in their chelae during escape from the approaching predator model. Therefore, no relationship existed between the likelihood of a fleeing crab carrying a food item and the mass of the latter. The food item was eventually dropped by the crab at some distance along its escape path. Larger food items tended to be dropped sooner than smaller food items, as indicated by the observed (and predicted) negative relationship between the mass of the food item and the distance it was carried (linear regression; F~,~57 = 6.60, r = -0.20, P < 0.02; Fig. 2).
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41
40
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2
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100
200
300
400
Food item size (mg) Fig. 2. Relationship between mass of the food item on which individual hermit crabs were feeding when attack.d by a lobster model and mean + SE distance they carried the food item whilst fleeing. Numbers above bars denote sample size. Line-of-best-fit was obtained by least-squares linear regression.
Hiding #~ shell The time withdrawn crabs spent hiding in their shell was not affected (two-way ANOVA; F3.~43 --- 1.69, P > 0.15) by the mass of the food item it was feeding on prior to the predator's attack, but was by how long the crabs were previously handled by the p r e d a t o r (F3,14 3 -- 12.93, P < 0.001); there was no statistical interaction between these two treatments (F9,143 = 1.15, P > 0.30). However, the expected inverse relationship between crab hiding time and food item weight (i.e., expected lost foraging gains) may have been masked by the fact that smaller food items tended to be located closer to the hiding crab, and thus were perhaps less costly to retrieve, than the larger items in our study, as noted above. Even when statistically controlled for the distance the fleeing crab carried a food item before retreating in its shell, its hiding time remained unaffected by food mass (ANCOVA; F3.~54 = !.27, P > 0.25). Hiding time thus appears to have been determined mainly by the crab's cor.finu;Jus assessment of its risk of predation, which is assumed here to be positively corre!ated with predator handling time. As expected, when statistically contrglled for both the
BEHAVIOURAL DECISIONS IN THREATENED HERMIT CRABS
233
distance and size of the food item carried during flight, the time individual crabs spent hiding in their shell increased with increasing duration of the period they were handled by the predator model (ANCOVA; F3.1s3 = 1339, P < 0.001; Fig. 3). Therefore, the longer a crab was handled by a potential predmor, the more reluctant it was to emerge from its shell, regardless of potential foraging gains.
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Predator handlingtime (s) Fig. 3. Relationship between time crabs were "handled" by predator and mean + SE time they subsequently spent hiding in their shell. Different letters above bars denote significant differences (P < 0.05) among means (Tukey-Kramer multiple-means comparison test). Numbers above bars represent sample, size.
Resumption of locomotion after an attack Following emergence from its shell, a previously refuging crab must resume its locomotory activity if it is to locate food, but presumably at the cost of increased exposure to predators. The crabs' latency time to resume locomotion following emergence from their shell was influenced by the mass of the food item on which they h..' been feeding (two-way ANOVA; F3.~43 = 4.79, P < 0.005), but was not affected by the time they had been previously handled by the predator (Fa.143 = 1.56, P > 0.20); there was no statistical interaction between these two treatments (F9.~43 = 1.35, P > 0.20). The significant foodosize treatment effect persisted (F3.1s3 - 4.83, P < 0.005) when the latency data were subjected to an ANCOVA, which statistically controlled for both the varying distance of the food item from the emerging crab and the time it had previously been handled by the predator. However, the expected negative relationship between latency time to resume locomotion and food item mass was not apparent (Fig. 4). With the exception efthe 300-rag class, variation in the weight of the food items available had relatively little effect on the crabs' latency time to resume locomotion.
234
A.M. SCARRATT A N D J.-G.J. G O D I N
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Food item weight (mg) Fig. 4. Relationship between mass of food item on which individual hermit crabs were feeding when "attacked" by a lobster model and their subsequent mean + SE latency time to resume locomotion following emergence from their shell. Other details are as in Fig. 3.
CONTROLS FOR PREDATOR MODEL
Hermit crabs behaved differently towards the realistic lobster model than to either the glass rod only or the rod with a sponge attached. First, none of the crabs tested stopped feeding to flee from the approaching rod. In comparison, the crabs fled from both the approaching sponge and the lobster model, but their mean + SE flight initiation distance for the sponge (5.8 + 1.2 cm) was significantly shorter (t = 2.36, d f - 13, P < 0.05) than that for the lobster model (12.7 + 1.2 cm). Secovdly, the crabs did not hide in their shell when "attacked" by either the rod or the sponge, but did in response to the approaching lobster model and remained hidden for 3.1 + 1.6 s on average. Lastly, following the removal of the "attacking" object, the crabs took significantly longer on average (t = 3.55, df - 13, P < 0.01) to resume locomotion when they had just previously been "attacked" by the lobster model (12.5 + 1.3 s) compared to the sponge (1.4 + 1.5 s). They did not stop moving about in response to the approaching rod. These observations strongly indicate that the hermit crabs were able to discriminate between the three different objects presented and apparently assessed the lobster model as the most threatening. Therefore, we conclude that the behaviour of hermit crabs observed in this study were elicited specifically in response to a lobster model and not simply to the novelty or disturbance associated with the presentation of this model. DISCUSSION The hermit crab P. acadianus possesses two major defences against mobile aquatic predators, viz.: fleeing and refuging in i.ts .3hell. Because antipredator behaviours have associated costs such as lost opportunities to forage and increased energy expenditure,
BEHAVIOURAL DECISIONS IN THREATENED HERMIT CRABS
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individual crabs ought to be sensitive to variations in these costs and the current risk of predation when making foraging and antipredator decisions (cf., Ydenberg & Dill, 1986; Dill, 1987; Abrahams & Dill, 1989; Hdfman, 1989; Lima & Dill, 1990). In the current study, hermit crabs responded to the simulated threat of predation from a lobster model in ways which are, for the most part, consistent with this general economic hypothesis. All hermit crabs (except two) fled in response to the approaching lobster model. However, contrary to the prediction of Ydenberg & Dill's (1986) economic model of escape from predators, crab flight initiation distance (FID) did not decrease progressively with an increase in the mass of the food item available (i.e., increasing potential cost of lost foraging opportunity due to flight). Therefore, it would appear that the timing of escape from an approaching predatory threat, and thus FID, in this hermit crab species is not sensitive to the potential lost opportunity cost of flight. In comparison, FID has previously been shown to be sensitive to variations in the costs of flight and the risk of mortality to predation in other animals (e.g., Dill & Ydenberg, 1987; Dill & Houtman, 1989; Dill, 1990). Perhaps animals which possess morphological defenses, such as shells in crabs and spines i, fishes (McLean & Godin, 1989), can afford to be relatively insensitive to varying risk of predation and lost opportunity costs of escape and thus to defer their flight until capture by a predator is imminent. Alternatively, our crabs may have assessed the different weights of food items presented as being of equal value, and thus initiated their flight at a similar distance from the predator, regardless of the mass of the food item on which they were feeding when "attacked". Animals (such as the hermit crabs in the current study) which forage on relatively large food items that cannot be consumed wholly and quickly may either: (i)escape without the food item; (ii) escape and carr~~the food item with them; or (iii) remain with the food and defend themselves when threatened by a predator (Formanowicz & Brodie, 1988). These behavioural option,~ have different benefits (expected energetic gains from the food) and costs (energetic cost of escape, risk of predation). Therefore, the forager should carry a food item whilst escaping only when the costs of carrying do not exceed the costs of interrupting feeding and lost foraging gains (Ydenberg & Dill, 1986; Formanowicz & Brodie, 1988). In the curren ~ study, all foraging hermit crabs (except two) carried the food item while fleeing from an approaching predator, regardless of the weight of the food item. Therefore, their decision to carry or abandon a food item at the instant of flight initiation was unaffected by the food item's weight (at least within the range of weights tested here). In contrast, ~orat~mg " " ..... ~-~" Procambarus clarkii (Bellman & Krasne, 1983) and fiddler crabs Uca panacea (Formanowicz & uu items Brodie, 1988) faced with a predator)' threat are: more likely to carry sm,m - - " ~t, c^^.~ than large ones when escaping. These different results may reflect differences between the studies in the relative size of food items used. On average, the weights of the food items presented to crayfish (Bellman & Krasne, 1983) and fiddler crabs (Formanowicz & Brodie, 1988) represented 30-300 and 19-128Y/o, respectively, of their live body weights, compared with 6-26°/o for hermit crabs in the current study.
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However, we further noted an inverse relationship between the weight of a food item and the distance it was carried by a fleeing hermit crab, before it was abandoned. We offer two possible explanations for this novel finding. First, hermit crabs may have assessed the relative benefits and costs of carrying or abandoning a food item during the course of their flight from the predator, but not before. Because predation risk (through decreased escape speed and increased conspicuousness) and energy expenditure likely increase in escaping crabs with increasing amount of weight carried (Formanowicz & Brodie, 1988), the costs of carrying a food item may exceed expected benefits (future foraging gains) sooner for larger food items than smaller ones. Therefore, a fleeing forager ought to carry a large food item over a shorter distance than a smaller one before dropping it, thereby trading off expected foraging gains and risk of mortality to predation. Our results are consistent with such an economic hypothesis. Alternatively, larger food items may have been more readily stripped from the fleeing crab's chela by drag forces, and consequently were carried shorter distances, than smaller items. Further experimentation is required to determine which mechanism is more plausible. Once "captured" by the lobster model, a fleeing crab typically withdrew within its shell. In doing so, the crab minimized its risk of predation but at the cost of lost energetic gains from foraging. Therefore, if hermit crabs are sensitive to variations in this cost, then their hiding time should be inversely related to the weight of the food item (i.e., expected future energetic gains) on which they were feeding prior to the predator's attack. We did not observe such a monotonic relationship, suggesting that the crabs' decision to emerge from their shell, at the cost of increased predation risk, is not based simply on their expected energetic gains from foraging in the immediate future. Greater risk taking in individuals with expectations of immediate or greater food rewards has been demonstrated in other species (e.g., Fraser & Huntingford, 1986; Godin & Smith, 1988; Godin & Sproul, 1988; Dill et al., 1990). However, since lobsters can also scavenge (cf., Elner & Campbell, 1987, pers. obs.), and may feed on any food dropped by fleeing prey, the presence nearby of a previously-dropped food item may be very uncertain to a refuging crab. This uncertainty may render the mass of such a food item an unreliable indicator of potential future r~wards and thus for basing decisions on when to emerge from hiding. Notwithstanding the potential effects of foraging opportunities, threatened hermit crabs may also have been sensitive to var.~ation in (apparent) predation risk in deciding when to emerge from their shell. As predicted, the time individual crabs spent hiding in their shell increased with increasing predator handling time, a presumed correlate of predation risk. This observed relationship suggests that this crab's shell refuging behaviour is ~hreat sensitive (sensu Helfinan, 1989). While hiding in its shell, a crab presumably cannot see its predator but may be able to smell it. Because a model predator was used in this study, predator olfactory cues were absent. Therefore, in the absence of visual and olfactory cues about the presence of the predator, a hiding hermit crab may alternatively be able to use mechanical stimuli transmitted through its shell, while being
BEHAVIOURAL DECISIONS IN THREATENED HERMIT CRABS
237
handled by the predator, to assess its current risk of predation. Our results support the notion that the crabs used the duration of the predator handling period as an indicator of the current risk of predation when deciding to emerge from their shell. Upon emerging from its shell following a threat of predation, a crab must then decide when to resume locomotory activity, perhaps in search of food. Such activity also has associated costs, in terms of energy expenditure and increased predation risk, and benefits, such as increased probability of encountering food. It would thus be prudent for the animal to delay movement if the predator is ~till nearby, which could be assessed visually or olfactorily. If it is not (as was the case in our study), then the decision to resume movement may be dependent on the crab's hunger level and (or) the expected value of a future food reward, which could be reinforced by chemical cues from the food item (cf., Hazlett, 1971). The expected inverse relationship between latency time to resume locomotion and food item mass was not observed in the current study. This could mean that the crabs do not use the assessed'quality of a resource ( = mass of a food item) to decide when to resume locomotion following a threat of predation, as they do when deciding to resume shell investigative behaviour following a startle stimulus based on the quality of another resource, the shell under investigation (Jackson & Elwood, 1990). Alternatively, as suggested above, the absence of the aforementioned expected relationship may have been due to the crabs having valued equally the different food sizes available in the current study, all of which could have exceeded a certain threshold mass above which food items are categorized similarly as high quality. Varying hunger level is unlikely to be important in our study since it was standardized among the experimental animals. In general, the results of this study support the hypothesis that hermit crabs are able to assess their current risk of predation and the costs of predator avoidance (or escape) in making a number of foraging and antipredator decisions. ..
ACKNOWLEDGEM ENTS
We gratefully acknowledge the assistance of R. W. Rangeley in the collection of crabs in the field, S. Davis in setting up the experimental apparatus, and D.J. Scarratt in providing the prepared crustacean food. The Huntsman Marine Science Centre provided diving and temporary animal holding facilities. We also thank R. Aiken, L.A. Dugatkin, R. W. Elwood, V. Gotceitas, R. W. Rangeley and two anonymous referees for their helpful comments on earlier versions of the paper. This study was supported by grants to J.-G.J. Godin from NSERC Canada and Employment & Immigration Canada's Challenge '89 summer program.
REFERENCES Abrahams, M.V. & L.M. Dill, 1989. A determination of the energetic equivalence of the risk of predation. Ecology, Voi. 70, pp. 999-1007.
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Bellman, K.L. & F.B. Krasne, 1983. Adaptive complexity of interactions between feeding and escape in crayfish. Science, Vol. 221, pp. 779-781. Dill, L. M., 1987. Animal decision making and its ecological consequences: the future of aquatic ecology and behaviour. Can. J. ZooL, Vol. 65, pp. 803-811. Dill, L.M., 1990. Distance-to-cover and the escape decisions of an African cichlid fish, Melanochromis chipokae. Environ. Biol. Fish., Vol. 27, pp. 147-152. Dill, L.M., A. H.G. Fraser & B.D. Roitberg, 1990. The economics of escape behaviour in the pea aphid, Acyrthosiphon pisum. Oecologia, Vol. 83, pp. 473-478. Dill, L.M. & R. Houtman, 1989. The influence ofdistance to refuge on flight initiation distance in the gray squirrel (Sciurus carofinensis). Can. J. Zool., Vol. 67, pp. 233-235. Dill, L.M. & R.C. Ydenberg, 1987. The group size-flight distance relationship in water striders (Gerris remigis). Can. J. Zool., Vol. 65, pp. 223-226. Elner, R.W. & A. Campbell, 1987. Natural diets of lobster Homarus americanus from barren ground and macroalgal habitats off southwestern Nova Scotia, Canada. Mar. Ecol. Prog. Ser., Vol. 37, pp. 131-140. EIwood, R.W. & A. Stewart, 1985. The timing of decisions duri" ~ shell investigation by the hermit crab, Pagurus benahardus. Anita. Behav., Voi. 33, pp. 620-627. Formanowicz, D. R., Jr. & E.D. Brodie, Jr., 1988. Predation risk and forager escape tactics. Anim. Behav., Vol. 36, pp. 1836-1838. Fraser, D.F. & F.A. Huntingford, 1986. Feeding and avoiding predation hazard: the behavioral response of the prey. Ethology, Vol. 73, pp. 56-68. Godin, J.-G. J., 1990. Diet selection under the risk of predation. In, Behavioural mechanisms offood selection, edited by R.N. Hughes, NATO ASI Ser., Vol. G20, Springer-Verlag, Berlin, pp. 739-769. Godin, J.-G.J. & S.A. Smith, 1988 A fitness cost of foraging in the guppy. Nature, Vol. 333, pp. 69-71. Godin, J.-G.J. & C.D. Sproul, 1988. Risk taking in parasitized sticklebacks under threat of predation: effects of energetic need and food availability. Can. J. Zoo'., Vol. 66, pp. 2360-2367. Hazlett: B.A., 1971. Chemical and chemotactic stimulation of feeding behavior in the hermit crab Petrochirus diogenes. Comp. Biochem. Physiol., Vol. 39A, pp. 665-670. Hazlett, B.A., 1981. The behavioral ecology of hermit crabs. Annu. Rev. Ecol. Syst., Vol. 12, pp. 1-22. Hazlett, B.A., 1987. Information transfer during shell exchange in the hermit crab Ciibanarius antiilensis. An#t, Behav., Vol. 35, pp. 218-226. Helfman, G.S., 1989. Threat-sensitive predator-avoidance in damselfish-trumpetfish interactions. Behav. Ecol. Sociobiol., Vol. 24, pp. 47-58. Jackson, N.W. & R.W. Elwood, 1990. Interrupting an assessment process to probe changes in the motivational state. Anita. Behav., Vol. 39, pp, 1068-1077. Lancaster, i., 1988. Pagurus benzhardus ( L . ) u an introduction to the natural history of hermit crabs. Field Stud,, Vol. 7, pp. 189-238. Lima° S.L. & L.M. Dill, 1990. Behavioral decisions made under the risk of predation: a review and prospectus. Cat,, J. ZooL, Vol. 68, pp. 619-640. Logan, A., A. A, Mackay & J. P. A. Noble, 1983. Sublittoral hard substrates. In, Marine and coastal systems of the Quoddy region, New Brunswick, edited by M. L. H. Thomas, Can. Spec. Publ. Fish. Aquat. Sci., Vol. 54, pp. 119-139. McLean, E.B. & J.-G.J. Godin, 1989. Distance to cover and fleeing from predators in fish with different • amounts of defensive armour. Oikos, Vol. 55, pp. 281-290. Milinski, M., 1986. Constraints placed by predators on feeding behaviour. In, The behaviour of teleostfishes, edited by T.J. Pitcher, Croom Helm~ ~ ondon, pp. 236-252. Reese, E.S., 1969. Behavioral adaptations of intertidal hermit crabs. Am. Zool., Vol. 9, pp. 343-355. Sih, A., 1987. Predators and prey lifestyles: an evolutionary and ecological overview. In, Predation: direct and indirect impacts on aquatic communities, edited by W.C. Kerfoot & A. Sih, University Press of New England, Hanover, pp. 203-224. Sokal, R.R. & F.J. Rohlf, 198l. Biometry. W.II. F~ce,',a~ & Co., New Y~z~%second ,u~uu,,~'~:':^-859 pp. Ydenberg, R.C. & L.M. Diq, 1986. The economics of fleeing from predators. Adv. Study Behav., Vol. 16, pp. 229-249.