Behavioral Ecology Advance Access published online on July 22, 2008
Behavioral Ecology, doi:10.1093/beheco/arn077
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Effects of autotomy and regeneration on detection and capture of prey in a generalist predator
Department of Biology, University of Cincinnati, PO Box 210006, Cincinnati, OH 45221, USA
Address correspondence to K.M. Wrinn, who is now at the Department of Zoology, Miami University, Oxford, OH 45056, USA. E-mail: wrinnkm{at}muohio.edu.
Received 2 February 2008; revised 17 June 2008; accepted 18 June 2008.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Many vertebrate and invertebrate taxa have the ability to autotomize and later regenerate appendages and with this process come both costs and benefits. For example, an animal might lose a leg to avoid a predator but as a result become a less effective predator itself. These impacts of autotomy and regeneration on foraging might differ based on habitat complexity as well. We used spiders as a model system to address this. We tested the effects of autotomy and regeneration on prey capture in juvenile Schizocosa ocreata wolf spiders in both artificial and seminatural settings. We tested spiders for prey capture efficiency in a laboratory arena with cricket prey. We also investigated sensory detection of prey through vibration by placing spiders in the same type of arena but visually isolating them from their prey. Subsequent analyses showed no effects of autotomy or regeneration on any measures of prey capture efficiency. Similarly, spiders’ vibratory sensory abilities were not significantly affected by autotomy or regeneration. However, we found that when spiders were tested in a seminatural habitat (a leaf litter–filled mesocosm), individuals with a missing or regenerating leg had reduced prey capture rates. This suggests that the negative effects of autotomy and regeneration on foraging might be higher for predators in more complex environments.
Key words: autotomy, prey capture, regeneration, wolf spiders.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Autotomy (self-amputation) of appendages and subsequent regeneration of the lost parts are common across many taxonomic groups including vertebrates (Dial and Fitzpatrick 1984
), echinoderms (Ramsey et al. 2001), crustaceans (Juanes and Smith 1995), and arachnids (Formanowicz 1990). Both these processes are presumed ancestral across the animal kingdom (Goss 1969); however, there must be a balance between the costs and benefits of autotomy and regeneration in order for them to be maintained within a taxon over evolutionary time. For example, the ability to autotomize an appendage when grasped by a predator might allow the animal to escape, providing a direct survival benefit (Formanowicz 1990; Klawinski and Formanowitz 1994; Punzo 1997; Wasson et al. 2002). However, loss of an appendage can impair foraging abilities (Vollrath 1990; Brock and Smith 1998; Ramsey et al. 2001), locomotion (Amaya et al. 2001), competitive abilities (Dodson and Beck 1993; Mariappan et al. 2000; Taylor and Jackson 2003), and mating (Bateman and Fleming 2005). Although regeneration of lost appendages might allow animals to negate some of the costs of autotomy, it can hinder growth and development (Goss 1969; Vitt et al. 1977; Juanes and Smith 1995; Wrinn and Uetz 2007). Additionally, a regenerated appendage can have reduced function, affecting competition (Brock and Smith 1998), mating (Uetz et al. 1996, Taylor et al. 2006), locomotion, and foraging (Brock and Smith 1998).
Autotomy is likely to have a major effect on fitness via reduction in foraging efficiency: Foraging can be linked to many of the other behaviors and life-history processes that are impacted by autotomy and regeneration. For example, an animal might allocate more energy to regrowing an appendage and less to body growth during regeneration (Fleming et al. 2007), and this could be exacerbated if the animal is not gaining enough nutrition because of reduced foraging. In addition to developmental trade-offs, impaired foraging might create behavioral trade-offs as well. If autotomy or regeneration reduces foraging success, this could be worse in complex habitats, where these individuals are more likely to spend time to avoid further predation attempts (Martin and Salvador 1992, 1993; Stoks 1999; Cooper 2003). Thus, the animal is faced with the choice of foraging where it is safe but prey is scarce or difficult to catch versus where predation risk is higher, but foraging is easier. In both the scenarios above, autotomy or regeneration through foraging can impact body size or condition, both of which ultimately can help determine fitness (Danielson-Francois et al. 2002). It is important to consider these sorts of trade-offs to understand the evolution and maintenance of these common processes.
Autotomy and regeneration have been widely studied in arthropods (for reviews, see Maginnis 2006; Fleming et al. 2007). These processes might be particularly important in spiders and other arachnids because they use their legs extensively for all aspects of prey capture, from sensory detection to physical restraint of prey. Sensory hairs (trichobothria) located on the legs are used to detect airborne vibrations, whereas lyriform organs, each made up of a series of flexible slits, detect substrate-borne vibrations. Lyriform organs on regenerated legs are sometimes malformed (Vollrath 1995), which could affect their function. Furthermore, in spiders, legs require multiple molts to regenerate and thus newly regenerated legs are undeveloped and smaller than normal. In many species, these undeveloped limbs are held rigidly away from the body and are thus nonfunctional (Vollrath 1990). If spiders missing or regenerating legs have a reduced ability to detect and restrain prey, foraging will likely be impaired.
Two previous laboratory studies have addressed the effects of autotomy on physical capture and restraint of prey during foraging in wolf spiders (Amaya et al. 2001; Brueseke et al. 2001). Neither study showed any reduction in overall prey capture in autotomized spiders. However, Brueseke et al. (2001) found that spiders with autotomized limbs tended to capture smaller crickets, indicating that prey size might be an important factor affecting the impacts of autotomy and regeneration on foraging. Additionally, these studies were conducted in a very simple habitat (a plastic container with filter paper). Prey capture can be more difficult for animals in a complex habitat (Rypstra et al. 2007), making any negative effects of autotomy on foraging more severe.
Both studies mentioned above used adult spiders. The ability to regenerate is lost in adult spiders of most species as they cease molting on maturity. Therefore, we used juvenile spiders in the present study to test for the impacts of regeneration as well as autotomy. We addressed how these processes impact foraging of spiders on different sized prey. Furthermore, we conducted foraging tests under both laboratory and simulated natural conditions. We used the wolf spider Schizocosa ocreata (Hentz), which readily autotomizes and regenerates legs (12–19% individuals—Wrinn and Uetz 2007). We addressed how autotomy and regeneration affect both the functional and sensory aspects of prey capture in S. ocreata.
Our objectives were 1) to determine the effects of autotomy and regeneration on the rate of capture (number of crickets captured/time) of different sized prey under simulated natural conditions, 2) to measure the effects of autotomy and regeneration on the capture efficiency (i.e., latencies to orient to, attack and subdue prey) of different sized prey under controlled laboratory conditions, and 3) to examine how autotomy and regeneration affect sensory perception (i.e., measures of accuracy of orientation). We predicted that intact spiders would 1) capture more crickets/time; 2) have decreased latencies to orient to, attack and subdue crickets; and 3) orient more often, more quickly and exhibit lower error in orientation than spiders with a missing or regenerated leg. Lastly, we predicted that these differences would be more acute when spiders were given larger prey.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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For the following experiments, we collected spiders from the forest floor leaf litter at the Cincinnati Nature Center, Rowe Woods, Clermont County, OH. Spiders were taken to the laboratory, and each was placed in an opaque 10-cm diameter plastic container with a clear lid. The spiders were provided with water ad libitum through a dental wick connected to a water dish below. We fed late juvenile/adult spiders 10-day-old crickets (Acheta domesticus) twice a week. For the duration of the experiments, spiders were maintained under controlled laboratory conditions including 65–80% relative humidity, room temperature (21–24 °C), and a light cycle of 13:11 h light:dark.
We captured adult females during June of 2003 and raised their offspring in the laboratory to produce individuals for experiments 1 and 2. We examined spiders daily for egg sac production and hatching. We took spiderlings for these 2 experiments randomly from a total of 11 egg sacs (each by a different female) to control for possible clutch effects. On hatching, we left spiderlings with the mother for 7–10 days during which they cling to the mother's abdomen. On dispersal from the mother, we placed spiderlings in separate 120-ml plastic cups and gave them water ad libitum through a damp dental wick placed in the container. We fed spiderlings 4–5 Collembolans twice per week until they reached their third molt. At that point, we fed them fruit flies (Drosophila melanogaster) or pinhead crickets (A. domesticus) twice per week. As spiders reached their fourth molt, we randomly assigned them to 2 experiments: 1) capture rate or 2) capture efficiency. At that time, we transferred spiders over to the larger containers (see METHODS above).
Ethical note
Both autotomy of a foreleg and live predation trials were necessary to perform the following experiments. We considered autotomy to be a natural process as 12–19% of individuals of this species in the field are captured with missing or regenerating legs (Wrinn and Uetz 2007). All autotomy was done in a humane fashion with attempts to minimize the stress on the animals. Furthermore, in live predation trials, we allowed spiders to forage on crickets which are their natural prey and what we generally feed laboratory spiders.
Experiment 1: effects of autotomy/regeneration on prey capture rate
We compared the capture rate of 2 prey sizes by intact spiders with that of individuals when missing a leg, early in regeneration and later in regeneration. Because cricket size can affect prey capture in autotomized individuals (Brueseke et al. 2001), we randomly assigned spiders to crickets equal to either 33% (medium prey) or 50% (large prey) of their body weight. We induced each experimental spider to autotomize one randomly chosen foreleg by restraining the femur with forceps. We chose the forelegs for autotomy as these are involved in prey capture (Rovner 1980) and are more frequently seen missing in the field (Wrinn and Uetz 2007). After autotomy, we allowed spiders 24 h to recover prior to a second trial (Brueseke et al. 2001). We then tested them a third and fourth time within 1 week of each consecutive molt (first and second regeneration) as these spiders required at least 2 molts for the regenerated leg to become full sized. A few spiders molted during a trial and we removed them from further analysis as this process can affect foraging behavior (Morse 2000). We tested a separate set of intact spiders in each time period to account for possible age or learning effects. Our final sample sizes were 15–20 spiders per group (sample sizes differed by group as some spiders were dropped from analysis due to molting during a trial or death before completing all 4 trials).
We fed each spider two 10-day-old crickets, 1 week before being run in trials to standardize hunger levels. For each trial, we placed a spider along with 5 crickets in a rectangular clear plastic container (32 x 17 x 9 cm) with 2–3 cm of leaf litter covering the bottom. This served as a mesocosm simulation of their natural habitat (Cady 1984). Preliminary experiments showed that prey capture rate was highest during the first day. Therefore, we checked boxes after 6 and 24 h had passed and recorded the number of crickets alive at each time period to get early and late comparisons of prey capture rates.
We used a repeated measures multiple analysis of variance (MANOVA) with cricket weight and manipulation (autotomy or not) as factors to analyze cricket consumption/time period for the 4 groups (intact spiders: medium and large prey and manipulated spiders: medium and large prey). We used the MANOVA because it does not assume equal variances between all repeated measurements (O'Brien and Kaiser 1985). This made it better suited to our experiment as it was unlikely that variances remained equal across all measurements for the current study. If significant factors were found in the initial repeated measures MANOVAs, we then ran 2-way analysis of variances (ANOVAs) with Bonferroni-adjusted 
levels for multiple tests to determine which time periods were significant for the other factors (Von Ende 2001). We conducted all data analyses for this and the following 2 studies using JMP version 4.0.2 software (SAS Institute Inc. 2000).
Experiment 2: effects of autotomy/regeneration on prey capture efficiency
We compared the capture efficiency of 3 prey sizes by intact spiders with that of individuals missing a leg early and later in regeneration. We tested each experimental spider 5 times (intact, 24 h postautotomy, 1 week postautotomy, and after the 2 molts needed for full regeneration). As cricket weight may affect prey capture in autotomized spiders (Brueseke et al. 2001), we randomly assigned spiders to 3 groups (n = 15–20), fed crickets 25% (small prey), 33% (medium prey), or 50% (large prey) of the spider's body weight. We tested a separate set of intact spiders for each cricket weight in each time period to account for possible age or learning effects. As in experiment 1, final sample sizes were 15–20 spiders per group.
During experimentation, we reduced the feeding schedules so each spider received only 2 crickets per week. We demonstrated in preliminary experiments that this was enough to maintain the spiders but kept them hungry enough to be more likely to feed during trials. We placed spiders in the experimental container 24 h prior to being run as preliminary experiments showed many of the spiders did not capture prey immediately when placed in the container without the acclimation period. For each trial, we restrained the spider under a vial in the center of a circular plastic testing arena (15 cm diameter x 6.5 cm high) with filter paper covering the bottom. The vial was opaque on the sides (so the spider was not distracted visually) but clear on the top (to reveal the direction the spider was facing). We changed the filter paper between trials and wiped the arena with cotton and 70% ethanol to remove any traces of chemical signals from the previous spider. For each trial, we introduced a cricket using a modified syringe via a hole in the side of the container behind the spider and approximately 4 cm above the bottom. When the cricket entered the arena, we released the spider and the trial began.
We recorded the spider/cricket interactions within the arenas from above using a Watec America Corporation WAT-902C video camera until the spider began to feed (or 10 min). We scored trials on playback for the following parameters: 1) latencies to orient to prey, 2) latencies to attack, 3) number of attacks necessary for capture, 4) whether capture was successful (y/n), and 5) time (s) to subdue prey. We scored latency to orientation as the time between when the spider was released and when it either turned or moved toward the cricket. If the spider's orientation and attack could be separated, we measured attack latency as the time between when the spider oriented to the cricket and when it initially lunged at and attempted to grab the prey. If the spider's orientation and attack could not be separated (e.g., if the cricket approached the spider from the front), then we scored attack latency as 0.5 s. We used this value as it was greater than 0 but less than the 1 s that was the smallest measurable difference between orientation and attack times. Sometimes spiders would require multiple attempts to capture the prey, so we recorded the number of attacks as well. We measured subdue time as the time between attack and when the spider successfully restrained the cricket.
We analyzed the nominal variable of prey capture success (+/–) by pairing trials (e.g., spiders [cricket weight medium]: trial 1 [intact] vs. trial 2 [autotomized]) and using McNemar's tests for paired sample data (Zar 1999). We used a natural log transformation on data for orient latency, attack latency, and subdue time to make them normal. For the reasons stated previously, we used separate repeated measures MANOVAs to analyze the 4 continuous parameters we measured (orient latency, attack latency, number attacks, subdue time) for each of the 6 groups (manipulated spiders: cricket weight—small, medium, large; intact spiders: cricket weight—small, medium, large).
Experiment 3: effects of autotomy/regeneration on ability to detect vibratory cues from prey
We compared the detection of prey via vibratory cues alone among individuals that were intact, missing a leg, early in regeneration or late in regeneration. We collected juvenile spiders (n = 160) in the field in fall 2004 and maintained them in the laboratory (see Methods above). We randomly assigned all spiders to 1 of 4 groups (n = 40/group) and allowed them to molt twice within the laboratory before being run in trials. To ensure that spiders in all groups were approximately the same age when they were run in experiments, we induced spiders to autotomize a foreleg at different time periods based on treatment. Thus, one group of spiders had a fully regenerated leg when they were run in trials, a second group had a partially regenerated leg, a third group was missing a leg, and the fourth group was intact, having been unmanipulated. We fed spiders 2 crickets (A. domesticus) 1 week before trials in order to standardize hunger levels.
For each trial, we placed the spider inside a 3.5-cm wide opaque circle of plastic in the center of a 15-cm diameter plastic arena with filter paper on the bottom (as in experiment 2). We then placed a cricket, also restrained by a 2-cm wide circle of plastic, on the filter paper at an approximately 90° angle to the spider. Thus, the spider and cricket could sense each other through vibrations in the substratum but were isolated visually. For spiders that had an autotomized or regenerated leg, we placed the cricket on the side where autotomy had occurred, whereas we randomly chose side placement for intact spiders. We weighted each spider prior to the trial and assigned it a cricket weighing approximately 50% of its weight. Preliminary trials showed that crickets of this weight, while still falling under the spider's normal prey size range, were more likely to be detected by the spider than smaller crickets. We taped each trial (duration: 5 min) from above using a Canon XL-1 digital video camera and later analyzed frame by frame for angle measurements using the program Image J (Wright Cell Imaging facility, Toronto Western Research Institute). We measured both the spider's time of initial orientation to the prey and the angle of orientation to the prey (Figure 1).
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We compared orientation with prey (+/–) between groups using a 4 x 2 chi-square contingency table. We conducted further analyses on the spiders that did orient. We used a Kruskal–Wallis test to compare error angle between treatments (Zar 1999
). Also we used a 4 x 2 chi-square contingency table to determine any differences between the numbers of spiders in each group that oriented in the correct direction. Finally, we natural log transformed for normality data for time to initial orientation and analyzed it using a 1-way ANOVA. If a spider did not orient, we used a maximum time of 300 s as their initial orientation. |
RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Experiment 1: effects of autotomy/regeneration on prey capture rate
We found that after 6 h manipulation (leg autotomy) itself did not significantly affect prey capture rate, although cricket weight and the cricket weight x manipulation interaction were significant (Table 1). After 24 h, manipulation, cricket weight, and the interaction between the 2 significantly impacted prey capture (Table 1). Manipulated spiders receiving medium-sized prey consumed significantly fewer crickets at the second trial (autotomy) but only after 24 h (Figure 2A,B; Table 1). For spiders receiving large prey, this reduction in capture rate by manipulated spiders was apparent at 6 h for both the second (autotomy) and third (partial regeneration) trials (Figure 2C). By 24 h, this difference was no longer significant for manipulated spiders after trial 2 (autotomy), although the trend for higher capture in intact spiders remained (Figure 2D; Table 1).
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Experiment 2: effects of autotomy/regeneration on prey capture efficiency
We dropped the group receiving large prey from analysis for all the following response variables except for orient latency as spiders in this group were often unresponsive, drastically reducing sample size (especially in the last 2 trials). According to the repeated measures MANOVAs, there were no effects of manipulation (autotomy vs. intact) on orient latency (F1,53 = 0.01, P = 0.92), attack latency (F1,38 = 0.06, P = 0.82), number of attacks (F1,36 = 0.08, P = 0.78), or latency to subdue a cricket (F1,25 = 0.00, P = 0.99). Likewise, McNemar tests for paired sample nominal scale data showed no significant differences in likelihood of prey capture between trials for either intact or autotomized spiders at any of the cricket weights (P > 0.10 for all). Cricket weight also had no effect on any of the measures of prey capture, and there were no significant manipulation x cricket weight interactions.
Experiment 3: effects of autotomy/regeneration on ability to detect vibratory cues from prey
We found that autotomy and regeneration did not significantly affect detection of vibration cues from prey. Treatment groups did not significantly differ in likelihood to orient (
, P = 0.62), or if the spiders did orient, there was no difference in likelihood of orienting correctly (
, P = 0.37). We broadly defined "correct" orientation as spiders with an error angle (
) smaller than the stimulus angle (β) as error angles tended to be high for all groups. We log-transformed latency to orient (seconds) for normality. Once again, we found no significant difference in groups by latency to orient (ANOVA: F3,198 = 0.92, P = 0.43). Finally, we found no significant difference between groups by mean error angles of orientation (Kruskal–Wallis test: 
, P = 0.67).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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We demonstrated in the first experiment with litter mesocosms that autotomy and in some cases regeneration can have negative impacts on rate of prey capture in a complex habitat. Interestingly though, these impacts were not extended to other aspects of foraging (prey capture efficiency and sensory detection) in the more simple habitats of laboratory arenas during the second and third experiments. As predicted, in experiment 1 (prey capture rate in leaf litter), spiders that were missing a leg had lower prey capture rates than intact spiders for both prey weight groups. Also as predicted, these effects did differ by cricket weight. The effects on capture rate for the large prey size group (50% of spider weight) did not appear until 24 h for the medium prey size group (33% of spider weight). Similarly, Brueseke et al. (2001)
found a cricket weight x autotomy interaction in the wolf spider Pardosa milvina, where individuals missing a foreleg were less likely to capture larger crickets (Brueseke et al. 2001).
In this experiment, differences in prey capture between manipulated and intact spiders reflect a slightly increased prey capture rate from the initial trial by intact spiders, whereas prey capture for autotomized spiders was either reduced or stayed the same (Figure 2). This may indicate learning on the part of the intact spiders, which allowed them to capture more crickets with experience (Heiling and Herberstein 1999; Morse 2000). Due to their injury, spiders with an autotomized leg may have been unable to increase their prey capture rate between trials as the intact spiders did and in fact had a slight decrease in capture rate. The average prey capture rate at 24 h for the second trial was lower for autotomized spiders in both cricket weight categories. In a field setting, lizards that have undergone tail autotomy make fewer attempts to capture prey per time than intact lizards (Cooper 2003). Likewise, if autotomized spiders did give up sooner when attempting to capture prey, this could have contributed to the lower rate of capture.
We predicted that the spiders with a partially regenerated leg would have decreased prey capture rates as newly regenerated legs are often nonfunctional (Vollrath 1990). This prediction was supported for the large prey treatment group at both 6 and 24 h. This supports previous research for other animals which has shown reduced capture rates, decreased feeding efficiency, and switching to suboptimal prey during regeneration (Vollrath 1990; Juanes and Smith 1995). We do not know what it was that caused the spiders with autotomized or regenerating legs to have a lower capture rate in experiment 1 (the leaf litter mesocosm). This result could be explained by the spiders with missing legs having diminished capacity to sense or physically grasp prey, although we were unable to measure this, because capture was often hidden from view by the leaves. We attempted to address this further by running experiments 2 (capture efficiency) and 3 (vibratory cue detection).
In experiment 2 (prey capture efficiency), we found no effects of autotomy/regeneration on prey capture, which matches results of other laboratory studies performed on adult wolf spiders (Amaya et al. 2001; Brueseke et al. 2001). As Brueseke et al. (2001) demonstrated a trend for autotomized spiders to be less likely to capture larger prey (within the range of size for the prey presented), we expected that S. ocreata would show similar trends in the current study. However, contrary to our predictions, there were no significant autotomy x cricket weight interactions at any of the trial periods.
We dropped the large prey treatment group from analysis in this experiment due to their lack of prey capture in the last 2 trials. Because spiders had molted prior to the last 2 trials, the weights of the crickets offered as prey were adjusted accordingly. However, even though the crickets still weighed the same in proportion to the spiders, they were often larger than the spiders. This probably led to a reduced rate of acceptance as prey (Nentwig and Wissel 1986). This is also reflected by reduced capture rates for spiders during the last 2 trials in experiment 1 (Figure 2). However, because these spiders were allowed longer capture time (6 h vs.10 min), the spiders given larger crickets did not refuse prey entirely.
Missing or regenerating a foreleg may not only affect a spider by hampering its efforts to grasp and capture prey but also by decreasing its vibration sensory abilities as well. Hergenroder and Barth (1983) showed that vibratory information from the forelegs was most important in determining turning angle during prey orientation by the hunting spider Cupiennius salei. We predicted that S. ocreata would show similar effects and that missing or regenerating a foreleg would impact orientation in experiment 3 (vibratory cue detection). Contrary to this prediction though, we found no difference between groups for any of the measures of orientation. Furthermore, in most cases regardless of leg condition, S. ocreata tended to have inaccurate orientation to isolated vibrations (a 68° ± 8° error angle for intact spiders). This might have masked any differences between the groups somewhat. As with C. salei (Hergenroder and Barth 1983), S. ocreata tended to under orient, turning at less of an angle than they needed to face the prey. Additionally, in this experiment, spiders would sometimes reorient if the first angle was incorrect. This is unlike other spiders such as the Web-spinning species Zygiella x-notata and Nephila clavipes, which have low error angles of 4–7° (Klarner and Barth 1982). Hergenroder and Barth (1983) suggested that as the prey of C. salei is moving and not stuck in a Web, then these spiders only orient far enough to reach the prey before it can escape. It is possible that this is also true for S. ocreata, which hunts prey capable of quickly fleeing as well.
Overall, we found no detectable costs of losing or regenerating a leg on foraging (capture efficiency or sensory detection of vibratory cues) by spiders in a structurally simple habitat (filter paper) but a significant decrease in prey capture rate for these groups in a complex habitat (leaf litter). Unlike the filter paper substrate, the leaf litter might provide refuges for the cricket prey and furthermore could hinder the spiders’ reception of prey cues. Spiders missing or regenerating a leg might be unable to compensate under these conditions, making sensory detection and capture more difficult. After autotomy, in the leaf litter, spiders captured one less cricket on average per 6–24 h compared with intact individuals. Any missed opportunity to capture prey, however, small, may be important in the field, as spiders are often food limited (Anderson 1974; Kreiter and Wise 2001).
In comparing our results to other studies of arachnids, if we only look at results from the simple habitat, they would seem to support the "spare legs hypothesis" (Guffey 1999). This hypothesis suggests that because arachnids have many legs, it takes the loss of more than one to be costly. In the Guffey (1999) study and other previous studies of autotomy and/or regeneration in arachnids (Amaya et al. 2001; Brueseke et al. 2001), the authors tested foraging in simple habitats. Therefore, it is unknown whether those animals would have also shown significant impairment in more complex habitats as did S. ocreata in this study. In other taxa, the impacts of autotomy can differ based on which leg is lost. For example, Bateman and Fleming (2006) found that for crickets, autotomy of the foreleg (with specialized hearing organs) took longer than hind legs, indicating the difference in importance of these legs. It would be interesting to see if there is any difference in the impacts of foreleg versus hind leg autotomy on foraging or other activities in S. ocreata. Although both leg positions are lost almost equally in the field (Wrinn and Uetz 2007), forelegs are used in prey capture and mating displays (Rovner 1980; Scheffer et al. 1996), so we expect their loss would be more detrimental.
Reduction of prey capture in a complex but not a simple habitat has implications for trade-offs in the costs and benefits of microhabitat use after autotomy and/or during regeneration. Previous work has shown that after autotomy, an animal might have a heightened sense of escape behavior, which leads to greater use of complex microhabitats for protection against predation (Martin and Salvador 1992, 1993; Stoks 1999; Cooper 2003). However, by using these habitats to stay safe, an animal might be faced with suboptimal foraging. An example of this is study of Martin and Salvador (1992) which showed that Iberian rock lizards (Lacerta monticola) with missing tails have increased use of large rocks and decreased use of bare ground compared with intact lizards. This use of habitat might increase the lizard's chance of escape behavior but at the same time reduce foraging opportunities (Martin and Salvador 1993). Further examples of animals with autotomy that show increased use of complex habitat and decreased foraging can be found for lizards (Cooper 2003) and damselflies (Stoks 1999). This decrease in foraging in complex habitats could be because animals with missing appendages have a lower capture rate (our study) or because the complex habitats themselves have less optimal prey (Martin and Salvador 1993). Either way, autotomy and/or regeneration can put an animal in a position where it must choose safety or nutrition.
Stoks (1999) tested this trade-off in damselflies. He found that damselfly larva with intact caudal lamellae made decisions to forage in an "unsafe" simple habitat which had more prey based on whether there was a predator present or not. However, larva with autotomized lamellae stayed in a "safe" complex habitat most of the time, regardless of predator presence (Stoks 1999). It would be interesting to see if these results extend to other animals as well. In further studies, predator density and prey density could be manipulated to determine the microhabitat choice of autotomized and regenerating individuals under different conditions. Our study was unique in that it considered foraging under both autotomy and regeneration at different stages. Decreases in foraging during regeneration could have serious impacts on the individual if it does not receive the energy needed to regrow an appendage. To gain further understanding of the evolutionary trade-offs of these processes, additional studies could address the impacts of differential foraging success on development during regeneration.
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FUNDING |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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National Science Foundation (grant IBN 0239164) to G.W.U.; Sigma Xi; the American Arachnological Society; and University of Cincinnati Weiman/Wendell Fund to K.M.W.
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ACKNOWLEDGEMENTS |
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This work represents a portion of a thesis submitted by K.M.W. in partial fulfillment of the requirements for the Master of Science degree from the Department of Biological Sciences at the University of Cincinnati. We thank the following people for assistance with design and statistical analysis: E. Buschbeck, M. Polak, and A. Roberts. For providing comments on the manuscript, we thank: the Miami University EEB reading group and the Rypstra laboratory. We thank S. Pruiett and M. Salpietra for help with collection and maintenance of spiders.
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REFERENCES |
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