Kinship Influences Cannibalism in the Wolf Spider, Pardosa milvina

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1 Journal of Insect Behavior, Vol. 16, No. 1, January 2003 ( C 2003) Kinship Influences Cannibalism in the Wolf Spider, Pardosa milvina Carl D. Anthony 1 Accepted April 18, 2002; revised October 11, 2002 Recent studies have called into question the role of Wright s coefficient of relatedness (r) in the interactions among relatives. Kin selection theory predicts a positive relationship between relatedness and frequency of altruistic acts, but a number of researchers have reported the opposite relationship. I used a lycosid spider ( Pardosa milvina) to test the hypothesis that genetic relatedness would affect the propensity of a cannibalistic species to prey on genetic relatives. I considered lack of predation to be a form of altruism where the predator incurs a cost (loss of a meal) that benefits potential prey. Specifically, I questioned whether direct genetic offspring would be avoided as prey items and whether the sex or reproductive condition of a cannibalistic predator would affect the likelihood of predation on conspecific juveniles. As predicted by kin selection theory, spiderling mothers ate significantly fewer of their own offspring than they did of nonkin spiderlings of the same age. Adult virgin female and adult male spiders ate significantly more spiders than females that had recently carried spiderlings. Females with egg sacs consumed significantly fewer spiderlings than did virgin female spiders. These findings support Hamilton s rule and suggest that, in some systems, genetic relatedness plays a strong role in governing altruistic behavior toward relatives. KEY WORDS: filial cannibalism; wolf spider; Lycosidae; Pardosa milvina; kin selection; kin recognition. 1 Department of Biology, John Carroll University, University Heights, Ohio Fax: canthony@jcu.edu /03/ /0 C 2003 Plenum Publishing Corporation

2 24 Anthony INTRODUCTION Hamilton (1964, 1972) provided a series of mathematical statements connecting Wright s coefficient of relatedness (r) to social behavior. He predicted that altruistic behavior would increase in a population as long as the benefit to the altruist exceeded the cost of performing the behavior. Kin selection should favor such behavior if the benefit received by the altruist results in an increase in inclusive fitness. Kin selection, then, should favor altruistic acts, not toward genetic strangers but toward relatives. Hamilton s hypotheses were framed in the context of the evolution of eusociality and a rich body of research on the social insects has shown that in many cases his hypotheses have withstood attempts at falsification (Trivers and Hare, 1976; Sundstrom, 1994; Strassman, 1996). Hamilton s model is equally suited to testing hypotheses about social behavior in other groups and it seems especially relevant to testing hypotheses regarding cannibalism and infanticide, both common behaviors in a wide variety of animal taxa (reviewed by Polis, 1981; Hausfater and Hrdy, 1984; Elgar and Crespi, 1992). In cannibalistic species, avoidance of cannibalism can be considered a form of altruism in that a predator incurs a cost that benefits the spared prey individual. Recent studies on cannibalism (Goff and Stevens, 1995; Walls, 1995; DeWoody et al., 2001), however, have shown the opposite relationship between this behavior and the coefficient of relatedness. Arthropod predators that carry their young (centipedes, lycosid spiders, and scorpions) provide a unique system in which to pose questions regarding kin recognition and prey discrimination. Many of these species practice intraguild predation and/or cannibalism (Elgar and Crespi, 1992) and juveniles, because of their small size and similarity to other prey types, are especially at risk (Yeargan, 1975; Polis, 1981, 1984). Because females carry eggs and offspring externally, opportunities for phenotype (scent) matching exist between females and offspring but do not exist between offspring and males or between offspring and nonmothers. Thus, hypotheses regarding kin recognition abilities and cannibalistic traits of various reproductive states and for the sexes can be devised and tested. Lycosid spiders (wolf spiders) are active predators that do not use webs to capture food but instead either ambush or chase prey (Edgar, 1969; Foelix, 1996). Cannibalism is thought to occur commonly in the family (Edgar, 1969; Hallander, 1970; Yeargan, 1975; Wagner and Wise, 1996, 1997), but females of some species avoid preying on conspecific juveniles (Eason, 1969; Wagner, 1995) and, in some cases, even avoid preying on heterospecific spiderlings (Higashi and Rovner, 1975; Miller, 1989; Moring and Stewart, 1992). The propensity of females to avoid preying on juvenile spiders seems, at least in some species, to be governed by the reproductive condition of the female.

3 Cannibalism in the Wolf Spider, Pardosa milvina 25 When carrying egg sacs, females of Pardosa amentata (Edgar, 1970), P. valens (Moring and Stewart, 1992), and Shizocosa ocreata (Wagner, 1995) all exhibit a reduction in predatory behavior toward juvenile spiders. In the absence of phenotype matching or recognition alleles (Halpin, 1991), the use of a reproductive state as a mechanism of discrimination may be an effective strategy for ensuring that mothers do not inadvertently prey upon their own offspring. This type of avoidance mechanism is considered a form of indirect kin recognition (Waldman et al., 1988) and has been termed temporal-based or state-mediated recognition (Elwood, 1994). Recent studies have, however, indicated that some wolf spiders can detect airborne chemical cues of conspecifics and that males likely use these cues to locate receptive female spiders (Tietjen, 1979; Searcy et al., 1999). The ability of wolf spiders to communicate via airborne chemical cues raises the possibility that female wolf spiders may not have to rely solely on temporal-based kin recognition but, instead, could use scent matching to make foraging decisions regarding juvenile conspecific spiders. Evidence for direct kin recognition and subsequent avoidance of filial cannibalism (Rohwer, 1978) is lacking in wolf spiders, but there may be reason to expect that such behavior has evolved. Wagner and Wise (1997) showed that cannibalism is likely a significant mortality factor in members of the genus Schizocosa and a number of researchers have reported cannibalism to be important in members of the genus Pardosa (Edgar, 1969; Hallander, 1970; Yeargan, 1975). Yeargan (1975) reported that conspecifics made up nearly 30% of prey of female P. pullata. Thus at least in some species, conspecific prey may be an important energy resource. The relatively large size of lycosid juveniles may increase their value as prey as well. Relative to web-building genera, cursorial spiders produce fewer and larger eggs (Simpson, 1995). This increases the cost incurred by a predator that inadvertently eats its offspring, but it also increases the cost to a predator of passing up relatively large, nutritious, nonkin prey. It would be especially advantageous for mothers to be able to recognize their own offspring if the probability of encountering unrelated spiderlings is high. In such systems, spiders that cannot recognize kin, and rely instead on temporal-based kin recognition, would be at a selective disadvantage. Thus four factors may contribute to selection for direct kin recognition in wolf spiders: (1) the use of airborne chemical cues in communication (Searcy et al., 1999); (2) the opportunity for scent matching afforded to females from carrying the offspring externally; (3) the production of relatively large, nutritious offspring (Simpson, 1995); and (4) the existence of high densities of reproductive females and their offspring (Yeargan and Cothran, 1975; Allen, 1999). I used a small, ground-dwelling lycosid spider, Pardosa milvina, to test hypotheses of kin recognition and its role in cannibalism. Individuals of

4 26 Anthony P. milvina typically live for a single year, but some females probably produce multiple egg sacs in the field (females have produced up to three viable egg sacs in the laboratory [Anthony, unpublished]). In northern Ohio, where the current study took place, mating occurs in late May and early June but may continue throughout the summer (Allen, 1999). Females with egg sacs are first observed in June, are most common in August, and can be found rarely as late as early October (Allen, 1999). The egg sac is carried by the female until the spiderlings hatch and is abandoned as dispersal occurs. Once the egg sac is opened by the female, the spiderlings crawl onto the female s abdomen and remain there for approximately 5 days. Females from the population that I studied typically produce 30 to 40 spiderlings from their first egg sac (Anthony, unpublished). I reasoned that in the absence of a direct kin recognition system, predators would be forced to play a best-odds game where those predators that had not previously reproduced would be free to prey on conspecifics indiscriminantly, but reproductively active predators would be forced to adjust their rates of cannibalism in proportion to the likelihood of encountering prey that were kin. Specifically, I reasoned that females that had never mated would be the most likely to prey on conspecfics because, in the field, the likelihood of their sharing genes with a randomly encountered spiderling would be low. I predicted that males would also show high levels of cannibalism for the same reason but that, compared to virgin females, they would be less likely to cannibalize juveniles because (1) their energy demands should be lower because they do not produce yolk or carry eggs, and (2) they would have a slightly higher chance of being related to spiderlings that they encounter because males may mate with multiple females. I predicted that females carrying egg sacs would exhibit some reduction in the propensity to prey on conspecifics because other researchers had established that the egg sac causes a cessation in feeding (Edgar, 1970; Moring and Stewart, 1992; Wagner, 1995). Finally, I predicted that mothers who had recently carried spiderlings would exhibit the lowest levels of cannibalism but that mothers should be able to recognize and avoid preying on their direct offspring. I predicted, then, that rates of cannibalism would be highest in virgin females, followed by males, females with egg sacs, foreign mothers, and, finally, the spiderlings own mothers. METHODS I collected males and females of Pardosa milvina between 11 May and 4 June 1999 from a grassy area (approx 1/8 ha) bordering beech and maple woodland in eastern Cuyahoga Co., Ohio ( N, W).

5 Cannibalism in the Wolf Spider, Pardosa milvina 27 Spiders were collected as adults but females had not yet produced egg sacs. Spiders were held individually in the field and were transferred to the laboratory where they were housed under a natural (Cleveland, OH) photoperiod in plastic chambers measuring cm. The chambers were opaque sided with clear lids and contained two moistened cotton balls as a water source. I fed spiders fruit flies, Drosophila virilis, ad libitum. Laboratory temperature ranged from 22.3 to 24.3 C. Because the spiders were obtained early in the breeding season, it is likely that females produced their first egg sac of the season in the laboratory. Females that produced egg sacs were monitored daily for emergence and dispersal of spiderlings. Once dispersal from the female s abdomen occurred (as indicated by % dispersal), I transferred spiderlings to circular experimental arenas measuring 5.5 cm in diameter. A small portion of moistened cotton ball, approximately 2 cm in diameter, served as a water source. Eight spiderlings were placed in each arena, where they were paired with either (1) their own mother (n = 23), (2) another mother from which spiderlings had dispersed on the same day (n = 23), (3) a female carrying an egg sac (n = 19), (4) a virgin adult female (n = 13), or (5) an adult male spider (n = 22). Virgin adult female spiders were those spiders that failed to produce fertile egg sacs during the summer of Testing began 1 day after spiderling dispersal on 2 consecutive days. Testing was conducted over 2 days because a mother could not be simultaneously paired with her own and another mother s offspring. Each mother was, therefore, paired with her own and another mother s offspring in random order on 2 consecutive days. Individual males, virgin females, and females with egg sacs were randomly paired with spiderlings, but treatments were dispersed evenly throughout the testing season (Hurlbert, 1984). I carefully placed adult spiders into the testing arenas and then, during the first 60 s of each trial, I noted whether or not spiderlings were attacked and, if so, whether or not they were released or eaten. I recorded the number of spiderlings eaten after 2 and 24 h for each treatment and the number of spiderlings that resettled (crawled back onto the abdomens of adults) in each of the treatments. I used nonparametric statistics because the data failed to meet the assumptions required of parametric statistics. A Kruskal Wallis ANOVA was applied to the number of spiderlings eaten in treatments 1 and 3 5 above, and Bonferroni multiple comparisons were made between treatments. The number of spiderlings eaten by their own mothers was analyzed with a repeated-measures analysis with time as a fixed factor. The number of spiderlings eaten by their own and by other mothers was analyzed with a paired Wilcoxon signed-ranks test as each mother was tested with her own and another spider s offspring. Frequencies of trials in which spiders caught and subsequently released spiderlings, where spiderlings resettled on adults,

6 28 Anthony and where spiderlings were immediately eaten were analyzed with a G test of independence with William s correction (Sokal and Rohlf, 1995). A total of 100 adult and 800 juvenile spiders was used in the study. RESULTS Spiderlings placed in contact with adult spiders either were immediately eaten (immediate predation), were seized and subsequently released by the adult (capture and release), or climbed onto the abdomen or carapace of the adult (resettlement). Frequency of immediate predation (G = 5.72, df = 4, P < 0.025), capture and release (G = 5.85, df = 4, P < 0.025), and resettlement (G = 10.99, df = 4, P < 0.001) was treatment dependent. I observed successful predation on spiderlings in all treatments during the 60-s direct observation phase. The frequency of predation during this short time period was lowest in treatments where spiders were paired with their own offspring and where they were paired with females carrying egg sacs (Fig. 1a). The frequency was highest in trials with virgin females, males, and foreign mothers (Fig. 1a). Only spiders from which spiderlings had recently dispersed (own mothers and foreign mothers) caught and subsequently released spiderlings. This occurred in 13.0% of trials where spiderlings were paired with their own mothers and 8.7% of trials where spiderlings were paired with foreign mothers (Fig. 1b). I observed resettlement by spiderlings only in trials with reproductive females. The frequency of resettlement was highest in trials with foreign mothers, somewhat lower for mothers of spiderlings, and lowest for females with egg sacs. Spiderlings were not observed to resettle on males or virgin females (Fig. 1c). There was a significant effect of treatment on the number of spiderlings eaten after 2h(P<0.0001) and 24 h (P < 0.001). At both time periods, adult virgin female spiders ate the most spiderlings, followed by males, females with egg sacs, and mothers of the spiderlings (Figs. 2a and b). After 2 h, significant differences in the number of spiderlings eaten were found be- Fig. 1. Data collected during the initial 60-s observation period directly following the introduction of an adult Pardosa milvina into the testing chamber containing eight conspecific spiderlings. Percentage of trials in which (a) spiderlings were immediately attacked and eaten, (b) spiderlings were captured and released, and (c) spiderlings resettled on adults. Spiderlings were paired with their own mother, a female from which spiderlings had recently dispersed (foreign mother), a female carrying an egg sac, a male spider, and a virgin female spider. Percentages were dependent on treatments in each case (G test with William s correction: predation, G = 5.72, df = 4, P < 0.025; capture and release, G = 5.85, df = 4, P < 0.025; resettlement, G = 10.99, df = 4, P < 0.001).

7 Cannibalism in the Wolf Spider, Pardosa milvina 29

8 30 Anthony Fig. 2. Mean number of spiderlings eaten after (a) 2 h and (b) 24 h of time spent with adult conspecifics. Spiderlings were paired with their own mother, a female carrying an egg sac, a male spider, and a virgin female spider. An ANOVA detected significant treatment effects after 2 h(f = 13.79, df = 3, P < ) and 24 h (F = 7.78, df = 3, P < 0.001). Treatments connected by a horizontal bar indicate that no significant differences existed between them. tween males and spiderling mothers (z = 3.19, df = 2, P < 0.05) and virgin females and spiderling mothers (z = 5.19, df = 2, P < 0.05). These differences persisted after 24 h (males and mothers, z = 3.22, df = 2, P < 0.05; virgin females and mothers, z = 3.35, df = 2, P < 0.05). Female spiders

9 Cannibalism in the Wolf Spider, Pardosa milvina 31 carrying egg sacs ate significantly fewer spiderlings than did virgin females, but only after 2, not 24 h, (z = 3.78, df = 2, P < 0.05). After 2 h, spiderling mothers had eaten significantly fewer of their own offspring compared to those of another spider s (z = 1.71, df = 1, P < 0.044; Fig. 3a). By 24 h, spiderling mothers had still eaten fewer of their own offspring, but the difference between treatments was not significant (z = 0.76, df = 1, P < 0.22; Fig. 3b). The number of spiderlings consumed by their mothers increased over the three time periods (0, 2, and 24 h) (F = 13.12, df = 2, P < ), suggesting that the ability to detect kin diminished with time. In all cases, spiderling mothers had abandoned their egg sacs prior to testing. DISCUSSION The negative fitness consequences of consuming one s own young have resulted in the evolution of prey discrimination in a number of otherwise cannibalistic taxa. The degree of discrimination varies, however, among taxa. Some cannibalistic species are apparently capable of distinguishing offspring from nonrelatives (Loekle et al., 1982; this study), while others refrain from feeding during risky time periods (e.g., after reproduction or when young are present [Elwood, 1977, 1994; Linsenmair, 1987]). The latter strategy, termed temporal-based kin recognition (Elwood, 1994), is thought to have arisen in cases where it is less costly to avoid certain prey types (or, in some cases, prey altogether) than it is to develop complex kin recognition systems. True kin recognition should evolve in situations where there is an opportunity for scent matching or phenotype matching and/or where it is especially costly to refrain from feeding on potentially valuable prey types. I found evidence for both indirect and direct mechanisms of kin recognition in Pardosa milvina. As reported for other lycosid spiders (Higashi and Rovner, 1975; Moring and Stewart, 1992; Wagner, 1995), females of P. milvina that were carrying egg sacs ate fewer conspecific spiderlings than did virgin females, suggesting that females time their reduction in feeding to coincide with an increase in risk of preying on direct offspring. However, mothers also displayed an ability to distinguish between direct and nonkin offspring, preferring to cannibalize nonkin over kin. This is the first report of direct kin recognition in a lycosid spider. Indirect Kin Recognition Cessation of feeding while carrying the egg sac has been postulated to function as a temporal (indirect) mechanism of kin recognition in that

10 32 Anthony Fig. 3. Mean number of spiderlings eaten after (a) 2 h and (b) 24 h of time spent with either their own mother or a conspecific female (foreign mother) from which spiderlings had recently dispersed. Females ate significantly fewer of their own offspring after 2 h (z = 1.71, df = 1, P < 0.044) but not 24 h (z = 0.76, df = 1, P < 0.22) (paired Wilcoxon signed-ranks test, one tailed). it decreases the likelihood of preying on direct offspring (Wagner, 1995). I found evidence for such a system in P. milvina. After 2 h of cohabitation, female spiders that were carrying egg sacs ate significantly fewer spiderlings than did virgin females. They also exhibited a low frequency of immediate attacks on spiderlings, similar to the frequency exhibited by

11 Cannibalism in the Wolf Spider, Pardosa milvina 33 the spiderlings own mothers. In some cases, females with egg sacs even allowed spiderlings to resettle on their abdomens. Higashi and Rovner (1975) described similar resettlement behavior for egg sac-carrying females of Lycosa rabida. I predicted that virgin females and males would exhibit the highest rates of cannibalism because these spiders would be unlikely to be related to juveniles that they encounter in the field. As predicted, virgin female spiders exhibited the highest frequencies of immediate attack and consumed the most spiderlings during the cohabitation experiments. Males behaved similarly. There were no significant differences between male and virgin female spiders in the number of spiderlings eaten after 2 and after 24 h of cohabitation, and males exhibited a similarly high frequency of immediate attack when paired with conspecific juveniles. Higashi and Rovner (1975) reported similar findings for males of L. rabida and Wagner (1995) reported a 100% acceptance rate of conspecific spiderlings by virgin females of the wolf spider, Scihzocosa ocreata. For females of semelparous species, and in species where the chances of multiple reproduction are slim, the cost of passing up nonkin prey is relatively low because there is no need to expend energy on vitellogenesis of subsequent clutches. In such species, temporal-based kin recognition may be an efficient way to discriminate among potential prey items because it does not require complex adaptations enabling recognition of relatives. However, in iteroparous species, the cost of passing up prey could translate directly into a lower reproductive output (Rohwer, 1978). Females of P. milvina are capable of producing up to three viable egg sacs in the laboratory and they produce smaller clutches when fed on a restricted diet (Anthony, unpublished). Other researchers have documented the production of multiple, viable egg sacs in other members of the genus in laboratory studies (up to five for P. ramulosa [Yeargan and Cothran, 1975] and up to four P. lapidicina [Eason, 1969]). Edgar (1970) reported that females of P. amentata produce two egg sacs per field season in The Netherlands. It is unknown whether females of P. milvina produce multiple egg sacs in the field, but their ability to store sperm and produce multiple egg sacs in the laboratory suggests that they may be iteroparous. If members of the genus Pardosa can be considered iteroparous, one would not expect early season females, such as those used in the current study, to stop feeding during any reproductive phase. My data support this prediction. Spiderlings were consumed by female spiders in all treatments, including those in which females were carrying egg sacs and those in which females had recently carried spiderlings. Females with eggs sacs did, however, eat fewer spiderlings than did virgin females (after 2 h), suggesting that some degree of temporal-based kin recognition is present.

12 34 Anthony Direct Kin Recognition Females of P. milvina possess the ability to recognize kin directly as evidenced by female spiders consuming significantly fewer of their own offspring than of same-aged conspecifics. Eason (1969) reported that, while carrying young, females of P. lapidicina would not consume either their own or other females spiderlings but that, after spiderling dispersal occurred, females resumed predatory behavior. Eason (1969) did not indicate whether females preferentially preyed on nonkin spiderlings. Most other studies have examined the predatory behavior of female lycosids when carrying egg sacs or young (Higashi and Rovner, 1975; Moring and Stewart, 1992; Wagner, 1995). These studies indicate that female lycosids are generally tolerant of spiderlings (often regardless of species) and that they suppress feeding during the egg sac phase. In the current study, mothers were tested h postdispersal, when predatory behavior would presumably resume. At the end of the 2-h cohabitation period, female spiders ate significantly fewer of their own offspring then they did of other conspecific females offspring. However, after 24 h of testing, no significant difference in consumption rates was detected and a repeated-measures analysis indicated that kin recognition by spiderling mothers diminished with time. It is possible that the artificial nature of the experimental arena interfered with the abilities of spiderlings to escape predation, but even a slight hesitation on the part of an adult spider could afford a juvenile spider an opportunity for escape in the complex three-dimensional litter layer. Postdispersal females exhibited the highest levels of attack and release of spiderlings, suggesting that these females are under energetic pressure to feed. In small experimental chambers, as used in this study, females may have inadvertently killed spiderlings after repeated captures. Iteroparity could provide an additional selective advantage for direct kin recognition. If females have the ability to continue to recognize offspring throughout the active season, they could use this information in foraging decisions involving later-instar spiders spiders that might be offspring from previous reproductive events. In the current study, spiders were separated from their mothers for only a short time period (24 48 h). It is unknown whether recognition persists through time or through successive molts. ACKNOWLEDGMENTS I thank Robert Kranz for help in collecting and maintaining spiders and Stacey Allen for identification of Pardosa milvina. Case Western Reserve University allowed spiders to be collected from their research property at

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