Autotomy-induced life history plasticity in band-legged ground cricket Dianemobius nigrofasciatusens_

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1 Entomological Science (2010) 13, 1 7 doi: /j x ORIGINAL ARTICLE Autotomy-induced life history plasticity in band-legged ground cricket Dianemobius nigrofasciatusens_ Nobuhiro MATSUOKA and Michihiro ISHIHARA Department of Biological Science, Graduate School of Science, Osaka Prefecture University, Sakai, Osaka, Japan Abstract Crickets can autotomize their limbs when attacked by predators. This enables them to escape death, but imposes a short-term cost on their escape speed and a long-term cost on their future mating ability. Therefore, adaptive response compensated for the cost of autotomy might be advantageous for autotomized individuals. In the present study, we examined whether autotomy induced life history plasticities compensating for the future cost in the band-legged ground cricket Dianemobius nigrofasciatus. Life history traits of D. nigrofasciatus were compared between autotomized and intact individuals. The developmental time and head width of the individuals that were autotomized as fourth instar nymphs were significantly shorter and smaller, respectively, than those of intact individuals. However, the adult longevity, number of eggs laid and oviposition schedule did not vary between autotomized and intact individuals. In addition, there was no difference between individuals autotomized at the fourth instar and adult stages in these three traits. Early maturation in the autotomized individuals might be advantageous through reducing the risk of predation owing to the shorter period in nymphal stages. The cost of small body size in the autotomized females might not be so great because of no significant difference in fecundity between autotomized and intact individuals. However, the cost of small body size was unclear in the autotomized males because in general larger males were preferred by females. These results indicated autotomy-induced life history that might reduce the cost of autotomy. Key words: defense system, life history traits, Orthoptera, phenotypic plasticity, predator risk. INTRODUCTION Phenotypic plasticity refers to the ability of a genotype to exhibit alternative morphological, behavioral and physiological characteristics in response to environmental variation (West-Eberhard 1989; Garland & Kelly 2006), which comprises both abiotic and biotic components including interactions among organisms. Phenotypic plasticity can increase the degree of adaptability by causing changes in correspondence with the environment. For instance, some organisms reduce predation risk by exhibiting phenotypic changes in morphology after direct contacts with predators, or chemical substances emitted from predators (e.g. Kusch 1993; Correspondence: Nobuhiro Matsuoka, Department of Biological Science, Graduate School of Science, Osaka Prefecture University, 1-1 Gakuen-cho, Naka-ku, Sakai, Osaka , Japan. delicateplanet@gmail.com Received 8 December 2008; accepted 28 May Trussell 2000; Kishida & Nishimura 2004). Such predator-induced plasticities, which can include changes in adult size or time to maturity, are common responses to stressors (reviewed in Blanckenhorn 2000; Peckarsky et al. 2001; Dahl & Peckarsky 2003). Typically, early maturation will reduce cumulative pre-reproductive mortality, but comes at the cost of reduced fecundity associated with a smaller body size (Johansson et al. 2001). Autotomy, the voluntary self-amputation of a limb or other appendage to aid escape from predators, occurs in many taxa including insects (reviewed in Fleming et al. 2007). The most prevalent benefit of autotomy is predation avoidance. An autotomized appendage can distract the predator through movement or can itself be sufficient attraction as a substitute meal (reviewed in Maginnis 2006; Fleming et al. 2007). For example, two species of terrestrial crabs (Potamocarcinus richmondi, Gecarcinus quadratus) autotomized their chelipeds after the chelae were firmly attached to a predator (Robinson

2 N. Matsuoka and M. Ishihara et al. 1970). Moreover, if an appendage is wounded, an animal can choose to autotomize it rather than carry around a useless limb that may be an encumbrance or even attract the attention of a predator (Shimizu & Masaki 1993; Johnson & Jakob 1999; McCarthy & Dickey 2002). Despite its immediate benefits, autotomy has costs such as impediments to locomotory speed, feeding behavior and mating success. For instance, in the cricket Gryllus bimaculatus, loss of a leg by autotomy results in a decrease in future escape speed and mating ability (Bateman & Fleming 2005). In the cricket Acheta domestica, the autotomy of a hind limb similarly results in significant reduction in escape speed and jumping ability, and therefore makes the animals more susceptible to predation (Bateman & Fleming 2006). Regeneration can offset many of the potential longterm costs of autotomy (reviewed in Maginnis 2006). However, autotomized limbs are not naturally regenerated in Orthoptera except by experimental operations at a non-predetermined breakage plane (reviewed in Bullière & Bullière 1985). Therefore, the adaptive plastic response, such as faster growth and altered oviposition behavior as a form of phenotypic plasticity compensating for the cost of autotomy, might be predicted in individuals autotomized as nymphs. Once individuals become adults, they have no more opportunity to make use of phenotypic plasticity excepting behavioral plasticity. In the ground cricket Dianemobius fascipes (Gryllidae), the severance of appendages by autotomy in the nymphal stage exerted a micropterizing effect on wing morphology (Shimizu & Masaki 1993). At a stable condition, micropterous individuals might have a higher fitness than macropterous individuals, as shown by mating and number of eggs laid in certain species of crickets (Tanaka 1976; Roff 1984; Crnokrak & Roff 1995, 1998). For autotomized individuals, early maturation might be adaptive through reducing the risk of predation in the nymphal stage. The slow growth/high mortality hypothesis predicts that individuals with slow growth should suffer higher predator-caused mortality owing to the longer period spent in vulnerable nymphal stages compared with individuals with fast growth (Feeny 1976; Clancy & Price 1987; Häggstörm & Larsson 1995). However, early maturation may cause their body size to be smaller, resulting in a decrease in fecundity and male male competitive ability. Therefore, it is necessary to consider not only the benefit of early maturation but also the cost of small body size caused by autotomy. However, only a few studies have focused on the importance of autotomy-induced life history plasticity in Orthoptera (Shimizu & Masaki 1993; Ortego & Bowers 1996; Bateman & Fleming 2005). In the present study, we compared life history traits of developmental time, body size, fecundity and adult longevity between individuals autotomized as nymphs and individuals left intact. MATERIALS AND METHODS Stock cultures Twelve adult females of D. nigrofasciatus were collected from grassland at Daisen-cho, Sakai (Osaka, Japan) on 7 July These crickets collected were regarded as mated because all females could lay fertile eggs. They were kept individually in plastic containers (80 mm diameter, 140 mm depth), with a sheet of filter paper on the bottom of each container. Crickets were fed an insect diet (Oriental Yeast, Tokyo, Japan) and pieces of carrot. The food was replaced every two days. A moist cotton plug, which served both as a water source and a site for oviposition, was provided in each case. Eggs laid were collected and maintained in a plastic container (78 mm diameter, 35 mm depth) at 23 C, under conditions of 16 h light : 8 h dark (LD 16:8). Ten nymphs hatched from the eggs that were laid by each collected female were introduced into a plastic container (125 mm diameter, 75 mm depth) and were reared together until the third molt but individually from the fourth instar to adult emergence at 25 C, LD 16:8. Adults emerged after the sixth molt. When adults emerged, they were paired (while avoiding sib-mating) and each placed in a plastic container (78 mm diameter, 35 mm depth). Individuals of the F2 generation were maintained in the same way at 25 C, LD 16:8. This photoperiodic condition does not induce embryonic diapause in D. nigrofasciatus (Shiga & Numata 1996). Experimental design F2 crickets of the stock culture were used in this experiment. These nymphs were randomly divided into three groups at the fourth instar. These three groups were treated as follows: the first and second groups were autotomized at the fourth instar and the adult stages, respectively. Autotomy was induced easily by nipping the right hind femur briefly with tweezers (following Fleming & Bateman 2007). Hind limbs were autotomized as, in the field, hind legs tend to be missing more often than middle or front legs (Bateman & Fleming 2005). Because they are the largest and most noticeable legs, hind legs are presumably more likely to be grabbed first by a predator (Wasson et al. 2002). In all cases D. nigrofasciatus autotomized their own legs at the point 2 Entomological Science (2010) 13, 1 7

3 Autotomy-induced plasticity in a cricket between femur and trochanter. Both the fourth-instar nymphs and adults were autotomized within 24 hours of molting. The third group was maintained intact as a control. These crickets were reared individually from fourth instar to adult emergence in plastic containers (78 mm diameter, 35 mm depth). When adults molted, we recorded the developmental times from hatching to adulthood, head width as an indicator of adult body size, and growth rates. Because in crickets head width is generally correlated with other characters reflecting body size such as pronotum length, ovipositor length and body weight, we used the head width as an index of the body size (e.g. Masaki 1967; Bertram 2000; Bégin et al. 2004). The growth rate was calculated as the head width divided by the developmental time. Each male from the control group was paired randomly with a female from any of the three treatment groups. In this way, sib-mating was avoided. When first oviposition was observed, we recorded the preoviposition period from adulthood to the first oviposition. The number of eggs laid in the cotton plugs was counted every day. When an adult died, we recorded the adult longevity from adult emergence to death. Statistical analysis Developmental times, growth rates, head widths and adult longevity were analyzed using three-factor mixed model analysis of variance (anova), where sex and treatment as fixed factors and family as a random factor were crossed. Developmental times were log 10- transformed before the analysis. Pre-oviposition period and the numbers of eggs laid were analyzed by twofactor mixed model anova, where treatment as a fixed factor and family as a random factor were crossed. Oviposition schedule was represented as the number of eggs laid each day (during the first nine days) divided by the total number of eggs laid over that period. Most females laid more than 90% of all eggs during the first nine days. Oviposition rate was arcsine-transformed before being analyzed by repeated-measures anova, where day and treatment as fixed factors were crossed. RESULTS There were significant sex, treatment and family effects and a sex family interaction on developmental time and head width (Table 1). The developmental times of autotomized individuals were shorter than those of intact individuals in both sexes (Fig. 1a) and head width of autotomized individuals was smaller than that of intact individuals in both sexes (Fig. 1b). There were Table 1 anova table for the effect of autotomy on developmental time, head width and growth rate Developmental time Head width Growth rate d.f. SS F P d.f. SS F P d.f. SS F P Treatment < Sex Family Treatment Sex 1 < < Treatment Family < Sex Family < Treatment Sex Family < Residual Entomological Science (2010) 13, 1 7 3

4 N. Matsuoka and M. Ishihara Figure 1 Effect of autotomy at the fourth instar on (a) developmental time, (b) head width and (c) growth rate. Bars show mean + SD. Sample sizes are shown in parentheses. Table 2 anova table for the effect of autotomy on adult longevity significant sex and family effects on growth rate but no treatment effect (Table 1, Fig. 1c). There was a significant sex effect on adult longevity (Table 2) and a significant family effect on the number of eggs laid (Table 3) but not a treatment effect on both traits (Figs 2,3a). For the pre-oviposition period and oviposition schedule, anova indicated no significant main effect or interaction (Tables 3,4, Figs 3b,4). There was no significant difference between individuals autotomized at the fourth instar and at the adult stage in all traits (Figs 2 4). DISCUSSION d.f. SS F P Treatment Sex Family Treatment Sex Treatment Family Sex Family Treatment Sex Family Residual This study shows that individuals autotomized as nymphs had a significantly shorter developmental time than those left intact (Fig. 1a). Because of decreases in escape speed and jumping ability in autotomized individuals (Bateman & Fleming 2005, 2006), autotomized nymphs are likely to be preyed on more frequently than intact nymphs. Once insects become adults, the adults missing a leg may be able to avoid predators better than juveniles without a leg although we have not had any evidence of this yet. Therefore, early maturation in the autotomized individuals might be adaptive through reducing the risk of predation in the nymphal stages. This is also supported by the slow growth/high mortality hypothesis (Feeny 1976; Clancy & Price 1987; Häggstörm & Larsson 1995). For instance, predation rate during the larval period of the leaf beetle Galerucella lineola was higher in larvae that developed slower than in those that developed faster (Häggstörm & Larsson 1995). In this experiment, however, the difference in developmental time between autotomized and intact crickets was only one day. It is unknown whether such a short difference in developmental time results in a difference in nymphal mortality by predation between autotomized and intact crickets. In this experiment, however, crickets were maintained at 25 C; this temperature may be too high to result in a large variation in developmental time between treatments. Moreover, if autotomy had occurred at earlier stages, developmental time of the autotomized individuals may become much shorter than intact individuals. In the field, nymphs of D. nigrofasciatus might encounter temperatures lower than 25 C and varying day lengths. In Sakai, Osaka, the average temperature in late May when the nymphs of the first generation grow is 20.7 C ( ) (National Astronomical Observatory 2006). Such field conditions may produce greater differences in developmental time between autotomized and intact individuals than under constant laboratory conditions. In addition to reduced developmental time, autotomized nymphs were significantly smaller as adults than intact individuals (Fig. 1b). The smaller size of autotomized individuals might result from a positive correla- 4 Entomological Science (2010) 13, 1 7

5 Autotomy-induced plasticity in a cricket Table 3 anova table for the effect of autotomy on fecundity Pre-oviposition period Number of eggs laid d.f. SS F P d.f. SS F P Treatment Family Treatment Family Residual Figure 2 Effect of autotomy on adult longevity. Bars show mean + SD. Sample sizes are shown in parentheses. Autotomy was induced at the fourth instar and adult stages. Table 4 anova table for the effect of autotomy on oviposition schedule d.f. SS F P Treatment Subject Day < Treatment Day Day Subject tion between developmental time and body size, because autotomized individuals did not differ in growth rate from intact individuals (Fig. 1c). In general, smaller body size is disadvantageous in reproduction because adult body size is correlated with fecundity in females and male male competitive ability in males (reviewed in Honek 1993). In the present study, however, the fecundity of autotomized females was not significantly different from that of intact females (Figs 3a,b,4). This result suggests that small adult body size in autotomized females does not impose a significant cost to their reproduction. Therefore, the benefit of early maturation in autotomized females might exceed the cost of small body size. In contrast to females, because in general larger males are preferred by females due to the song structure or large nuptial gifts as a form of parental investment (Simmons 1986; Galliart & Shaw 1994; Brown et al. 1996; Gray 1997; Fedorka & Mousseau 2002), the smaller body size in autotomized males may be disadvantageous in reproduction. It is unclear that the benefit of early maturation in autotomized individuals might exceed the cost of small body size in males. Predation has long been implicated as a major selective force in the evolution of several morphological and behavioral characteristics of animals (Lima & Dill 1990). Empirical investigations of predator-induced morphological and behavioral plasticity have documented an extensive list of prey responses to a diverse array of predators. Predator-induced plasticity associated with morphology in prey has received considerable attention (e.g. Dodson 1989; Skelly & Werner 1990; Stoks 2001; Kishida & Nishimura 2004). Nevertheless, only a few studies have focused on the predator-induced plasticity of life history traits, such as longevity and reproductive traits (e.g. Riessen 1999; Peckarsky et al. 2002; Bateman & Fleming 2005). Autotomy is usually induced by predation and studying autotomy is a way of looking at indirect predator-induced impacts on reproduction. In orthopteran species, a few studies have compared nymphal developmental times between autotomized and intact individuals and they did not find autotomy-induced plasticity in this trait (Shimizu & Masaki 1993; Ortego & Bowers 1996). The present study showed autotomy-induced plasticity as an adaptive response that helps compensate for the cost of autotomy in Orthoptera. More studies should thus focus on predator-induced life history plasticity to achieve a more complete understanding of the mechanisms and evolution of predator-induced plasticity. ACKNOWLEDGEMENTS We thank Dr T. Namba and Dr K. Tanida of Osaka Prefecture University for their valuable comments, and Dr H. Numata and Dr S. Shiga of Osaka City University for assistance with collecting and advice on rearing of Entomological Science (2010) 13, 1 7 5

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