Epipompilis insularis (Hymenoptera: Pompilidae), a parasitoid of hunting spiders

Abstract

Epipompilis insularis females were found to attack 2 species of hunting spider, Clubiona cambridgei and Salticus sp., and oviposit on them. All spiders were females which had oviposited and were inside their nests with their eggs. After eating the spiders, the larval parasitoids fed on the developing eggs or post-embryos, a facet of behaviour not previously reported for a pompilid wasp.     

Attack Behavior of Two Wasp Species of the <Emphasis Type="Italic">Polysphincta</Emphasis> Genus Group (Hymenoptera,Ichneumonidae) on their Orb-Weaver Spider Hosts (Araneae,Araneidae)

Species in the Polysphincta genus group, as far as is known, are exclusively koinobiont ectoparasitoids of spiders. These wasps attack their hosts, inflicting a temporary paralysis, and then lay one egg on the host’s abdomen or prosoma. Parasitoid attack behavior is highly variable among species, including occasions where the wasp darts directly and holds the spider, as well as instances involving complex behavioral sequences. In the present study, we describe the attack behavior of Polysphincta sp. nr. purcelli and P. janzeni on Cyclosa fililineata and C. morretes, respectively. All attacks occurred at night. Initially, the female wasp landed on the web hub at the position occupied by the spider, with the spider always escaping from this initial attack. Subsequently, the wasp waited for up to 14 h at the web hub for the spider’s return. The wasp then inserted its ovipositor into the mouth of the spider, after which the spider became paralyzed and remained motionless for at least 30 min. The wasp laid one egg on the surface of the host’s abdomen and remained on the web for at least 1 h thereafter. The lie-in-wait and attack only after the return of the host to the web hub, as well as the permanence of the wasp on the web after the attack are not frequent behaviors described for polysphinctines. Behavioral idiosyncrasies, such as those observed here, are common among polysphinctines, suggesting a high level of specific adaptive matching of polysphinctine parasitoid behavior to their hosts’ biological characteristics.     

Life history of the spider parasitoid Zatypota percontatoria (Hymenoptera: Ichneumonidae)

The life history of polysphinctine parasitoids is poorly understood. As a result, their effect on their host has not been evaluated. Here, we present the phenology of Zatypota percontatoria, an ectoparasitoid wasp of theridiid spiders, using rich field, semi‐field and laboratory investigations of selected life‐history parameters. The wasps overwintered as larva attached to the spider abdomen and the imagos of the first generation emerged at the beginning of May. The sex ratio (F/M) of overwintered wasp larvae was 1.4. The wasp spent an average of 6.4 days in the egg stage, 27.67 days in the larval stage and 9.6 days in the pupal stage. Adult longevity was on average 14.34 days. Oviposition occurred on average 8.44 days following maturity. The wasp laid on average 0.35 eggs/day. The total fecundity was on average 7.4 eggs per wasp and decreased with age (data from unmated females). The developmental rate increased with experimental temperature up to 28 °C. The lower developmental threshold for pupae was estimated at 6.6 °C. The sum of effective temperatures for pupae was estimated at 157.8 degree days. Using daily temperature records from the Czech Republic over the last 41 years, we estimated an average of 3.5 generations of Z. percontatoria per year. Mortality was 48% in semi‐field conditions and 23% in the laboratory. The incidence of mortality was highest during egg and larval stages caused by the detachment of eggs or larvae during spider molting, the mortality of the spider‐host and egg deposition on the spider prosoma.     

A New Record of a Host-Parasitoid Interaction: Hymenoepimecis veranii Lofredo & Penteado-Dias, 2009 (Hymenoptera: Ichneumonidae) Parasitizing Araneus orgaos Levi, 1991 (Araneae: Araneidae)

The genus Hymenoepimecis only occurs in the Neotropics. In some species of this genus, the larval stage modifies the behavior of the spider hosts, inducing then to construct a modified web. The wasp Hymenoepimecis veranii has been previously described as an ectoparasitoid of the spider Araneus omnicolor. This study provides detailed information about the natural history of the host-parasitoid interaction involving this wasp with a new host, the spider Araneus orgaos (Araneae: Araneidae), which occurs sympatrically with A. omnicolor.     

Possible Causes of Variation in Territory Tenure in a Lekking Pompilid Wasp (Hemipepsis ustulata) (Hymenoptera)

Territorial males of the pompilid wasp Hemipepsis ustulata occupy their landmark territories for from less than 1 day to several weeks. Variation in territory tenure could arise if territories differ in their value and cost to defend (the tradeoff hypothesis). If superior sites attract more male competitors, raising the cost ofterritorial defense of these locations, we would expect (1) tenure times to be shorter at top-ranked sites and (2) tenure times to decline in years of high male density and competition. Although mean tenure times for males able to hold territories for at least 2 days were shorter at top-ranked sites, the difference was only statistically significant in one of three years. In the year of highest male density, a significantly higher proportion of all territorial males failed to hold the top-ranked sites for more than a single day; however, mean tenure duration at all occupied sites did not decline in this year. Thus, the tradeoff hypothesis received only partial support. An alternative hypothesis is that variation in male resource holding power, as reflected in male size or wing condition, contributes to differences in territorial tenure. However, although larger males were more likely to become territorial residents at the top-ranked sites, the duration of tenure at these locations was not positively correlated with body size. In addition, although wing condition declined throughout the flight season in concert with a sharp decrease in the duration of tenure at the top-ranked sites, males with fresher wings did not hold territories longer than males whose wings were in poorer condition when they assumed control of a site.     

Fecundity and sexual size dimorphism of wolf spiders (Araneae: Lycosidae) along an elevational gradient in the Arctic

Fecundity and body size are central fitness-related traits, and their intra-specific responses to environmental variation are receiving increasing attention in the context of climate change. Recent results from Greenland indicate that temporal and spatial variation in body size differences between sexes (sexual size dimorphism) may be widespread among wolf spider species and could be related to climate. Here, we tested whether variation in elevation affected body size of three wolf spider (Araneae: Lycosidae) species in low-Arctic Canada, whether the sexes differed in their response to the cline, and whether changes in local density influenced this relationship. We also tested whether fecundity changed with elevation in two of the species, independent of body size variation. We found a significant sex–elevation interaction for Pardosa lapponica: female size decreased more in response to elevation than that of males. Males and females of Pardosa uintana decreased significantly in size with elevation at a similar rate. Alopecosa aculeata males increased in body size along the gradient while females did not. Pardosa lapponica females, but not P. uintana females, showed significant reduction in fecundity in response to elevation. P. uintana showed significant decreases in body size with increases in its population density. Changes in temperature and potential resource availability along the elevational gradient are probably causing these species- and sex-specific responses. Further summer warming of the region may alleviate current constraints on growth and reproduction of these species although sex-specific responses may affect their population dynamics.     

Intersexual trophic niche partitioning in an ant-eating spider (Araneae: Zodariidae)

Background

Divergence in trophic niche between the sexes may function to reduce competition between the sexes (“intersexual niche partitioning hypothesis”), or may be result from differential selection among the sexes on maximizing reproductive output (“sexual selection hypothesis”). The latter may lead to higher energy demands in females driven by fecundity selection, while males invest in mate searching. We tested predictions of the two hypotheses underlying intersexual trophic niche partitioning in a natural population of spiders. Zodarion jozefienae spiders specialize on Messor barbarus ants that are polymorphic in body size and hence comprise potential trophic niches for the spider, making this system well-suited to study intersexual trophic niche partitioning.

Methodology/Principal Findings

Comparative analysis of trophic morphology (the chelicerae) and body size of males, females and juveniles demonstrated highly female biased SSD (Sexual Size Dimorphism) in body size, body weight, and in the size of chelicerae, the latter arising from sex-specific growth patterns in trophic morphology. In the field, female spiders actively selected ant sub-castes that were larger than the average prey size, and larger than ants captured by juveniles and males. Female fecundity was highly positively correlated with female body mass, which reflects foraging success during the adult stage. Females in laboratory experiments preferred the large ant sub-castes and displayed higher capture efficiency. In contrast, males occupied a different trophic niche and showed reduced foraging effort and reduced prey capture and feeding efficiency compared with females and juveniles.

Conclusions/Significance

Our data indicate that female-biased dimorphism in trophic morphology and body size correlate with sex-specific reproductive strategies. We propose that intersexual trophic niche partitioning is shaped primarily by fecundity selection in females, and results from sex-differences in the route to successful reproduction where females are selected to maximize energy intake and fecundity, while males switch from foraging to invest in mating effort.     

Male-male interactions and their influence on the mating behavior and success in the fountain darter, <Emphasis Type="Italic">Etheostoma fonticola</Emphasis>

Behavioral interactions between individuals of the same sex can affect the outcome of intersexual selection. For this reason, intrasexual selection is oftentimes examined independently from intersexual selection in studies aimed at understanding mating behaviors. However, a more complete understanding of sexual selection effects within a population can only come from exploring both intrasexual and intersexual selection and the potential interactions between the levels of selection. Association preferences in male and female Etheostoma fonticola do not reveal a size preference for same sex or opposite-sex individuals. However, male-male interactions may influence female choice in E. fonticola. We examined whether male E. fonticola that differ in body size exhibit differences in agonistic behaviors and mating success. Larger males do exhibit higher rates of aggressive behaviors and smaller males, in turn, exhibit more defensive behaviors. However, differences between larger and smaller males in male-male interactions did not translate into differences in spawning success. These results suggest that male size influences dominance relationships in E. fonticola but not mating success. There were also no differences between large and small males in mating attempts, which could be an outcome of the year-round breeding season found in this species, females laying eggs singly, or males fertilizing eggs individually.     

The Sex Determination Gene transformer Regulates Male-Female Differences in Drosophila Body Size

Almost all animals show sex differences in body size. For example, in Drosophila, females are larger than males. Although Drosophila is widely used as a model to study growth, the mechanisms underlying this male-female difference in size remain unclear. Here, we describe a novel role for the sex determination gene transformer (tra) in promoting female body growth. Normally, Tra is expressed only in females. We find that loss of Tra in female larvae decreases body size, while ectopic Tra expression in males increases body size. Although we find that Tra exerts autonomous effects on cell size, we also discovered that Tra expression in the fat body augments female body size in a non cell-autonomous manner. These effects of Tra do not require its only known targets doublesex and fruitless. Instead, Tra expression in the female fat body promotes growth by stimulating the secretion of insulin-like peptides from insulin producing cells in the brain. Our data suggest a model of sex-specific growth in which body size is regulated by a previously unrecognized branch of the sex determination pathway, and identify Tra as a novel link between sex and the conserved insulin signaling pathway.     

Sexual Selection in the Water Spider: Female Choice and Male–Male Competition

The water spider Argyroneta aquatica is the only spider spending its whole life under water, and one of the few spider species in which males are larger than females. Previous studies indicated that males can cannibalize females, which is uncommon among spiders. Here we aimed to further test for a potential influence of sexual selection on male body size. We examined the importance of female choice by testing whether females prefer the larger of two simultaneously presented males as mating partners. Further, we examined the influence of male–male competition by comparing the fighting behaviour between large and small males when alone or when together with a female, and we determined the outcome of fights. We found that females approach and choose large males as mating partners, despite the risk of male cannibalism. Additionally, males intensively compete for females, and large males clearly win against smaller ones. Hence sexual selection seems to be important for the evolution of the peculiar sexual size dimorphism of water spiders, as large size is beneficial for males in both the intra‐ and intersexual context. Previous studies have suggested an important role of natural selection in the sex‐specific body size of water spiders, but natural and sexual selection mechanisms apparently work in the same direction, favouring large male size.     

Predation versus resource limitation in survival of adult burrowing wolf spiders (Araneae: Lycosidae)

Summary The influences of food supply and density on adult survival were examined in the burrowing wolf spider Geolycosa rafaelana (Lycosidae), using manipulations of spider populations on eight 400 sq m experimental plots. A total of 110 adult spiders were captured, weighed, marked, and returned to their burrows during April–May 1983. Treatments of (1) food supplementation, (2) density reduction, (3) food supplementation combined with density reduction, and (4) no manipulation (control) were applied to the eight populations, and adult survival and reproduction were monitored during May–October 1983. Survival rates were higher for nonreproducing adult female populations with reduced density, and lower for nonreproducing females in populations with food supplementation. A pompilid wasp, Paracyphononyx funereus, was documented as a parasitoid of G. rafaelana, producing 50%–65% mortality in adult females during winter, and 4–5% mortality in adult females during summer. The observed survival responses were correlated with variations in predation, while parasitism did not appear to be strongly density-dependent.     

Sex ratios in field populations of two parasitoids (Hymenoptera: Chalcidoidea) of Coccus hesperidum L. (Homoptera: Coccidae)

We tested several assumptions and predictions of host-quality-dependent sex allocation theory (Charnov et al. 1981) with data obtained for the parasitoid Metaphycus stanleyi Compere on its host, brown soft scale (Coccus hesperidum L.), in a California citrus grove and in the laboratory. Scales ceased growing after parasitization by M.?stanleyi. Thus, M. stanleyi may gauge host quality (=size) at oviposition. Host size positively influenced adult parasitoid size, and parasitoid size in turn influenced adult longevity of M. stanleyi. However, parasitoid fitness gains with host size and adult size were similar in males versus females. Sex allocation to individual hosts by M. stanleyi depended on host size; females consistently emerged from larger hosts than males. Host size was important in a relative sense; the mean host sizes of females versus males, and of solitary versus gregarious parasitoids varied with the available host size distribution. The offspring sex ratio of M. stanleyi reflected the available host size distribution; the sex ratio of emerging parasitoids varied with the available host size distribution. We did not detect a “critical host size” below which males emerged, and above which females emerged; rather, only females emerged from hosts in the upper size range, and a variable ratio of males and females emerged from hosts in the lower size range. We conclude that the sex ratio of field populations of M.?stanleyi is driven largely by the available size distribution of C. hesperidum. In addition, we tested predictions resulting from theoretical analyses of sex allocation in autoparasitoids with data obtained on Coccophagus semicircularis (Förster) parasitizing brown soft scale in the field. The sex ratio of C. semicircularis was consistently and strongly female biased (ca. 90% females). Based on available theoretical analyses, we suggest that this sex ratio pattern may have resulted from a very low encounter rate of secondary hosts coupled with a strong time limitation in C. semicircularis females. This explanation was the most plausible given constraints stemming from the detection of secondary hosts, their variable location within primary hosts, and their handling times. Finally, the size of hosts which yielded single versus multiple parasitoids, and the sizes of these parasitoids, were compared. These comparisons suggested that: (1) M. stanleyi females gauge host sizes precisely, and in terms of female offspring; thus a fitness penalty is not incurred by females which share a host, while males benefit from sharing a host, and; (2) instances where multiple C. semicircularis emerged from a single host were probably the result of parasitism by different females, or during different encounters by a single female.     

Male morphological variation and the determinants of body size in two Otiteselline fig wasps

The chalcid wasps (Hymenoptera) that develop in fig tree inflorescences(Ficus: Moraceae) have often been used to study alternativereproductive behaviors. However, recent work suggests that suchbehaviors are more complex than previously thought. We investigatedthis in Otitesella longicauda and O. rotunda. In addition toknown dimorphisms in the two species (each have "religiosa"males that use their mandibles to fight for mates in the fig,and "digitata" males that disperse from the fig to mate), wefound that religiosa males below species-specific body sizeswitch points have relatively larger mandibles and are lesssclerotized than those above. Thus, they are actually trimorphic.We suggest that the religiosa morph variation is linked to fighter/nonfighteralternative mating behaviors, with small (nonfighting) maleshaving relatively larger mandibles because they also use themto pull females out of their galls before mating. Also, we investigatedthe determinants of wasp body size, and whether females (foundresses)adjust their offspring allocation strategies according to expectedoffspring size. We found that wasp size is larger in ovariesnear the center of the fig, and more females and fewer religiosamales are laid in such ovaries than in those further away. Thisprobably indicates that foundresses lay females when they areexpected to be large because their fitness is more body size–dependentthan that of religiosa males. We then discuss the implicationsof our findings for the study of alternative reproductive behaviorsand foundress offspring allocation strategies.     

Sex-ratio adjustment in response to local mate competition is achieved through an alteration of egg size in a haplodiploid spider mite

Sex-ratio adjustments are commonly observed in haplodiploid species. However, the underlying proximate mechanisms remain elusive. We investigated these mechanisms in Tetranychus urticae, a haplodiploid spider mite known to adjust sex ratio in response to the level of local mate competition (LMC). In this species, egg size determines fertilization probability, with larger eggs being more likely to be fertilized, and thus become female. We explored the hypothesis that sex-ratio adjustment is achieved through adjustment of egg size. By using spider mites from a large population, we found that females produced not only a higher proportion of daughters under high levels of LMC, but also larger eggs. Moreover, in populations experimentally evolving under varying levels of LMC, both the proportion of females and the egg size increased with LMC intensity. These results suggest that sex-ratio adjustment in spider mites is mediated by egg size, although the causal relationship remains to be tested.     

Maternal defensive behaviors of <Emphasis Type="Italic">Uloborus</Emphasis> sp. (Araneae,Uloboridae): behavioral repertoire and influence of clutch size and female size on female aggressiveness

Maternal care in spiders often involves behaviors associated with the protection of eggs and spiderlings against parasitoids and predators (including conspecifics). The females of several species have been documented to move their egg sacs away from natural enemies or to invest in active defense behaviors against web invaders, such as parasitoid wasps or araneophagic spider species, to protect their brood. In this study, we present observations of protective behavior by Uloborus sp. females carrying egg sacs. We also investigated whether brood size and female size influence female aggressive behaviors and response time against an artificial source of disturbance. Females carrying egg sacs almost immediately perceived and reacted aggressively against the artificial stimulus, whereas females without egg sacs moved away or ran to the web margins, avoiding the source of disturbance. The aggressive response was independent of clutch size and female body size, indicating that all females will risk interacting with potential agents of egg mortality. This systematic response by all females with egg sacs may be important for reducing the incidence of attack by the egg predator wasp Bathyzonus sp. (Ichneumonidae).     

Insemination Capacity and Dispersal in Relation to Sex Allocation Decisions in Goniozus legneri (Hymenoptera: Bethylidae): Why Are There More Males in Larger Broods?

Models considering sex ratio optima under single foundress strict local mate competition predict that female bias will be reduced by stochasticity in sex allocation, developmental mortality of males and limited insemination capacity of males. In all three cases the number of males per brood is expected to increase with brood size. Sex ratio optima may also be less female biased when several mothers contribute offspring to local mating groups or if non‐local mating occurs between members of different broods; again more males are expected in larger broods. In the parasitoid wasp Goniozus legneri (Hymenoptera: Bethylidae), sex allocation has only a small stochastic component, developmental mortality is low and non‐siblings are unlikely to develop in the same brood. However, the number of males per brood increases with the size of the brood (produced by a single mother). We investigated the further possibilities of limited insemination capacity and non‐local mating using a naturalistic experimental protocol. We found that limited insemination capacity is an unlikely general explanation for the increase in number of males with brood size. All males and females dispersed from both mixed and single sex broods. Although most females in mixed sex broods mated prior to dispersal, these data suggest that non‐local mating is possible, for instance via male immigration to broods containing virgin females. This may influence sex ratio optima and account for the trend in male number.     

Adaptiveness of sex ratio control by the pupal parasitoid Itoplectis naranyae (Hymenoptera: Ichneumonidae) in response to host size

Adaptiveness of sex ratio control by the solitary parasitoid wasp Itoplectis naranyae (Hymenoptera: Ichneumonidae) in response to host size was studied, by examining whether differential effects of host size on the fitness of resulting wasps are to be found between males and females. The offspring sex ratio (male ratio) decreased with increasing host size. Larger hosts yielded larger wasps. Male larvae were less efficient in consuming larger hosts than female larvae. No significant interaction in development time was found between parasitoid sex and host size. Larger female wasps lived longer than smaller females, while longevity of male wasps did not increase with increasing wasp size. Smaller males were able to mate either with small or with large females, while larger males failed to mate with small females. Larger female wasps had a greater number of ovarioles and mature eggs at any one time than smaller females, although the number of eggs produced per host-feeding was not influenced by female wasps. Thus, the differential effect of host size on the fitness of males and females exists in I. naranyae. The basic assumption of the host-size model was therefore satisfied, demonstrating that sex ratio control by I. naranyae in response to host size is adaptive.     

Bacterial infections associated with the son-killer trait in the parasitoid wasp Nasonia (= Mormoniella) vitripennis (Hymenoptera: Pteromalidae)

The son-killer (sk) trait in the parasitoid wasp, Nasonia vitripennis, causes the production of very female-biased sex ratios through the mortality of males. Some 80% of all male eggs fail to hatch. The trait is both maternally and contagiously transmitted. Here evidence is presented that the trait is associated with systemic and chronic bacterial infections in adult wasps. Infections develop trans-stadially, originating in the midgut of larvae and subsequently spreading to other tissues, including the brain, fat body, muscles, eyes, and hemocytes. Female reproductive tracts often show infections but infections are absent in male reproductive organs; other sex differences occur as well. The bacteria involved are pleomorphic, with straight rods being the most common form.     

The genetic architecture of behavioral traits in a spider

The existence of consistent individual differences in behavior has been shown in a number of species, and several studies have found observable sex differences in these behaviors, yet their evolutionary implications remain unclear. Understanding the evolutionary dynamics of behavioral traits requires knowledge of their genetic architectures and whether this architecture differs between the sexes. We conducted a quantitative genetic study in a sexually size‐dimorphic spider, Larinioides sclopetarius, which exhibits sex differences in adult lifestyles. We observed pedigreed spiders for aggression, activity, exploration, and boldness and used animal models to disentangle genetic and environmental influences on these behaviors. We detected trends toward (i) higher additive genetic variances in aggression, activity, and exploration in males than females, and (ii) difference in variances due to common environment/maternal effects, permanent environment and residual variance in aggression and activity with the first two variances being higher in males for both behaviors. We found no sex differences in the amount of genetic and environmental variance in boldness. The mean heritability estimates of aggression, activity, exploration, and boldness range from 0.039 to 0.222 with no sizeable differences between females and males. We note that the credible intervals of the estimates are large, implying a high degree of uncertainty, which disallow a robust conclusion of sex differences in the quantitative genetic estimates. However, the observed estimates suggest that sex differences in the quantitative genetic architecture of the behaviors cannot be ruled out. Notably, the present study suggests that genetic underpinnings of behaviors may differ between sexes and it thus underscores the importance of taking sex differences into account in quantitative genetic studies.     

Mate guarding, competition and variation in size in male orb-web spiders, Metellina segmentata: a field experiment

In the common orb-web spider Metellina segmentata, males are more powerfully built with longer legs, although females are heavier because of their egg load. Males guard females before attempting to mate, and there is considerable male-male competition because of the male-biased operational sex ratio. We used a field removal experiment to examine (1) seasonal changes in the average morphology of guarding males and (2) whether there is a pool of small males that is excluded from the webs of females. Morphological measures were subjected to a principal components analysis and changes in PC scores were examined for seasonal effects and the effects of previous removal of males. The size of guarding males (PC1) increased over the season, suggesting that smaller males were increasingly excluded from webs, but the condition of guarding males (PC2) decreased, indicating that energy reserves are depleted because the males gain little access to food during the reproductive season. When guarding males were removed, smaller males were able to take up residence. Our results show that large males have a clear advantage in monopolizing females. We discuss the manner in which selection acts to maintain large male size in this spider.Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.