Eat or Not to Eat: Reversed Sexual Cannibalism as a Male Foraging Strategy in the Spider Micaria sociabilis (Araneae: Gnaphosidae)

Reversed sexual cannibalism represents an unusual situation in which a male kills and consumes a female. We examined this rare phenomenon in the spider Micaria sociabilis, whose males were observed to regularly cannibalise old females. In this study, we investigated male motivation for such behaviour in the light of ecological conditions such as mate availability and prey availability. We found that male cannibalism is not affected by short‐term starvation but rather by male feeding history during the ontogenetic development in combination with prey availability during the adult stage. Males from the summer generation reached bigger sizes than males from the spring generation and females from both generations. They developed in the period with exceptionally high prey occurrence, but when they reached the adult stage, the prey availability decreased. In this period, we observed the highest frequency of cannibalism, however, only when the sex ratio was female biased. Reversed sexual cannibalism in M. sociabilis seems to represent an advantageous male foraging strategy, which is affected by prey availability and male feeding history, tuned by sex ratio and directed towards females of inferior quality.     

Female fecundity and offspring survival are not increased through sexual cannibalism in the spider Larinioides sclopetarius

Many hypotheses explaining the evolution and maintenance of sexual cannibalism incorporate the nutritional aspect of the consumption of males. Most studies have focused on a fecundity advantage through consumption of a male; however, recent studies have raised the intriguing possibility that consumption of a male may also affect offspring quality. In particular, recent studies suggest prolonged survival for offspring from sexually cannibalistic females. Here, we measured the protein and lipid content of males compared to insect prey (crickets), quantified female nutrient intake of both prey types and finally assessed how sexual cannibalism affects female fecundity and spiderling quality in the orb‐web spider Larinioides sclopetarius. We found no evidence that sexual cannibalism increased fecundity when compared to a female control group fed a cricket. Contrary to previous studies, spiderlings from females fed a male showed reduced survival under food deprivation compared to spiderlings from the control group. Offspring from females fed a male also tended to begin web construction sooner. The low lipid content of males compared to crickets may have reduced offspring survival duration. Whether additional proteins obtained through consumption of a male translate to enhanced silk production in offspring requires further investigation.     

Family Affects Sibling Cannibalism in the Black Widow Spider,Latrodectus hesperus

Adaptive foraging tactics are shaped by genes, the environment and gene–environment interactions. Because of relatively high levels of agonism toward conspecifics, spiders have been a popular focus for behavioral–ecological examinations of conspecific predation, or cannibalism. Surprisingly, studies examining the underlying, proximate assumption that cannibalism in spiders is a heritable trait shaped by interactions between genes and the environment are virtually non‐existent. Here, we examine the influence of family on the expression of sibling cannibalism in the post‐hatching, group‐living phase of an otherwise solitary, web‐building spider, the North American black widow (Latrodectus hesperus). Our results showed significant levels of variation in cannibalistic propensity among 26 sibships, with some families cannibalizing full sibs within 2 d and other families waiting 3 wk before resorting to cannibalism. A similar family‐level effect was evident in measures of sibling cohabitation, voracity toward cricket prey, and development speed. Negative correlations between maternal egg sac investment and offspring cannibalism suggest that this family effect may stem, at least in part, from a maternal effect, although we were not able to directly test the prediction that cannibalism is most common from spiderlings in poor condition. Thus, we present novel data suggesting family effects seem to be responsible for cannibalism in L. hesperus spiderlings; however, future work will be required to disentangle the relative importance of shared genes and shared maternal environment. We discuss several mechanisms that could explain the persistence of family‐level variation in cannibalism, a trait that seems likely to be subject to strong directional selection.     

Does a single meal affect female reproductive output in the sexually cannibalistic praying mantid Iris oratoria?

1. One explanation of the evolution of sexual cannibalism, the female’s consumption of a male during or following courtship or copulation, is that this behaviour increases the female’s fitness. This study tests the assumption that a single meal increases female reproductive output significantly in the sexually cannibalistic praying mantid Iris oratoria L. 2. In 38 mating trials, seven of the females cannibalised the males. In order to augment the number of females that fed, an additional nine females were each fed one cricket nymph at the end of the mating trial. 3. Three measures of female reproductive output – the occurrence of oviposition, the mass of the first ootheca, and the number of eggs in the first ootheca – increased significantly with female feeding condition, which was a reflection of food consumed before the mating trial. Females that copulated later in the season tended to lay lighter oothecae. 4. The females’ consumption of a meal during the mating trial, either a conspecific male or a cricket, did not influence any measure of reproductive output significantly, although possible effects upon subsequent oothecae cannot be ruled out. 5. If, as the present study suggests, a single meal provides a negligible or delayed benefit to female reproductive output, the evolution of sexual cannibalism might lie in alternative explanations, which include possible fitness benefits to cannibalistic females in the nymphal stage or possible paternity benefits to the cannibalised males.     

Physiological costs during the first maternal care in the wolf spider Pardosa saltans (Araneae,Lycosidae)

Many arachnids like other terrestrial arthropods, provide extensive maternal care. Few studies have quantified the underlying physiological costs of maternal care. We investigated how maternal care affects the free-moving wolf spider’s (Pardosa saltans) energy requirements. We described in detail their basic reproduction biology (i.e. carrying cocoon and young) and we evaluated the variation in the females’ energy reserves during maternal care. Our results show that mothers guard eggs until hatching and then guard their spiderlings for 27–30 more days. Laboratory observations indicated that spiderlings start leaving the maternal abdomen gradually 5–7 days after hatching. Females carry an egg sac (cocoon) that can weigh up to 77% of their post-reproduction weight and carry young that weigh 87–100% of their body mass. Females lost weight over time despite regular food intake, while carrying cocoon and young; but their weights increased gradually during the dispersal of young. The contributions of proteins, glucose and triglycerides to maintain females’ energy were calculated. Their energetic state varied during maternal care, in particular lipid levels declined, during the care of spiderlings when the females’ predatory behaviour was inhibited. Our results show that the maternal care provided by P. saltans females is particularly costly physiologically, during the 30 days following egg sac formation and development of spiderlings, even when food is available.     

Effects of the sex of the resident adult and of the sex of the opponent on interactions in Mongolian gerbils (Meriones unguiculatus)

Mated pairs of Mongolian gerbils were rejoined by two of their own young, one of each sex, after periods of separation starting when the young were four or seven weeks old and lasting either one or four weeks. An additional sub-group of litters was separated when six weeks old, for a period of separation of two weeks. In another group of mated-pairs, mated-adults were introduced and observed in the same way. Occurrences of sniffing, opposition and pursuit between each adult and each intruder was noted over a period of one hour.A clear effect of the sex of the resident adult on agonistic behaviour was evident. The adult female develops its agonistics acts sooner than the male i.e. it is more responsive than the male to a short duration of separation from the juveniles. The adult female shows either pursuit or opposition to juveniles but shows almost no agonistic behaviour in the presence of unrelated adults. As for the adult male, its agonistic acts begin to appear after four weeks of separation and persist with very frequent opposition, in adult-adult meetings. The sex of the intruder only appeared to be a significant factor after four weeks of separation. After four weeks of separation, opposition of the adult male to the young male was significantly higher than that to the young female. Sniffing of the young male by the adult female was significantly higher than that of the young female. With the same period of separation, but with opponents of eleven weeks, as well as in meetings of adults, each resident adult had a greater number of interactions with the intruder of the same sex.     

Does Female Personality Determine Mate Choice Through Sexual Cannibalism?

Animal personalities (e.g. consistent across‐context behavioural differences between individuals) can lead to differences in mate choice. However, evidence for this link remains limited. Pre‐mating sexual cannibalism can be a behavioural syndrome (i.e. a suboptimal personality) in which adaptive female aggression towards heterospecific prey spills over on non‐adaptive aggression towards courting males, independently of the female mating or feeding status (i.e. the ‘aggressive spillover hypothesis’, ASH). On the other hand, sexual cannibalism can also be a form of mate choice by which females selectively kill or mate with males depending on the male phenotype. We introduce the hypothesis that the most aggressive females in the population will not only attack males more frequently, but will be less likely to impose sexual selection on males through sexual cannibalism. Assuming that in a field common garden experiment in which females were fed ad libitum the rate of weight gain by a female may reflect her voracity or aggressiveness, we show that in the cannibalistic burrowing wolf spider Lycosa hispanica (formerly L. tarantula), voracity towards heterospecific prey predicts a female's tendency towards sexual cannibalism. Unmated females with higher weight gains were more cannibalistic and attacked males regardless of the male phenotype. On the other hand, females that were less voracious tended to be less cannibalistic, and when they did kill a male, they were selective, killing males in poorer condition and mating with those in better condition. Our results demonstrate that females with different phenotypes (growth rates) differently imposed selection on male condition, tentatively supporting the hypothesis that female aggression levels can spill over on sexual selection through sexual cannibalism.     

Squid egg mops provide sensory cues for increased agonistic behaviour between male squid

Males of many species compete for access to females. In order to avoid performing potentially costly agonistic behaviour for their entire adult lives, many group-living males use environmental cues to limit agonistic behaviour to times when it will be of most benefit. Long-finned squid, Loligo pealeii, live less than a year and aggregate in mixed- and single-sex schools. Adults participate in several spawning events, then die. During spawning events, males actively compete for females. Winning males pair with females, which subsequently lay eggs in communal sites on the ocean floor (‘egg mops’). To determine whether males use sensory cues provided by egg mops to regulate agonistic behaviour, we conducted four laboratory experiments. We measured the agonistic responses of pairs of adult males before, during and after exposure to conspecific egg mops. In three experiments, egg mops were manipulated to provide differing sensory stimuli (tactile, water-borne, visual). The addition of conspecific egg mops to tanks of paired male squid dramatically increased agonistic behaviour above control levels within minutes. Male squid were first attracted to the egg mops visually, but contact with the capsules was necessary to increase agonistic behaviour. After initial contact, agonistic behaviour was almost continuous as long as egg mops remained present, even when squid touched the egg mops infrequently. Visual stimuli seemed important in maintaining elevated agonistic behaviour between egg mop touches. When egg mops were removed from the tank, measured agonistic behaviour declined within minutes. When egg mops were added to the tank while covered by an opaque and porous cover that allowed water-borne stimuli to circulate into the tank, squid did not approach the covered egg mop or show increased agonistic behaviour. This result suggests that water-borne stimuli are not sufficient to increase agonistic behaviour. It is unusual for male agonistic behaviour in any species to be increased by contact with fertilized eggs. In this species, however, egg capsules might signal that sexually mature, receptive females are about to lay eggs. Indirect evidence suggests that mating with a female immediately before she lays eggs increases male paternity. If this prediction is true, the presence of egg mops may indicate the optimal time for male squid to establish mating precedence through agonistic bouts. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Haltung und Zucht der Geißelspinne (Damon variegatus) (Phrynichidae) (Chelicerata: Amblypygi)

In the temporary carboniferous hall of „GONDWANA – Das Prähistorium“ in Germany, whip spiders (Damon variegatus) were kept and bred. 3,3 were purchased from a dealer in summer 2007. The night active spiders were kept together in a terrarium. No aggresions were observed. The animals were fed little locusts, young hissing cockroaches, and crickets. In 2008 courtship display and mating could be observed. The biggest male was the only active one. After 7 days after the intake of the spermatophores all females carried eggsacs under the ophistosoma. Each egg sack contained approximately 25–30 eggs. During the carrying phase only one female feasted on a cricket. 98 days after the egg sack was produced the young spiderlings hatched. The coloration of the spiderlings was completely different from the coloration of the adults. The spiderlings were carried by the female for the next 9 days. Then, the spiderlings moulted and left the female immediately. The adults were now separated from their young. The three groups of spiderlings stayed together in a smaller terrarium. However, each group from each female stayed separate from the others for weeks. The second moulting took place 41 days after the first one. No cannibalism was observed. Obviously Damon variegatus seems to be a spider with a social touch. If the terrarium and the climate conditions inside are adapted to the needs of the whip spiders keeping and breeding is possible. The species is highly attractive to visitors.     

Haltung und Zucht der Geißelspinne (Damon variegatus) (Phrynichidae) (Chelicerata: Amblypygi)

In the temporary carboniferous hall of „GONDWANA - Das Prähistorium“ in Germany, whip spiders (Damon variegatus) were kept and bred. 3,3 were purchased from a dealer in summer 2007. The night active spiders were kept together in a terrarium. No aggresions were observed. The animals were fed little locusts, young hissing cockroaches, and crickets. In 2008 courtship display and mating could be observed. The biggest male was the only active one. After 7 days after the intake of the spermatophores all females carried eggsacs under the ophistosoma. Each egg sack contained approximately 25-30 eggs. During the carrying phase only one female feasted on a cricket. 98 days after the egg sack was produced the young spiderlings hatched. The coloration of the spiderlings was completely different from the coloration of the adults. The spiderlings were carried by the female for the next 9 days. Then, the spiderlings moulted and left the female immediately. The adults were now separated from their young. The three groups of spiderlings stayed together in a smaller terrarium. However, each group from each female stayed separate from the others for weeks. The second moulting took place 41 days after the first one. No cannibalism was observed. Obviously Damon variegatus seems to be a spider with a social touch. If the terrarium and the climate conditions inside are adapted to the needs of the whip spiders keeping and breeding is possible. The species is highly attractive to visitors.     

Adverse effects of fluorescent dust marking on the behavior of western black widow spiderlings

Fluorescent dust marking is commonly employed to identify and track small arthropods for studies of ecology, demography, and behavior. Despite its widespread use, no study to date has empirically tested the suitability of dust marking for studies of spider behavior. Here, we test the effects of fluorescent dust marking on proximity of cohabitation, sibling cannibalism, and non‐cannibalistic mortality of western black widow spiderlings, Latrodectus hesperus Chamberlin & Ivie (Araneae: Theridiidae). Results indicate that dust‐marked spiderlings cohabitated at closer proximities and died sooner than undusted spiderlings due to a greater incidence of cannibalism in the dust‐marked group. Thus, we conclude that fluorescent dust marking significantly affected the cohabitation and cannibalistic behavior of L. hesperus spiderlings. Although few studies have reported adverse effects of dust marking on arthropods, our results should serve as a warning to future studies that normal behavior may be disrupted by the use of these fluorescent dust markers. Therefore, preliminary testing should be routine when determining the suitability of any marking technique for not only new species, but also new life stages and behaviors.     

Contrasting patch choice behaviour by immature ambush predators, a spider (Misumena vatia) and an insect (Phymata americana)

1. Spiderlings of the crab spider Misumena vatia and nymphs of the ambush bug Phymata americana normally ambush prey in flowers, as do the adults. The immatures of M. vatia are more mobile, by ballooning, than the ambulatory but largely sedentary adult female spiders, but the apterous immatures of P. americana are less mobile than the alate adults. The aim of the work reported here was to investigate how immatures, as compared with adults, select sites from which to ambush their prey. 2. Individual immatures of both species were released in experimental arenas with variously manipulated natural stems: normal, with and without leaves, and with and without flowers of three species of plants. 3. The spiderlings and nymphs showed discriminatory behaviour but not in accordance with optimal foraging in either case. The spiderlings chose more leafy stems than any other kind of stem. For the nymphs, the importance of leaves was less marked, food apparently being more important than shelter. 4. Neither of the predators discriminated among flowering stems of Solidago canadensis, Daucus carota, and Cirsium arvense. 5. In other experiments, in which flowered and deflowered stems were located in two separated groups in the arena and the individual was released in a bare area between the two groups, the spiderlings chose either group as predicted by chance but the nymphs showed a slight preference for the flowered sector. Nevertheless, once in either of the groups, the predators showed similar behaviour in choosing leafy stems more often than other stems. 6. Nymphs of P. americana are much more selective than adults but spiderlings of M. vatia are less selective than adult females. These results appear to accord with the time and energy costs of changing hunting sites, walking being slower than flying or ballooning. 7. The results indicate the need to include other parameters, such as enemy‐free space and time spent in not being able to forage, in the analysis of foraging behaviour.     

From sneaker to bourgeois male: Long-term observations on recognized tompot blenny Parablennius gattorugine individuals reveal new information on their biology

The behaviour of the tompot blenny Parablennius gattorugine was studied by underwater observation and photography on the south-west coast of the UK over an 11 year period, with >50 individuals identified at two locations by their distinctive skin markings. Observations showed males engaging in rapid swimming behaviour when approached by a female, and younger males using alternative ‘sneaker’ tactics before becoming ‘bourgeois’ territory-holders. The noninvasive recognition technique also facilitated detailed observations on territory retention (up to 7 years) and agonistic behaviours among both males and females.     

Variation in group cohesion during the maternal social period of a subsocial spider

During the maternal social period, Amaurobius ferox spiderlings (Araneae: Amaurobiidae) show mutual tolerance, group cohesion and cooperation in prey capturing, which are recognized as the main characteristics in the evolution of spider sociality. Measuring spatial volume occupied by the spiderlings within the maternal web, this study investigated variation in group cohesion over the maternal social period, from emergence to dispersal. The results showed that the spatial volume of spiderlings varied greatly during the maternal social period and was associated with the development of the spiderlings. Strong group cohesion appeared to be related to maternal food provision, trophic egg laying and matriphagy. An increase of the spatial volume was obviously observed after matriphagy. The experiment revealed that group cohesion decreased after the second molt. A compact group of spiderlings should facilitate maternal food production at the prompted time, and reduced group cohesion after the second molt might lead to eventual dispersal of A. ferox spiderlings.     

Maternal Care and Infanticide by Males in Helvibis longicauda (Araneae: Theridiidae)

Maternal care in spiders varies from just the construction of a protective silken structure for the eggs and the selection of a safe site to place them, to a long period of association between the mother and spiderlings. Such extended care may involve the active protection from predators and parasitoids, food regurgitation, the production of trophic eggs and even matriphagy. In this study, we describe extended maternal care in Helvibis longicauda (Theridiidae) and evaluate the effectiveness of maternal protection against predators of eggs and spiderlings. We conducted experiments comparing the frequency of egg sac destruction and mortality of spiderlings in the presence and absence of mothers. We also observed the behaviour of the mother and spiderlings during prey capture events and interactions with possible predators. Helvibis longicauda females guard their egg sacs until the emergence of the young and guard the spiderlings for several instar stages, fighting possible predators, including conspecifics. We found that aggressive behaviour by females increased the survival of both eggs and spiderlings in our experiments. Intruder males were the main source of mortality in the absence of females. The benefits of maternal care for the young also include the acquisition of prey items that are captured, immobilized and pre‐digested by the mother. Effective maternal protection and the extended period of supplying food to juveniles probably contribute to the late dispersal of offspring in H. longicauda.     

Social Facilitation of Synchronized Molting Behavior in the Spider Amaurobius ferox (Araneae, Amaurobiidae)

During the social period, molting behavior of the young spider, Amaurobius ferox, is highly synchronized within the clutch. Result of the experimental study suggests that social facilitation among group members increased the synchronization. The duration of the molting period of grouped spiderlings was significantly shorter than that of individually isolated spiderlings. Involving the particular maternal strategy in food supply, this phenomenon might have adaptive values in the maintenance of mutual tolerance among the siblings by decreasing the interindividual difference in development and in the avoidance of cannibalism on molting individuals. This probably will also serve to make the peaceful collective behaviors of the spiderlings in matriphagy and cooperative prey capture during their social period.     

Male aggression,limited female choice and the ontogeny of mating behaviour in the flesh fly Sarcophaga crassipalpis

Previous work has shown that male flesh flies (Sarcophaga crassipalpis Macquart) exhibit an ontogeny of behaviour from eclosion through sexual maturity that includes extensive changes in the expression of aggressive, non‐aggressive interactive and non‐interactive behaviours. To determine how the presence of a female flesh fly influences the manifestation of these behaviours, male flesh flies of different ages post‐eclosion are paired with same‐age females and their behaviours are monitored in a simple arena during a 50‐min observation period. All flies are socially isolated until pairing. Although the levels of expression of aggressive and non‐aggressive interactive behaviours are depressed relative to previous findings in male‐opponent pairs, the ontogeny of aggression still occurs as indicated by a significant increase, with age, in the agonistic behaviour ‘hold’. Similar to male‐opponent pairs and individual males, the performance by males of the non‐interactive behaviours ‘walking’ and ‘standing’ diminishes, whereas ‘upside‐down’ increases with age. By contrast, ‘grooming’ shows a significant age‐related decline. No courtship behaviours are observed in the males, although the aggressive behaviour ‘hold’ is a significant transition to mating. Females show no obvious courtship or rejection behaviours, although the significant increase in ‘upside‐down’ with age could possibly be a behavioural gateway to mating. The results of this study indicate that extensive age‐related changes encompassing the entire behavioural repertoire are intrinsic to male flesh flies and persist under a variety of different social contexts.     

Filial cannibalism in Tilapia mariae

In 152 isolated pairs of Tilapia mariae the parents ate 41% of their broods before these reached the frees-wimming stage. The cannibalized broods were usually eaten at the egg-stage. Most brood-eating was done by the males, as concluded from direct observations and from variation between males (but not between females) in the tendency of eat broods. Cannibalistic behaviour was more common when: 1. the relative weight of female (female weight to male weight) was small (< .4) 2. the relative weight was large (> .7) but not too large (> .85) 3. the female was large (> 70 g) 4. the pair spawned at certain times of the year (outside breeding peaks) 5. the spawn was exceptionally small (less than 100 eggs). In normally sized spawns neither the number of eggs nor the size of the eggs or the spawn could be related to cannibalism. The probability of cannibalism was not altered in the second spawnings of the pairs after an experience of a first unsuccessful spawning. Many of these changes in frequency of cannibalism can be related to the males' expected reproductive success. Thus they possibly reflect an underlying natural adaptive variation which partly has been modified by the aquarium milieu.     

Seasonal aspects of sexual cannibalism in the praying mantis (<Emphasis Type="Italic">Mantis religiosa</Emphasis>)

According to the adaptive foraging hypothesis of sexual cannibalism, females face a trade-off between mating and consuming a courting male. Because male and prey availability can change seasonally, sexual cannibalism may change with season. However, we are not aware of any work examining how sexual cannibalism in insects relates to the time of season. Here, we examined the seasonal pattern of sexual cannibalism and reproductive behaviour in the sexually cannibalistic praying mantis (Mantis religiosa). We repeatedly collected the last instars of praying mantises from the field and brought them up under natural weather and photoperiod, but standardised feeding and socioecological conditions. After the females reached sexual maturity, we allowed all of the females to mate during two mating trials. In comparison to female praying mantises maturing later in the season, early-maturing females were larger but of poorer body condition on the day of a mating trial (20 days after the adult moult). During the first round of mating trials, early-maturing virgin females cannibalised males more frequently than their late-maturing counterparts. In contrast, late-maturing females that mated in the first round of mating trials were more likely than early-maturing, nonvirgin females to be cannibalistic in the second round of mating trials. The latency time until copulation was correlated with a risk of sexual cannibalism and was longer in early-maturing females. Our study suggests that the date of the last (adult) moult plays an important role in the occurrence of sexual cannibalism.     

Sexual cannibalism: high incidence in a natural population with benefits to females

Background

Sexual cannibalism may be a form of extreme sexual conflict in which females benefit more from feeding on males than mating with them, and males avoid aggressive, cannibalistic females in order to increase net fitness. A thorough understanding of the adaptive significance of sexual cannibalism is hindered by our ignorance of its prevalence in nature. Furthermore, there are serious doubts about the food value of males, probably because most studies that attempt to document benefits of sexual cannibalism to the female have been conducted in the laboratory with non-natural alternative prey. Thus, to understand more fully the ecology and evolution of sexual cannibalism, field experiments are needed to document the prevalence of sexual cannibalism and its benefits to females.

Methodology/Principal Findings

We conducted field experiments with the Mediterranean tarantula (Lycosa tarantula), a burrowing wolf spider, to address these issues. At natural rates of encounter with males, approximately a third of L. tarantula females cannibalized the male. The rate of sexual cannibalism increased with male availability, and females were more likely to kill and consume an approaching male if they had previously mated with another male. We show that females benefit from feeding on a male by breeding earlier, producing 30% more offspring per egg sac, and producing progeny of higher body condition. Offspring of sexually cannibalistic females dispersed earlier and were larger later in the season than spiderlings of non-cannibalistic females.

Conclusions/Significance

In nature a substantial fraction of female L. tarantula kill and consume approaching males instead of mating with them. This behaviour is more likely to occur if the female has mated previously. Cannibalistic females have higher rates of reproduction, and produce higher-quality offspring, than non-cannibalistic females. Our findings further suggest that female L. tarantula are nutrient-limited in nature and that males are high-quality prey. The results of these field experiments support the hypothesis that sexual cannibalism is adaptive to females.