Adaptive advantages of maternal care and matriphagy in a foliage spider,Chiracanthium japonicum (Araneae: Coubionidae)

I examined the function of maternal care in a foliage spider,Chiracanthium japonicum. Females of this species make breeding nests with rolled-up grass leaves and provide themselves to spiderlings as food at the end of maternal care. By removing mothers from their offspring at 2 different times, the effects of maternal care on egg and spiderling survival rates were estimated separately. Mother attendance greatly improved survival and development of eggs as well as spiderlings. Detailed observations on the fate of immatures in breeding nests with and without their mothers showed lower hatching and spiderling emergence rates when mothers were removed. Furthermore, spiderlings that fed on their mother’s body showed accelerated growth and quickly molted into the 3rd instar with the delay of dispersal. This suggests that matriphagy, or eating the mother, enables spiderlings of this species to disperse at a later instar. Therefore, I conclude that the maternal care of this spider consists of guarding offspring, supporting offspring development and feeding spiderlings.     

Kin recognition in a social spider

Social spiders accept immigrant spiders into their kin-based groups, suggesting that spiders cannot recognise kin and may lose inclusive fitness benefits. A field and two laboratory experiments on Diaea ergandros, a social crab spider, demonstrated that younger and older instar D. ergandros do discriminate siblings, but potential benefits were variable and not equally distributed. First, proportional survival was greater in large groups regardless of the within-group relatedness, so accepting immigrants increases probability of group survival (although relatedness was more important among smaller groups). Second, juvenile D. ergandros ate unrelated spiders instead of siblings when starved, so immigrants might represent a food reserve in times of food shortage. Third, subadult resident, sibling females cannibalised unrelated, immigrant females and their brothers instead of immigrant males when starved, suggesting that subadult female spiders may maximise outbreeding opportunities. These benefits provide selective pressure for groups to accept immigrants, but as benefits are realised differentially, conflict and cooperation will exist within spider groups similar to that shown in other group-living taxa.     

Adaptive advantages of matriphagy in the foliage spider, Chiracanthium japonicum (Araneae: Clubionidae)

Young of the Japanese foliage spider, Chiracanthium japonicum, show matriphagy, whereby they consume their own mothers before dispersal. By removing mothers in the laboratory, I examined the importance of this sacrificial habit for offspring survival and dispersal behavior. Spiderlings that cannibalized their mothers gained weight more than threefold and dispersed from their breeding nests after molting into the third instar. The third-instar spiderlings had relatively longer legs than the previous instars and appeared to be more adapted to a solitary hunting life style. On the other hand, most spiderlings separated from their mothers could not molt into the third instar and dispersed significantly earlier than those with matriphagy. Furthermore, the lack of matriphagy decreased the survival rate of predispersal spiderlings. These results showed that matriphagy of C. japonicum has a great advantage in allowing offspring to disperse at a more developed and active instar. Received: October 23, 2000 / Accepted: March 15, 2001     

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.     

Costs and Benefits of Maternal Care in a Subsocial Spider,Coelotes terrestris

The maternal social spider Coelotes terrestris demonstrates extended care towards its progeny: the mother guards its egg sac for 3–4 weeks, then stays with its young from the time of their emergence until their dispersal about 1 month later. The present investigation evaluates the adaptiveness of these maternal behaviours by comparing the fitness of females performing them with that of females separated from the egg sac or the spiderlings. By protecting their egg sacs from predation and parasites, and by pursuing this task while supplying the young with food, mothers enhance the survival rate and the development of many of their spiderlings. The costs linked with these activities, estimated by the ability to produce another clutch, appear variable according to the stage in the reproductive cycle. In such terms, the egg sac guarding appears to have a low cost in relation to the care given to the spiderlings.     

Factors influencing the evolution of social behaviour in Australian crab spiders (Araneae: Thomisidae)

The social Diaea are non-territorial, periodically-social spiders that do not weave a snare web, a factor considered to be important in spider sociality. Maternal care and heritable retreats are factors common to most group living animals, including social Diaea; suggesting that they are important factors in the evolution of spider sociality. A 4 year survey, along with field and laboratory experiments revealed that mother spiders provided crucial care in the form of a protective Eucalyptus leaf nest and large prey for their offspring. After the mother's death, the nest was inherited and expanded by the offspring. Larger groups built larger, more protective nests, but expended less individual effort doing so, and so survived better than smaller groups.     

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.     

Reproductive state and care giving in Stegodyphus (Araneae: Eresidae) and the implications for the evolution of sociality

Cooperative brood care is a rare phenomenon in spiders and is restricted to a few social species, including three in the genus Stegodyphus. Brood care in Stegodyphus begins with regurgitation feeding followed by matriphagy: the young consume the body fluids of their mother causing her to die quickly. Whether such an extreme form of maternal care can become a communal task should depend on physiological or historical preconditions. I investigated whether femaleStegodyphus lineatus feed young or allow matriphagy according to their own reproductive state. Broods of young of two age classes (2 or 10 days after hatching) were isolated or fostered out to adult females that were unmated, had eggs or had young. Growth and survival of females and broods were followed over 21 days. The timing of matriphagy depended on the interaction between age of young and state of the foster mother. All broods that were fostered out to females with young grew and survived. Two-day-old young did not survive when isolated or fostered out to unmated females, but some survived and gained weight when placed with foster mothers that cared for egg sacs. Young of 10 days of age grew when fostered out to females with eggs but did not grow or lost weight when isolated or fostered out to unmated females. Survival among 10-day spiderlings was relatively high in all groups but differed significantly between treatments (young isolated or fostered out to unmated females or females with eggs) and control (left with the mother). The results show that these spiders will care for young from other females only when they are in the right developmental state. Such a constraint can have important consequences for the evolution of allomaternal care in social species: unless such a mechanism is overcome, nonreproductives cannot help in brood care. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

State-dependent decisions in nest site selection by a web-building spider

Foraging decisions may reflect a trade-off between food intake and safety and can also be influenced by the animal's internal state. Foraging in the web-building spider Stegodyphus lineatus depends on a capture web associated with a retreat (the nest). The relocation of nests, including the take-over of conspecific nests, may be viewed as a foraing decision, which depends on risk of exposure, cost of silk production and hunger state. We investigated a possible state-dependent trade-off in nest site choice of S. lineatus spiderlings. The philopatric nature ofS. lineatus implies a high risk of encounters with potentially cannibalistic conspecifics and a potential loss of inclusive fitness because encountered conspecifics are likely to be kin. To test for state dependence of foraging decisions, we compared preferences of well-fed and hungry spiders for their own nests and those of siblings and nonsiblings. We expected satiated spiders to prefer their own to conspecific nests and hungry spiders to choose the risky option of a conspecific nest. SinceS. lineatus is less aggressive towards kin, we tested the ability of spiders to discriminate kin by silk-bound cues. Because of this reduced aggression, preference for kin nests should be safer than preference for nonkin nests. A strong preference for self-nests demonstrated self-recognition in well-fed spiders. However, neither well-fed nor hungry spiders discriminated between nests of siblings and nonsiblings. Well-fed spiders preferred self-nests to empty chambers, but showed no discrimination between nonself-nests and empty chambers. Hungry spiders showed a reduced preference for self-nests, suggesting that hunger elicits a more risky foraging strategy. A tendency of hungry spiders to adopt the nests of conspecific spiders may reflect a silk-saving strategy. We conclude that S. lineatus spiders show state-dependent decision making in nest site selection. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Male work and sex ratio in social crab spiders

Summary: Biased sex ratios may alter the contribution that individuals of either sex make to group living. Such a possibility has not been examined in social spiders, in part as adult male spider anatomy and behaviour are focussed on mating. Subadult male behaviour was examined in two congener social crab spiders that have similar ecological niches, Diaea ergandros with an equal sex ratio and D. socialis with a female-biased sex ratio. A laboratory experiment that varied sex ratios of groups of subadults of the two species found that nest construction in D. ergandros did not vary with sex ratio, but that of D. socialis did as males did not contribute to nest construction. This may suggest that among social species, biased sex ratios might influence the appearance of drone-like behaviour.     

Maternal inheritance in a subsocial spider: web for collective prey capturing of the young

Construction of a safe refuge is the first step toward the evolution of social organization in spiders. In the case of the subsocial spider Amaurobius Jerox (Araneae, Amaurobiidae), the young remain in the natal nest after consuming their mother's body (matriphagy). The benefit that the young could obtain from the maternal web was investigated in their collective prey capture. The results demonstrated the adaptive value of the maternal web. The prey capturing activity was more effective when the young were allowed to stay on the maternal web than when they used the web constructed by themselves. Maternal web may also provide a better transmission of information on prey state and clutch mates' activities, because more spiderlings were recruited to contact and hold the prey in a shorter period of time than when they were on a spiderling-constructed web. The young's inheritance of the maternal nest is probably one of the crucial ways in which the mother influences the post-maternal social period of the young.     

Lactating Females Do Not Discriminate Between Their Own Young and Unrelated Pups in the Communally Breeding Rodent, Octodon degus

Females in numerous rodent species engage in communal nesting and breeding, in which they share one or more nests to rear their young. A potential cost of communal nesting and breeding is that mothers divert resources to unrelated offspring. One way mothers could avoid this cost is to recognize and favour their own young over unrelated offspring when allocating maternal effort. We assessed whether female degus (Octodon degus), a communally nesting and breeding caviomorph rodent, discriminate between their own and unrelated offspring during lactation. Female degus previously have been shown to distinguish between their own and unrelated pups when exposed to odours from both. We measured pup discrimination based on differences in the retrieval behaviour of females that were in early or intermediate lactation directed towards their own and unrelated offspring; offspring presented were of similar or different age. Before any event of pup retrieval, lactating females spent similar amounts of time and interacted to a similar extent with their own and unrelated pups. During pup retrieval, all lactating females transported both pups to the nest. Neither relatedness to pups, nor pup‐age differences, influenced the order in which pups were retrieved to the nest. Dams waited similar amounts of time before retrieving the first pup when the first transported young was their own or unrelated. Likewise, females waited similar amounts of time before retrieving the second pup when the pup transported first was their own or unrelated. The time between first and second pup transport events was longer when dams were in early when compared with intermediate lactation, but only when pups were of similar age. All experimental subjects nursed unrelated pups after they were retrieved. Collectively, our results do not support the hypothesis that communally breeding female degus use their recognition ability to discriminate against unrelated offspring in favour of their own young.     

Differential Growth of Own and Alien Pups in Mixed Litters of Mice: A Role for Genomic Imprinting?

Female mice are said to be unable to distinguish own from alien offspring and will indiscriminately nurse each other's young in communal nests. Here, we present results of a split‐litter experiment that tested whether offspring growth was affected depending on whether they were nursed by their own or unrelated foster mothers. Pups of reciprocal crosses between C57/B6 and CBA/Ca strains were fostered in mixed litters that consisted half of their natural siblings and half of unrelated littermates of the reciprocal genotype. Analysing the relative growth of the two pup types showed that offspring gained proportionally more weight when nursed by their own mothers than their cross‐fostered litter mates during the period from day 15 until weaning, during which maternal provisioning effort contributes to pup weight gain. Before day 15 of the pups’ life, however, we found no advantage of being nursed by biological mothers, and we suggest that this may be due to the effects of paternally expressed genes in young that mask their maternal identity, thus favouring indiscriminate nursing of all young in a communal nest.     

Offspring dynamics affect food provisioning,growth and mortality in a brood-caring spider

In brood-caring species, family members are faced with a conflict over resource distribution. While parents are selected to adapt the amount of care according to their offspring''s needs, offspring might be selected to demand more care than optimal for parents. Recent studies on birds have shown that the social network structure of offspring affects the amount of care and thus the fitness of families. Such a network structure of repeated interactions is probably influenced by within-brood relatedness. We experimentally manipulated the group composition in a brood-caring spider to test how the presence of unrelated spiderlings affects the dynamics between female and brood as well as within broods. Broods consisting of siblings grew better and had a lower mortality compared with mixed broods, no matter whether the caring female was a genetic or foster mother. Interestingly, we found that foster mothers lost weight when caring for sibling broods, whereas females caring for mixed broods gained weight. This indicates that females may be willing to share more prey when the brood contains exclusively siblings even if the entire brood is unrelated to the female. Resource distribution may thus be negotiated by offspring dynamics that could have a signalling function to females.     

Chemical mediation of reciprocal mother–offspring recognition in the Southern Water Skink (Eulamprus heatwolei)

Abstract Kin recognition has been demonstrated to play an important role in the social structure of a wide range of animals. Most studies to date have examined parent–offspring recognition only in species that provide offspring with direct parental care, however, there are several advantages to parent–offspring recognition even in the absence of direct parental care. In this study we investigated reciprocal mother–offspring recognition in the Australian scincid lizard Eulamprus heatwolei, a species that does not show direct parental care. We examined whether neonates could discriminate between their mothers and unrelated females, and whether females could discriminate between their offspring and unrelated neonates, via chemical cues, using retreat site selection experiments. We conducted trials when neonates were 1 and 4 weeks old to investigate whether responses are maintained as neonates age. We found that both neonates and mothers could discriminate between related and unrelated individuals when neonates were 1 week old. Mothers were more likely to take refuge under tiles treated with the odours of their own offspring, while neonates spent less time in areas treated with the odours of unrelated females. At 4 weeks of age, mothers no longer exhibited discriminatory behaviour between their offspring and unrelated neonates, while neonates were more likely to associate with the odour of any female over the odourless control. We hypothesize that reciprocal mother–offspring recognition in E. heatwolei reduces interference competition between mothers and their offspring and also may be important in habitat selection and territory establishment.     

Adoption by captive parturient rhesus macaques: Biological vs. adopted infants and the cost of being a “twin” and rearing “twins”

Four rhesus macaque (Macaca mulatta) mothers each spontaneously adopted and reared an abandoned, unrelated neonate in addition to their own neonate. Data on relative time spent in maternal contact and who maintained proximity were collected for the biological and adopted “twins” and singleton control infants using focal animal sampling. Infant weight gain and the subsequent conception history for each mother were obtained for the following year. Biological infants spent more time in maternal contact than their adopted “twin” siblings. When in contact with their mothers, biological “twins” spent more time in the ventro-ventral position and more ventral time alone than adoptees. Mothers initiated more contacts with their biological infants than their adopted infants, suggesting these differences may be due to differential maternal behavior. “Twins” gained weight at a slower rate than singletons, and mothers rearing “twins” produced significantly fewer offspring the following season. Am. J. Primatol. 43:259–264, 1997. © 1997 Wiley-Liss, Inc.     

Relationship between reproductive resource allocation and resource capacity in the matriphagous spider, <Emphasis Type="Italic">Chiracanthium japonicum </Emphasis>(Araneae: Clubionidae)

Females of the Japanese foliage spider, Chiracanthium japonicum, are eaten by their offspring at the end of the maternal care period. To examine the patterns of allocation of maternal investment to their offspring associated with female resource capacity, the amounts of female body reserves accumulated before oviposition, reproductive components at the egg-production phase and those at the matriphagy phase were measured using an artificial breeding nest. Regardless of size, female bodies were completely consumed by the offspring, and larger females, i.e. those having larger reserves, produced a larger number of offspring, but not larger offspring. Furthermore, the proportion of reserves allocated to egg production was not affected by the total amount of the reserves, which indicated that the females systematically divided the resources for individual offspring between egg yolk and food for the growth and survival of the offspring. These results suggest that C. japonicum females adjust egg production to their own resource capacity so that they can achieve an investment per individual offspring which is not dependent on resource capacity. Electronic Publication     

Alloparental Care in the African Striped Mouse Rhabdomys pumilio is Age‐Dependent and Influences the Development of Paternal Care

Alloparents contribute to offspring care and alleviate the workload of breeders. The help provided varies with the age and/or experience of helpers, but it is not known whether breeders vary their investment based on the age of helpers by adjusting the parental care they provide. We studied the alloparental care provided by juvenile and subadult philopatric daughters in biparental African striped mice Rhabdomys pumilio with and without the mother as a measure of alleviation of maternal workload. We showed in a previous study that alleviation of maternal workload directly affects the development of paternal care in their sons, so we studied the expression of paternal care in young males raised by helpers as a proxy of the long‐term consequences of helping. Both juvenile and subadult daughters provided care but the level of alloparental care and concomitant alleviation of maternal care was age‐dependent. In the absence of the mother, juvenile daughters provided just 6% of care compared with 24% of subadult daughters. Sons raised by mothers and juvenile helpers displayed the expected exaggerated levels of care also observed when mothers raise litters on their own. While our results show the direct value of subadult daughters, juvenile daughters could contribute indirectly (e.g. nest maintenance) to alleviating maternal workload. The development of paternal care indicates that mothers do distinguish between the care provided by different aged helpers. Overall, the type of alloparental care provided by female striped mice is expected to change over their lifetimes, resulting in increased inclusive fitness through caring for siblings and acquisition of parenting skills.     

Kinship Influences Cannibalism in the Wolf Spider, Pardosa milvina

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.     

Major benefits of guarding behavior in subsocial bees: implications for social evolution

Parental care is a behavior that increases the growth and survival of offspring, often at a cost to the parents' own survival and/or future reproduction. In this study, we focused on nest guarding, which is one of the most important types of extended parental care; we studied this behavior in two solitary bee species of the genus Ceratina with social ancestors. We performed the experiment of removing the laying female, who usually guards the nest after completing its provisioning, to test the effects of nest guarding on the offspring survival and nest fate. By dissecting natural nests, we found that Ceratina cucurbitina females always guarded their offspring until the offspring reached adulthood. In addition, the females of this species were able to crawl across the nest partitions and inspect the offspring in the brood cells. In contrast, several Ceratina chalybea females guarded their nests until the offspring reached adulthood, but others closed the nest entrance with a plug and deserted the nest. Nests with a low number of provisioned cells were more likely to be plugged and abandoned than nests with a higher number of cells. The female removal experiment had a significantly negative effect on offspring survival in both species. These nests frequently failed due to the attacks of natural enemies (e.g., ants, chalcidoid wasps, and other competing Ceratina bees). Increased offspring survival is the most important benefit of the guarding strategy. The abandonment of a potentially unsuccessful brood might constitute a benefit of the nest plugging behavior. The facultative nest desertion strategy is a derived behavior in the studied bees and constitutes an example of an evolutionary reduction in the extent of parental care.