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.     

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.     

Matriphagy in the hump earwig, Anechura harmandi (Dermaptera: Forficulidae), increases the survival rates of the offspring

Females of the hump earwig, Anechura harmandi, are completely consumed by their offspring at the end of their care (matriphagy). The effect of this matriphagy was assessed by manipulative experiments. Matriphagy led to a delay in the dispersal of the nymphs and an increase in their survival rate. The same results were obtained when mothers were removed and the nymphs were given sufficient food. Females separated from their offspring after larval hatching failed to produce a second clutch, and three-quarters of them did not develop their ovaries. These results suggest that the survival of nymphs and their stay in the nest are dependent on food availability and that A. harmandi females are strictly semelparous.     

Offspring recognition by mother crab spiders with extreme maternal care

Maternal care is provided by several spider species, but there are no reports of mother spiders recognizing their young, which suggests that maternal care can be exploited by unrelated individuals. Diaea ergandros, a crab spider with extreme, sacrificial maternal care, does accept unrelated spiderlings (ca. 43.9% of spiderlings) into its nest in areas of high nest density. However, a field and a laboratory experiment with mother spiders and natural and adoptive spiderlings demonstrated that mothers did recognize their own offspring. Recognition was not expressed in survival as adopted (unrelated) spiderlings had similar survival rate to that of natural offspring. Instead it was displayed in growth; mother D. ergandros caught large prey items for their own offspring, but not for adopted spiderlings, and so natural offspring grew more than adopted spiderlings. Also, mothers produced trophic oocytes, which are important for the sacrificial care that influences spiderling survival, only when they lived with their own offspring.     

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.     

Functional Value of Matriphagy in the Spider Amaurobius ferox

The adaptive value of matriphagy, the consumption of the mother by her offspring, in the sub-social spider Amaurobius ferox (Araneae, Amaurobiidae) was experimentally evaluated in terms of the benefits to the offspring and the costs to the mother. Matriphagy resulted in a 2.5-fold weight gain in the offspring over their initial weight, advancement of their moulting time, and larger body mass at dispersal in comparison with clutches deprived of matriphagy, but otherwise well provisioned with prey. Matriphagous offspring were also more successful at capturing large prey items, had a more extended social period, and a higher survival rate at dispersal. Mothers separated from their broods just prior to matriphagy were able to produce second clutches, effectively producing 33% more viable offspring (compared with the first clutches). However, the estimated reproductive outputs of the alternative maternal strategies (being devoted to the first clutch vs. deserting the first and producing a second one) suggest that mothers of A. ferox that are cannibalized by their broods enjoy greater reproductive success than those that escape cannibalism and produce second clutches.     

Synchronized contractive movement of Amaurobius ferox spiderlings

During the post-matriphagy period, Amaurobius ferox spiderlings (Araneae, Amaurobiidae) show synchronous movement, contracting their bodies simultaneously. This paper describes this behavior for the first time and identifies influencing factors. The spiderlings’ contractions triggered by web vibration caused by intruders result in a strong pulsation of the whole web that a single individual would not be able to induce by itself. Repetition of the contractions was synchronized among individuals (n = 60 clutches). The movement appeared on the first day after matriphagy. The proportion of participants was maximum on the third day post-matriphagy, when on average 60.7% of the individuals were involved; thereafter the synchronicity progressively decreased. The spiderling groups performed contractions at the highest frequency on the fourth day post-matriphagy, and stopped contracting after the second molt. Experiments using mechanical stimuli produced by an electronic vibrator and a cricket’s movement showed that the vibrational intensity of the external stimuli was positively correlated with the number of contractions performed. Nestmate presence increased the number of contractions performed by individuals, and members of densely packed groups showed more contractions per individual than those in less dense groups. Contractions appeared only during the period when the mother was absent (after matriphagy, or when the mother was removed after the first molt of spiderlings and before matriphagy), and the young were not yet capable of capturing prey. Contractions may function as an antipredatory behavior.     

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     

Matriphagy in the Spider Amaurobius ferox (Araneidae,Amaurobiidae): an Example of Mother-Offspring Interactions

In the spider Amaurobius ferox, the mothers are systematically devoured by their young at a fairly constant interval. Observation of broods maintained under normal conditions showed the cannibalistic processes to be achieved within a few hours, in the course of which mothers and offspring appeared to exchange stimulation. In particular, the mothers exhibited ‘solicitation’ behaviours which appeared to activate and synchronize the young. An experiment was carried out to specify the respective role played by the two parties of the dyad in this case of matriphagy. The female's attitude towards the young (‘solicitation’, tolerance or predatory response) appeared to depend on her reproductive state. The attitude of the young towards the female (cannibalism, attraction, or flight) was shown to depend on their stage of development, but also on the female's attitude. These results support the hypothesis that, in A. ferox, matriphagy is regulated by mother-offspring interactions. Such a mechanism could ensure precise tuning of matriphagy in relation to the requirements of the young, and a certain amount of flexibility in reproduction.     

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.     

Trophic egg laying in the spider, Amaurobius ferox: mother-offspring interactions and functional value

Offspring of the spider Amaurobius ferox (Araneae, Amaurobiidae) were provided with trophic eggs of their mother the day after their emergence from the egg sac. This precisely timed egg laying followed after a series of mother-offspring interactions involving specific behaviors. Experiments showed that the trophic egg laying of the mother (providing she is in the appropriate reproductive condition) necessitated not only their presence, but also the stimulating behavior of the spiderlings. By stimulating their mother the spiderlings actually inhibited the normal maturation of the second generation of maternal eggs and prompted the release. Comparing to the trophic egg-deprived clutches, the clutches provided with the trophic eggs developed with higher body mass, earlier moulting and matriphagy. More offspring survived at the matriphagy with the mother normally provisioning the first clutch with trophic eggs rather than with the mother that did not produced the trophic eggs for her first clutch but for her second clutch. By turning her potential second generation into food, the mother increases her reproductive success.     

Maternal exposure to predator scents: offspring phenotypic adjustment and dispersal

Predation is a strong selective pressure generating morphological, physiological and behavioural responses in organisms. As predation risk is often higher during juvenile stages, antipredator defences expressed early in life are paramount to survival. Maternal effects are an efficient pathway to produce such defences. We investigated whether maternal exposure to predator cues during gestation affected juvenile morphology, behaviour and dispersal in common lizards (Zootoca vivipara). We exposed 21 gravid females to saurophagous snake cues for one month while 21 females remained unexposed (i.e. control). We measured body size, preferred temperature and activity level for each neonate, and released them into semi-natural enclosures connected to corridors in order to measure dispersal. Offspring from exposed mothers grew longer tails, selected lower temperatures and dispersed thrice more than offspring from unexposed mothers. Because both tail autotomy and altered thermoregulatory behaviour are common antipredator tactics in lizards, these results suggest that mothers adjusted offspring phenotype to risky natal environments (tail length) or increased risk avoidance (dispersal). Although maternal effects can be passive consequences of maternal stress, our results strongly militate for them to be an adaptive antipredator response that may increase offspring survival prospects.     

Maternal investment in a spider with suicidal maternal care, Stegodyphus lineatus (Araneae, Eresidae)

Providing parental care is costly for the parent, but generally beneficial for the young whose survival, growth and reproductive value can be increased. Selection should strongly favour an optimal distribution of parental resources, depending on the relationship between the costs and benefits for parents and their offspring. Parental care is characterized by trade offs in investment, for example between egg size and number of young or providing resources at the egg stage versus the post-hatching stage. Females of the spider Stegodyphus lineatus (Eresidae) produce a single small brood with small eggs and provide the young with regurgitated fluid and later, with their body contents via matriphagy. We asked whether females adjust the investment of resources differentially into eggs, regurgitation feeding and matriphagy, and how maternal investment affects the size of the young at dispersal. We followed the growth of young of broods in the lab and in the field and manipulated brood size in order to determine the pattern of resource allocation. We found that brood size was positively correlated with body mass: larger females had larger broods. Females provided 95% of their body mass to the young, allocating more resources to regurgitation than to matriphagy. Females provided regurgitated food to the young according to the brood size, providing less food when the brood was reduced. Maternal resources had a large influence on offspring mass at dispersal, which is likely to affect their future fitness. The study shows the importance of the female's body mass and her resource allocation decisions for her reproductive outcome.     

Genetic inhomogeneous Poisson processes describing the roles of an isolated mature tree in forest regeneration

The spatial distribution of genotyped adult plants and offspring can be modeled by genetic inhomogeneous Poisson processes. This paper reports the development of a previously proposed point process model to cover safe site conditions for sapling survival, unknown seed sources and wider ranges of dispersal kernels. Suppose that a species has limited seed dispersal and shade-tolerance, and that young trees are clustered around highly isolated adults. The clustering might be formed solely by dispersed seeds from adults. However, the survival of the offspring might be influenced by shading by the adults crowns. The new genetic processes are applicable to such cases, as demonstrated for a young population of Fagus crenata, a shade-tolerant canopy tree species, in a 55-year-old stand regenerated after shelterwood logging. Isozyme analysis revealed that the regenerating trees were genetically related to the nearest adults, but some were not their respective daughters. The maximum likelihood method has led us to the following regeneration: seeds were dispersed mostly within 20 m of their mothers; two residual adults in the plot had equal female reproductive success; about 10% of offspring even close to the adult were not their daughters; the adults crowns reduced the survival of offspring up to 20–25 m away. However, the degree of model fitting was unsatisfactory. Hence, our models, in principle, can quantify two roles of highly isolated adults: providing seed sources and safe sites, but the case study suggests that other, unknown factors influence F. crenata regeneration after shelterwood harvesting.     

Environmentally-based maternal effects: a hidden force in insect population dynamics?

Summary The nutritional environment of the parental generation of the polyphagous gypsy moth, Lymantria dispar, can significantly influence the growth and reproductive potential of the next generation through environmentally-based maternal effects. In the first experiment, members of the parental generation were reared on red oak trees (Quercus rubra L.) with known defoliation and phenolic levels. Diet in the offspring generation was homogeneous (synthetic diet). With genetic effects accounted for 1) offspring attained greater pupal weights when their mothers fed on trees with higher leaf damage levels, 2) daughters had a shorter prefeeding stage, a trait associated with dispersal tendency, when their mothers experienced higher condensed tannin levels, and 3) sons had lower pupal weights when their mothers experienced greater condensed tannin levels. In the second experiment, members of the parental generation were reared on either red or black oak (Q. velutina) trees. Offspring of each mother were divided among four diets: red oak, chestnut oak (Q. prinus L.), a standard synthetic diet, and a low-protein synthetic diet. The parental host species accounted for 24% of the variation in daughters' development time; offspring diet accounted for 52%. When mothers were reared on black oak rather than red oak, their offspring developed significantly faster when the F1 diet was chestnut oak. Environmentally-based maternal effects can significantly influence the expression of offspring dispersal potential, growth rate, and offspring fecundity. These traits contribute to natality and survival in natural populations and, hence, to population growth potential. Theoretical models of insect population dynamics demonstrate that the presence of a time delay in a density dependent response can induce destabilization. Maternal effects act on a time delay and may participate in the destabilization characteristic of outbreak species.     

Effects of sibling-rearing experience on future reproductive success in two species of callitrichidae

The survival rate for offspring of mothers who either had or did not have previous experience rearing younger siblings was compared in two callitrichid species, Callithrix jacchus and Saguinus oedipus. Offspring of mothers with sibling-rearing experience had a higher survival percentage than offspring of inexperienced mothers in both species. While 50–60% of offspring of inexperienced C. jacchus mothers survived, no offspring of inexperienced S. oedipus mothers survived. The results suggest that sibling-rearing experience is necessary for adequate maternal behavior in S. oedipus, but not necessary to the development of maternal behavior in C. jacchus. Effects of previous sibling-rearing experience of S. oedipus fathers on offspring survival were also examined. Whether the father had rearing experience was not related to the survival of their offspring.     

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.     

Effects of ants,ground beetles and the seed-fall patterns on myrmecochory of Erythronium japonicum Decne. (Liliaceae)

Erythronium japonicum (Liliaceae) inhabits deciduous mesic forests of Hokkaido, northern Japan. Myrmecochory of this species was investigated, especially the dispersal frequency, the effect of seed predators and the seed fall pattern. In the quadrat census using marked seeds of E. japonicum, the ant Myrmica kotokui frequently transported the seeds. However, the frequency of seed removal was low and most seeds were dispersed as little as 1 m or less. The spatial distribution of E. japonicum individuals was nearly random and most seedlings were established 5–20 cm away from the fertile plants, indicating that even this small scale of seed dispersal contributes to avoiding crowding of seedlings. Some arthropods, e.g. springtails, spiders and ticks, hindered seed dispersal by devouring elaiosomes and seeds. Although ground beetle species also damaged seeds and elaiosomes, a few of them exhibited seed removal behaviour. E. japonicum dropped their seeds not all at once but bit by bit, taking 3–6 days to drop all seeds. This seed-fall pattern was effective in raising the frequency of seed removal by ants and reducing seed predation by some arthropods.     

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.     

Early fate of Myristica hypargyraea seeds dispersed by Ducula pacifica in Tonga,Western Polynesia

Abstract Although pigeons from the genus Ducula are considered among the best avian dispersers of large seeds in Asia and the Pacific, little has been documented on their role. The early fate of dispersed and undispersed seeds of the large‐seeded tree Myristica hypargyraea A. Gray was studied in order to understand the advantage of seed dispersal by the Pacific Pigeon, Ducula pacifica Gmelin in Tonga. Frequency of visits by frugivores to fruiting trees and dispersal distance of seeds were measured. Pre‐dispersal vertebrate seed predation was assessed, then post‐dispersal predation was measured over 160 days. Overall, pre‐dispersal seed predation by parrots was low but variable among trees sampled. Most seeds (54.7%) in the study area were estimated to be dispersed by D. pacifica; 79.7% of those ingested were expelled directly beneath conspecific fruiting crowns, 20% were dispersed locally and < 0.3% were dispersed more than 300 m into a different forest type. Flying foxes (Pteropus tonganus Quoy and Gaimard) dispersed very few seeds (0.7%) and all were dropped below fruiting crowns. Between 4% and 39% of dispersed and undispersed seeds were still viable, or had established seedlings after 160 days. Most seeds had been removed or killed by rats, and seed survival was highest for locally dispersed seeds (approx. 20 m from source trees and within the M. hypargyraea forest). Although D. pacifica was the only frugivore observed to disperse seeds into this higher zone of survival, overall they did not confer a great advantage to seed survival since significant numbers of seeds/seedlings also persisted under fruiting crowns (27% under crowns compared with 39% locally dispersed). Nevertheless, D. pacifica was the only vector by which seeds were regularly moved within the M. hypargyraea forest and over longer distances, and hence, D. pacifica still plays a significant role in the regeneration of M. hypargyraea.