Comparison of infant care in family groups of the common marmoset (Callithrix jacchus) and the cotton-top tamarin (Saguinus oedipus)

The involvement of parents and siblings in infant care in similarly composed groups of common marmosets (Callithrix jacchus) and cotton-top tamarins (Saguinus oedipus) was compared during the infants' first 8 weeks of life. The results indicate an earlier infant independence in C. jacchus than in S. oedipus due primarily to a more frequent rejection of carried infants in C. jacchus. There was no species difference in extent of maternal involvment in carrying infants. However, S. oedipus fathers carried infants significantly more often during weeks 5–8 than did C. jacchus fathers. Siblings were generally more involved in infant care at an earlier infant age in C. jacchus than in S. oedipus.     

Maternal care and infant development in <Emphasis Type="Italic">Callimico goeldii</Emphasis> and <Emphasis Type="Italic">Callithrix jacchus</Emphasis>

Callimico goeldii gives birth to single offspring, whereas other callitrichids, including Callithrix jacchus, twin. This study compares maternal effort and infant development in C. goeldii and C. jacchus; it is the first study to look at nursing frequency. Infants were observed from birth for 7 weeks in two captive groups each of C. goeldii and C. jacchus. C. goeldii mothers physiologically invested the same or less than C. jacchus mothers. C. goeldii mothers gained the same amount of weight during pregnancy in absolute terms as did the smaller C. jacchus. This results in a smaller gain in proportion to maternal weight but an equivalent proportional gain on a per fetus basis. C. goeldii mothers nursed their infants less based on duration of nursing bouts compared with C. jacchus mothers. C. goeldii mothers transported their infants exclusively through the first 2 weeks of life, which is longer than C. jacchus mothers, who exclusively transported infants only during the first week of life. As maternal infant carriage declined, other group members transported offspring in both species. C. goeldii infants engaged in independent locomotive sequences later in development and tasted solid foods less frequently than C. jacchus infants when compared at equivalent ages. A single, opportunistic milk sample obtained from a C. goeldii mother when her infant was 48 days old indicates that C. goeldii milk contains gross energy from crude protein within the range of variation observed in Callithrix milk. Despite the similarities in milk quality and prenatal effort in individual fetuses, C. goeldii infants gain weight faster from 0 to 18 months than do C. jacchus infants. A reduction in litter size allows C. goeldii mothers to spend more time carrying their infant and to delay weaning, thereby allowing accelerated infant and juvenile growth rates compared with C. jacchus.     

Age of epiphyseal closure in tamarins and marmosets

Estimates of the chronological age for animals of unknown age provide useful information for medical, demographic, and evolutionary studies. Skeletal development, as indicated by epiphyseal closure, can be used to estimate an animal's chronological age or specify its stage of development. Many studies of Primate skeletal development have used animals of unknown age, with the order of epiphyseal closure providing a relative age for each animal. This study examines the age of epiphyseal closure at 22 epiphyseal sites using animals of known age at death in three calitrichid species (Saguinus fuscicollis, Saguinus oedipus, and Callithrix jacchus). The observed average age of epiphyseal closure is similar in these tamarins and marmosets. There is a significant difference in rate of development between the species. Regression equations can predict the age of unknown animals to within 4.8 months for S. fuscicollis, 8.6 months for S. oedipus, and 7.6 months for C. jacchus (twice the standard error of the estimate). These age estimates allow us to determine if an animal is relatively mature or immature, but are largely unacceptable for studies in which precise age estimates are necessary. The order of epiphyseal closure is similar across 11 monkey species (using additional data from published literature) and supports the suggestion of a general pattern in Primate skeletal development. Am. J. Primatol. 41:129–139, 1997. © 1997 Wiley-Liss, Inc.     

Only mothers feed mature offspring in European Ceratina bees

Parental care directed to adult offspring is uncommon in animals. Such parental care has been documented in Xylocopinae bees (Hymenoptera: Apidae). Moreover, some Ceratina bees (Xylocopinae) are known to feed mature siblings, and feeding of mature siblings is achieved by dwarf eldest daughters when mothers died. These daughters are intentionally malnourished by mothers and usually originate from the first brood cell. Here, we examined the pattern of care provided to young adults in three small European carpenter bees: Ceratina (Ceratina) cucurbitina, C. (Euceratina) chalybea, and C. (E.) nigrolabiata. Observations of nest departures and arrivals were performed to study foraging behavior. We detected intensive foraging behavior of mothers in all three studied species. However, we did not observe regular foraging behavior of daughters in any species. The experimental removal of mothers in C. cucurbitina led to the emigration of young adults and did not initiate foraging activity in daughters. We conclude that the feeding of siblings does not occur in these species unlike in the American species C. calcarata. We detected female-biased sex ratios in the first brood cell in C. cucurbitina and C. chalybea. Female offspring in the first brood cell was smaller than other female offspring only in C. cucurbitina. Our results show that a female-biased sex ratio and the small size of daughters in the first brood cell do not provide sufficient evidence for demonstrating the existence of an altruistic daughter and also that the pattern of maternal investment is not exclusively shaped by social interactions.     

Reproductive experience differentially affects spatial reference and working memory performance in the mother

The transition to motherhood results in a number of hormonal, neurological, and behavioral changes necessary to ensure offspring survival. Once motherhood is established, further neurological and behavioral changes may result with additional parity and mothering. Recent research has shown that motherhood enhances both hippocampal-dependent learning and memory and oxytocin-induced long-term potentiation, suggesting that the hippocampus is affected by mothering. In turn, degree of maternal behavior, either high or low, has been shown to affect spatial learning and memory performance in adult offspring. The present experiment aimed to investigate the effect of reproductive experience (nulli-, primi-, and multiparity and mothering) and degree of maternal behavior on hippocampus-dependent learning and memory in the mother. Results show that regardless of error type, primiparous rats make fewer errors compared to nulliparous rats, while multiparous rats show a trend towards making fewer errors compared to nulliparous rats. In addition, mothers who spend less time licking and nursing offspring had fewer reference memory errors. Perhaps the enhanced learning and memory in the inexperienced, new mother allows her to effectively acquire the suite of maternal behaviors necessary to ensure offspring survival and achieve reproductive success with subsequent reproductive experience.     

The impact of maternal experience on post-weaning survival in an endangered arctic fox population

Behavioural differences in parental care can influence offspring survival through variation in e.g. antipredator behaviour and ability to provide food. In a broad range of species, offspring survival has been found to be higher for experienced females compared to inexperienced first-time breeders. The increase in offspring survival for experienced females has mainly been explained by improved experience in providing food. In this paper, we have studied post-weaning juvenile survival in relation to maternal experience in an endangered population of arctic foxes (Vulpes lagopus) in Fennoscandia. For cubs raised by inexperienced and experienced females, the survival rate was 0.42 (CI 95% ± 0.31) and 0.87 (CI 95% ± 0.08), respectively. There was no difference in body condition between the cubs and no observations of starvation. We suggest that the difference in survival was due to lack of experience to one of the most common predators, the golden eagle (Aquila chrysaetos). Golden eagles were mainly observed on dens with litters where the females were inexperienced first-time breeders. From a conservation perspective, it is therefore important to increase adult survival through actions to enlarge the proportion of experienced breeders.     

Species differences in response to conspecific intruders inCallithrix jacchus andSaguinus oedipus

In this study, the first performed on two species of callitrichid primates under identical conditions, the responses elicited in newly mated individuals by conspecific intruders were compared in four pairs of Callithrix jacchusand four pairs of Saguinus oedipus.Intruders were systematically varied in terms of sex and the social context in which they were met. Clear sexual dimorphism was observed in the behavior of Saguinus oedipus,but the behavior of males and females was less dimorphic in Callithrix jacchus.Males and females of both species showed an increase in agonistic and display behavior in the presence of same-sex intruders, but the mode of behavior varied both with sex and species. Social facilitation, as indicated by increased frequencies of agonistic and display responses in the presence of a mate, was observed only in males of both species. Neither C. jacchusnor S. oedipusdisplayed clear evidence of a monogamous mating system like that of Callicebusor of a polygynous mating system like that of Saimiri.Observed differences in the responses to conspecifics between these two species in the laboratory may be explained by facultative differences in mating systems resulting from differences in ranging and foraging behavior under freeranging conditions.     

Effects of host plant on life‐history traits in the polyphagous spider mite Tetranychus urticae

Studying antagonistic coevolution between host plants and herbivores is particularly relevant for polyphagous species that can experience a great diversity of host plants with a large range of defenses. Here, we performed experimental evolution with the polyphagous spider mite Tetranychus urticae to detect how mites can exploit host plants. We thus compared on a same host the performance of replicated populations from an ancestral one reared for hundreds of generations on cucumber plants that were shifted to either tomato or cucumber plants. We controlled for maternal effects by rearing females from all replicated populations on either tomato or cucumber leaves, crossing this factor with the host plant in a factorial design. About 24 generations after the host shift and for all individual mites, we measured the following fitness components on tomato leaf fragments: survival at all stages, acceptance of the host plant by juvenile and adult mites, longevity, and female fecundity. The host plant on which mite populations had evolved did not affect the performance of the mites, but only affected their sex ratio. Females that lived on tomato plants for circa 24 generations produced a higher proportion of daughters than did females that lived on cucumber plants. In contrast, maternal effects influenced juvenile survival, acceptance of the host plant by adult mites and female fecundity. Independently of the host plant species on which their population had evolved, females reared on the tomato maternal environment produced offspring that survived better on tomato as juveniles, but accepted less this host plant as adults and had a lower fecundity than did females reared on the cucumber maternal environment. We also found that temporal blocks affected mite dispersal and both female longevity and fecundity. Taken together, our results show that the host plant species can affect critical parameters of population dynamics, and most importantly that maternal and environmental conditions can facilitate colonization and exploitation of a novel host in the polyphagous T. urticae, by affecting dispersal behavior (host acceptance) and female fecundity.     

Population differences in host use by a seed-beetle: local adaptation, phenotypic plasticity and maternal effects

For insects that develop inside discrete hosts, both host size and host quality constrain offspring growth, influencing the evolution of body size and life history traits. Using a two-generation common garden experiment, we quantified the contribution of maternal and rearing hosts to differences in growth and life history traits between populations of the seed-feeding beetle Stator limbatus that use a large-seeded host, Acacia greggii, and a small-seeded host, Pseudosamanea guachapele. Populations differed genetically for all traits when beetles were raised in a common garden. Contrary to expectations from the local adaptation hypothesis, beetles from all populations were larger, developed faster and had higher survivorship when reared on seeds of A. greggii (the larger host), irrespective of their native host. We observed two host plant-mediated maternal effects: offspring matured sooner, regardless of their rearing host, when their mothers were reared on P. guachapele (this was not caused by an effect of rearing host on egg size), and females laid larger eggs on P. guachapele. This is the first study to document plasticity by S. limbatus in response to P. guachapele, suggesting that plasticity is an ancestral trait in S. limbatus that likely plays an important role in diet expansion. Although differences between populations in growth and life history traits are likely adaptations to their host plants, host-associated maternal effects, partly mediated by maternal egg size plasticity, influence growth and life history traits and likely play an important role in the evolution of the breadth of S. limbatus’ diet. More generally, phenotypic plasticity mediates the fitness consequences of using novel hosts, likely facilitating colonization of new hosts, but also buffering herbivores from selection post-colonization. Plasticity in response to novel versus normal hosts varied among our study populations such that disentangling the historical role of plasticity in mediating diet evolution requires the consideration of evolutionary history.     

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.     

Direct and transgenerational effects of an experimental heatwave on early life stages in a freshwater snail

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Tradeoff between offspring mass and subsequent reproduction in a highly iteroparous mammal

When resources are limited, current maternal investment should reduce subsequent reproductive success or survival. We used longitudinal data on marked mountain goats Oreamnos americanus to assess if offspring mass at weaning affected maternal survival and future reproduction. Offspring mass was positively correlated with survival of old mothers, suggesting that mothers produced lighter kids, and hence reduced reproductive effort, in their last reproduction. Offspring mass at weaning did not affect survival of young and prime‐aged mothers, but females that had weaned heavy offspring had a reduced probability of subsequent reproduction in years of low population density. Because offspring survival is correlated with weaning mass, mothers’ allocation to reproduction involves a tradeoff between current and future fitness returns. We demonstrate for the first time that allocation to current offspring mass in an iteroparous mammal reduces the probability of subsequent reproduction.     

Persistent maternal identity effects on life history traits in<Emphasis Type="Italic"> Daphnia</Emphasis>

The aim of the present study was to examine the magnitude and persistence of maternal effects in Daphnia, in particular maternal identity effects. I studied life history traits of a single clone of Daphnia galeata born to 40 different mothers belonging to three age groups. Maternal identity had large effects on offspring traits, that is, identically treated clonal females differed substantially in respect to the traits of their offspring, including size at birth, age at maturity, and number of second generation offspring. The effects of maternal identity on these traits were largely independent of maternally induced differences in offspring size, indicating that maternal effects were mediated through offspring quality. Maternal age also affected offspring traits: older mothers gave birth to larger offspring which matured earlier, were larger and more fecund, and survived better until maturity. Individuals which were larger at birth also had a better chance of survival. Contrary to expectation, I found little evidence that maternal identity or maternal age had any influence on their offsprings response to fish kairomones.     

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     

Paternal levels of DNA damage in spermatozoa and maternal parity influence offspring mortality in an endangered ungulate

Understanding which factors influence offspring mortality rates is a major challenge since it influences population dynamics and may constrain the chances of recovery among endangered species. Most studies have focused on the effects of maternal and environmental factors, but little is known about paternal factors. Among most polygynous mammals, males only contribute the haploid genome to their offspring, but the possibility that sperm DNA integrity may influence offspring survival has not been explored. We examined several maternal, paternal and individual factors that may influence offspring survival in an endangered species (Gazella cuvieri). Levels of sperm DNA damage had the largest impact upon offspring mortality rates, followed by maternal parity. In addition, there was a significant interaction between these two variables, so that offspring born to primiparous mothers were more likely to die if their father had high levels of sperm DNA damage, but this was not the case among multiparous mothers. Thus, multiparous mothers seem to protect their offspring from the deleterious effects of sperm DNA damage. Since levels of sperm DNA damage seem to be higher among endangered species, more attention should be paid to the impact of this largely ignored factor among the viability of endangered species.     

Trans‐generational effects of maternal rearing density on offspring development time in a parasitoid wasp

Maternal pre‐reproductive experience can impose phenotypic changes on offspring traits. These modifications may result from physiological constraints, although they can also increase the adaptation of offspring to their anticipated environment. Distinguishing between the two interpretations is often difficult. The effects of virgin female rearing density on their longevity and the characteristics of their male offspring are explored in the polyembryonic parasitoid wasp Copidosoma koehleri (Blanchard) (Encyrtidae: Hymenoptera). High rearing density may adversely affect maternal physiology or, alternatively, act as a cue for anticipated competition during the lives of the mothers and their offspring. Male offspring of group‐reared females reach pupation significantly sooner than male offspring of females reared alone. This accelerated development may provide an advantage when competition from superparasitising individuals is expected. The lifespan of high‐density females is longer than that of singly‐reared females, and their male offspring survive longer, suggesting that crowded rearing does not reduce the fitness of females or offspring. The shortened development time of male offspring may reflect an adaptive epigenetic response to predicted competitive conditions.     

Rethinking the thermal melanism hypothesis: rearing temperature and coloration in pygmy grasshoppers

Selection for efficient conversion of solar radiation to body heat has favored the evolution of dark coloration in many ectotherms. The thermal melanism hypothesis posits that dark coloration is beneficial under conditions of low ambient temperatures because it results in faster heating rates and higher body temperatures. Fast heating rates, however, may come at a cost of overheating unless compensated for by thermal physiology or behaviour. Pygmy grasshopper (Orthoptera, Tetrigidae) populations that inhabit fire-ravaged areas characterized by blackened backgrounds and hot surface temperatures due to high absorbance of solar radiation show an increased frequency of black phenotypes. I raised the progeny of wild-captured Tetrix undulata in cold and hot temperatures and used data on color patterns and survival in a greenhouse to examine whether a cold thermal environment triggered the development of melanic coloration or differently affected survival of melanic versus non-melanic individuals. My results indicate that melanism was not influenced by rearing temperature but by genes or epigenetic maternal effects. Temperature also did not affect survival. However, melanic individuals produced by melanic mothers survived longer than melanic individuals produced by non- melanic mothers, whereas non-melanic individuals produced by non-black mothers survived longer than melanic individuals produced by non-black mothers. This suggests a mismatch between color and physiology in offspring belonging to a different color morph than their mother. Future investigations into the evolution of melanism should consider conflicting selection pressures on thermal capacity and camouflage as well as the influence of correlated responses to selection on traits associated with coloration.     

Performance of Sclerodermus brevicornis,a parasitoid of invasive longhorn beetles,when reared on rice moth larvae

Biological control efficiency can be improved by developing effective mass‐rearing systems to produce large numbers of high‐quality parasitoids. This study explored an alternative host for rearing Sclerodermus brevicornis (Kieffer) (Hymenoptera: Bethylidae), a potential biocontrol agent for the suppression of exotic and invasive wood‐boring longhorn beetle (Coleoptera: Cerambycidae) populations in the European agroforestry ecosystems. We tested larvae of the rice moth, Corcyra cephalonica Stainton (Lepidoptera: Pyralidae), as host for the parasitoid. We quantified the probability and timing of host attack and parasitism as well as reproductive success, offspring production, and the characteristics of adult offspring. As S. brevicornis is a quasi‐social species (multiple females, communally produced offspring broods), we also explored the effects of varying the number of females to which individual hosts were presented, with the aim of determining the optimal female‐to‐host ratio. As time to host attack can be a limiting factor in S. brevicornis rearing protocols, we tested the use of adult females of another bethylid species, Goniozus legneri Gordh, to paralyse C. cephalonica larvae prior to presentation. We identified the conditions within our experiment that maximized offspring production per host and offspring production per adult female parasitoid. We found that C. cephalonica is suitable as a factitious host and, as it is considerably more straightforward for laboratory rearing than cerambycid species, it is a good candidate for adoption by future S. brevicornis mass‐rearing and release programmes.     

Better‐surviving barn swallow mothers produce more and better‐surviving sons

Sex allocation theory predicts that parents are selected to bias their progeny sex ratio (SR) toward the sex that will benefit the most from parental quality. Because parental quality may differentially affect survival of sons and daughters, a pivotal test of the adaptive value of SR adjustment is whether parents overproduce offspring of the sex that accrues larger fitness advantages from high parental quality. However, this crucial test of the long‐term fitness consequences of sex allocation decisions has seldom been performed. In this study of the barn swallow (Hirundo rustica), we showed a positive correlation between the proportion of sons and maternal annual survival. We then experimentally demonstrated that this association did not depend on the differential costs of rearing offspring of either sex. Finally, we showed that maternal lifespan positively predicted lifespan of sons but not of daughters. Because in barn swallows lifespan is a strong determinant of lifetime reproductive success, the results suggest that mothers overproduce offspring of the sex that benefits the most from maternal quality. Hence, irrespective of mechanisms causing the SR bias and mother–son covariation in lifespan, we provide strong evidence that sex allocation decisions of mothers can highly impact on their lifetime fitness.     

Predation risk affects the levels of maternal immune factors in avian eggs

Predation risk is an environmental stressor that can induce changes in prey behavior and physiology. Perception of predation risk may indirectly affect offspring traits and future fitness prospects via impacts on the condition of parents. Females may influence the survival of their offspring via maternal effects, especially when breeding in stressful conditions. We investigated the effects of continuous predation risk perceived by mothers on the maternal allocation of immune factors and carotenoids in eggs of the pied flycatcher Ficedula hypoleuca. We collected eggs from wild pied flycatchers that bred in the vicinity of a predator nest (pygmy owl Glaucidium passerinum), were exposed to cues of a mammalian nest predator (urine of least weasel Mustela nivalis), or received appropriate controls for these two groups. Pied flycatchers transferred more immunoglobulin in eggs under high predation risk in both owl and mammalian predator treatments. The presence of owl nests also lowered the level of lysozyme transferred in the eggs in one of the two study years. Predation risk did not modify egg size or overall carotenoid levels. Our results show that continuous predation risk perceived by females during egg‐laying affects egg composition. This different allocation of maternal immune factors may be an adaptive response evolved to increase the probability of offspring survival.