Production and perception of sex differences in vocalizations of Wied's black‐tufted‐ear marmosets (Callithrix kuhlii)

Males and females from many species produce distinct acoustic variations of functionally identical call types. Social behavior may be primed by sex‐specific variation in acoustic features of calls. We present a series of acoustic analyses and playback experiments as methods for investigating this subject. Acoustic parameters of phee calls produced by Wied's black‐tufted‐ear marmosets (Callithrix kuhlii) were analyzed for sex differences. Discriminant function analyses showed that calls contained sufficient acoustic variation to predict the sex of the caller. Several frequency variables differed significantly between the sexes. Natural and synthesized calls were presented to male–female pairs. Calls elicited differential behavioral responses based on the sex of the caller. Marmosets became significantly more vigilant following the playback of male phee calls (both natural and synthetic) than following female phee calls. In a second playback experiment, synthesized calls were modified by independently manipulating three parameters that were known to differ between the sexes (low‐, peak‐, and end‐frequency). When end‐frequency‐modified calls were presented, responsiveness was differentiable by sex of caller but did not differ from responses to natural calls. This suggests that marmosets did not use end‐frequency to determine the sex of the caller. Manipulation of peak‐and low‐frequency parameters eliminated the discrete behavioral responses to male and female calls. Together, these parameters may be important features that encode for the sex‐specific signal. Recognition of sex by acoustic cues seems to be a multivariate process that depends on the congruency of acoustic features. Am. J. Primatol. 71:324–332, 2009. © 2008 Wiley‐Liss, Inc.     

Serum levels of prolactin during the ovarian cycle,pregnancy, and lactation in the common marmoset (Callithrix jacchus)

A homologous double-antibody radioimmunoassay developed for humans was used to measure serum prolactin, progesterone, and estradiol in common marmosets. In the ovarian cycle of common marmosets, serum progesterone began to increase after an estradiol surge, attained a peak level, and then declined before the ensuing pre-ovulatory rise in estradiol. During the luteal phase, the change in serum concentrations of estradiol was synchronized with that of progesterone. During the ovarian cycle there was no consistent change in serum prolactin concentrations. During the last 75 days of pregnancy the prolactin level was higher than during the ovarian cycle and the first 70 days of pregnancy. Moreover, during lactation, mothers with suckling twin infants had a higher prolactin level than during the final stage of pregnancy.     

Neonatal behavioral scoring of common marmosets (Callithrix jacchus): relation to physical condition and survival

A seven-task behavioral test was performed on 86 common marmoset (Callithrix jacchus) infants, 24-36 h following birth. This report describes the test outcome and its relation to physical condition and survival of the infants. The percentage of infants receiving a perfect score on a given task ranged from 30.6 (rooting) to 70.6% (grasping). Heavier infants were more likely to have perfect scores for crawling (F=4.20, P=0.044) and infants with a longer knee-heel length tended to be more likely to have a perfect grasping score (F=3.63, P=0.06). While the modal score was a perfect score for most individual tasks, the modal number of total perfect scores that a given infant received was 3-4 and only 4.7% of infants received perfect scores on all seven tasks. These results suggest that this group of behavioral tasks will produce a variable response within a population of neonates. While no individual behavioral score predicted survival during week 1, the number of perfect scores across all tasks was predictive of survival outcome; infants with a higher total number of perfect scores were more likely to survive (F=6.02, P=0.018). When all combinations of tests were compared, the best predictor of survival was outcome on four of the seven tests, all related to motor skills (F=7.46, P=0.009).     

Hormonal changes related to paternal and alloparental care in common marmosets (Callithrix jacchus)

The physiological mechanisms of parental and alloparental care in cooperatively breeding nonhuman primate species such as the common marmoset (Callithrix jacchus) are poorly known. In this study, we examined prolactin and cortisol plasma levels of fathers and older offspring of both sexes, with and without previous experience in infant carrying, around parturition and during infant carrying. Blood samples were collected from fathers and older offspring and prolactin and cortisol were measured by RIA and EIA, respectively. Prolactin levels of both caretakers were not influenced by infant's birth, previous experience or proximity to parturition. However, prolactin levels increased in both caretakers while in physical contact with infants and also with the number of infants being carried in older offspring. These findings suggest that increased prolactin seems to be mainly due to physical effort rather than a physiological trigger of paternal and alloparental care in common marmosets. Cortisol levels were higher for experienced fathers shortly before parturition which could act to reinforce affiliative bonds between breeding males and females at this time or in the ability of males to detect the proximity of the parturition or both.     

Treatment with CRH-1 antagonist antalarmin reduces behavioral and endocrine responses to social stressors in marmosets (Callithrix kuhlii)

Corticotropin-releasing hormone (CRH) has multiple roles in coordinating the behavioral and endocrine responses to a host of environmental challenges, including social stressors. In the present study we evaluated the role of CRH in mediating responses to a moderate social stressor in Wied's black tufted-eared marmosets (Callithrix kuhlii). Male and female marmosets (n=14) were administered antalarmin (a selective CRH-1 receptor antagonist; 50 microg/kg, p.o.) or vehicle in a blind, counterbalanced, crossover design. One hr after treatment, marmosets were separated from long-term pairmates and then housed alone in a novel enclosure for 7 hr. Behavior was recorded during separation and upon reunion with the partner, and urine samples for cortisol assay collected before, during, and after the intervention. Separation from partners elevated urinary cortisol concentrations over baseline for both conditions, but antalarmin treatment reduced the magnitude of the elevation. Antalarmin also lowered rates of behavioral patterns associated with arousal (alarm and "e-e" vocalizations, object manipulate/chew), but had no effect on contact calls, locomotory activity or alertness. Although most patterns of social behavior upon reunion with the partner were not affected by antalarmin, antalarmin-treated marmosets displayed more sexual behavior (mounts and copulations) upon reunion. These data indicate that antagonism of the CRH-1 receptor acts to reduce the magnitude of both endocrine and behavioral responses to a moderate social stressor without causing any overall reduction in alertness or general activity. This supports the hypothesis that CRH, acting through its type 1 receptor, is involved in coordinating the responses to anxiety-producing events. These results further suggest that the marmoset is a useful model for exploration of the role of CRH in mediating the behavioral and neuroendocrine responses to psychosocial stressors, particularly in the context of heterosexual social relationships.     

Fertility status,dominance, and scent marking behavior of family-housed female cotton-top tamarins (Saguinus oedipus) in absence of their mothers

The effect of the mother's absence on the fertility status and expression of scent marking behavior was examined in 12 sexually mature female cotton-top tamarins (Saguinus oedipus) living in four motherless families. Behavioral data and urine samples were collected on an average of five times per week and levels of estrone-glucuronide (E1G) were quantified directly by radioimmunoassay to establish whether the females showed ovarian cyclicity. Of the 12 females investigated only the dominant female in each motherless group exhibited regular E1G cycles. By contrast, low and acyclic hormonal profiles were found for subordinate sisters. In addition to differences in the patterns and levels of E1G, scent gland morphology and rates of scent marking differed between females: dominant, cycling females had elaborate glands and significantly higher rates of scent marking than subordinates. These results indicate that the presence of the mother (breeding female) is one important factor regulating ovarian function in cotton-top tamarin daughters. The findings also show that dominance status is a vital determinant of each female's subsequent physiological reproductive competence, with only the dominant female obtaining complete fertility and probably inhibiting ovulatory activity in her subordinate sisters. Scent marking behavior seems to be involved in the regulation of this phenomenon of intrasexual reproductive competition.     

Exploratory behavior and learning in laboratory marmosets (Callithrix jacchus jacchus): Comparisons between experimental-cage and home-cage activity

In this paper I examine exploratory behavior and learning in two groups of common marmosets (Callithrix jacchus jacchus), both living under laboratory conditions. The main aim of my studies was to compare behavior occurring in an experimental testing situation with home-cage behavior, and to assess conditions under which exploration is enhanced. One group of marmosets was tested individually in an experimental room away from a larger animal holding room, and a second group was observed in their own home cages, surrounded by other marmosets. Marmosets in both groups were given the opportunity to learn simple tasks, such as pressing a lever for food or jumping on to a wire grid to open a door and see a neighbouring marmoset, and were provided with sets of novel or familiar objects to encourage play and exploration. In the isolated experimental cage, marmosets which learnt a lever-pressing task showed higher general activity levels than controls; in the home cages the mere addition of novel objects resulted in enhancements in exploratory behavior (measured in terms of contacts with the objects). Although the activities associated with learning tended to decline over time, the novel objects remained a constant interest throughout the experiment. The results have implications for maintaining marmosets in captivity, especially in situations when they are housed separately.     

Effects of reproductive status on behavioral and endocrine responses to acute stress in a biparental rodent, the California mouse (Peromyscus californicus)

In several mammalian species, lactating females show blunted neural, hormonal, and behavioral responses to stressors. It is not known whether new fathers also show stress hyporesponsiveness in species in which males provide infant care. To test this possibility, we determined the effects of male and female reproductive status on stress responsiveness in the biparental, monogamous California mouse (Peromyscus californicus). Breeding (N = 8 females, 8 males), nonbreeding (N = 10 females, 10 males) and virgin mice (N = 12 females, 9 males) were exposed to a 5-min predator-urine stressor at two time points, corresponding to the early postpartum (5-7 days postpartum) and mid/late postpartum (19-21 days postpartum) phases, and blood samples were collected immediately afterwards. Baseline blood samples were obtained 2 days prior to each stress test. Baseline plasma corticosterone (CORT) concentrations did not differ among male or female groups. CORT responses to the stressor did not differ among female reproductive groups, and all three groups showed distinct behavioral responses to predator urine. Virgin males tended to increase their CORT response from the first to the second stress test, while breeding and nonbreeding males did not. Moreover, virgin and nonbreeding males showed significant behavioral changes in response to predator urine, whereas breeding males did not. These results suggest that adrenocortical responses to a repeated stressor in male California mice may be modulated by cohabitation with a female, whereas behavioral responses to stress may be blunted by parental status.     

Mate feeding, offspring investment, and sexual differences in katydids (Orthoptera: Tettigoniidae)

Food stress in the katydid Requena veriicalis (Orthoptera: Tettigoniidae)decreases the relative availability of males able to supplynutritious spermatophores to females and increases the valueof the male courtship meal (i.e., relative male parental investment).These changes cause female sexual competition in katydid populations.Here we examine the effect of food stress on male and femaleinvestment in single offspring and test the prediction thatmale-derived nutrients in eggs increase relative to nutrientsfrom the female's reserves. We varied the diet of female R.veriicalis and determined the fate of nutrients from male andfemale sources using I4C and 3H radiolabeled amino acids. Low-dietfemales retained more nutrients from male and female sourcesin somatic tissues and invested less in reproduction both becausethey produced fewer eggs and because they invested less peroffspring (egg) than females maintained on a high-quality diet.Moreover, opposite to our prediction, relative male investmentin individual eggs decreased in foodstressed females; femalesretained more nutrients in somatic tissues from the male sourcethan the female source. Food-stressed females may retain nutrientreserves, particularly those from the male, as an adaptive trategyfor immediate survival needs and future reproduction. Such afemale strategy is unlikely to compromise male reproductivesuccess; first-male sperm precedence means that males matingwith virgin females are likely to father most eggs laid, evenin future reproductive bouts. The decrease in male investmentin eggs of low-diet females does not conflict with the contentionthat relative parental investment controls male intrasexualcompetition because, in mate-feeding species, male investmentinfluencing this competition includes more than investment incurrent offspring; females should compete for males if courtshipgifts aid survival and later reproduction.     

Relative male and female contributions to the supercooling point of their offspring in Microvelia reticulata (Heteroptera: Veliidae)

Cold hardiness is a key life history trait in temperate and polar ectothermic species, as it affects survival during overwintering, but its evolution is poorly understood. While many studies of cold hardiness in insects have shown differences between species, populations or developmental stages, data on the relative contribution of individual genotypes to cold hardiness are scarce and mainly limited to drosophilid fly species. We used a sib‐analysis (paternal half‐sib/full‐sib breeding design) to estimate the relative contributions of parental generation to the supercooling point (SCP) of the offspring of a heteropteran non‐model insect species, Microvelia reticulata (Heteroptera: Gerromorpha: Veliidae). We found that parent identity affected significantly SCP values of their offspring. Magnitudes of estimated sire and dam variance components were similar but the distributions of individual contributions to SCP differed between sires and dams, which points to sex‐specific genetic or parental effects on SCP in this species. The animal model failed to find a realistic estimate of heritability (h²) of SCP, suggesting that the underlying genetics of SCP in M. reticulata can not be characterized by purely additive effects.     

Extrapair paternity in the blue tit (Parus caeruleus) : female choice, male charateristics, and offspring quality

Extrapair paternity is common in many birds, and it is now generallyaccepted that female choice plays an important role. However,die benefits that females obtain from extrapair paternity aremuch less dear. To test the hypothesis that females obtain indirectfitness benefits, we studied paternity in a blue tit populationover 4 years. Extrapair paternity occurred in 31-47% of allnests and accounted for 11-14% of all offspring. Most malesthat fathered extrapair young did not lose paternity themselves,males never "exchanged" paternity, and within nests the extrapairoffspring were usually fathered by a single male. Comparisonsbetween males that did and did not lose paternity and pairwisecomparisons between the extrapair male(s) and the within-pairmale showed that successful males had longer tarsi and sangon average longer strophes during the dawn chorus. Successfulmales weighed less (relative to their size) during the nettlingstage, but nevertheless they survived better. Male age did notinfluence their likelihood of losing paternity, but extrapairmales were usually older than the within-pair male they cuckolded.Within nests with mixed paternity, extrapair young were morelikely to survive than within-pair young in cases of partialbrood mortality. Our data also suggest that extrapair offspringwere more likely to be males. Because extrapair males were usuallyclose neighbors, male quality should be considered relativeto the quality of the neighbors. Despite this, we found consistencyin female choice over years. Our observations provide supportfor the hypothesis that female blue tits engage in extrapaircopulations to obtain good genes for their offspring.     

樟叶蜂两性生殖与孤雌生殖方式下雌虫生殖适合度及子代生活史特征的比较

【目的】樟叶蜂Mesoneura rufonota是危害樟树Cinnamonum campora的重要食叶性害虫,该虫的繁殖策略包括两性生殖和孤雌生殖两种模式。本研究旨在明确孤雌生殖在樟叶蜂生活史中的生物学意义。【方法】在室内25℃恒温条件下,测定并分析了樟叶蜂孤雌生殖和两性生殖两种生殖方式在亲代生殖适合度(雌虫寿命、产卵量和卵孵化率)和子代生活史(各虫态发育历期、死亡率、子代性比和产卵量等)特征上的差异。【结果】孤雌生殖的樟叶蜂雌虫寿命显著长于两性生殖的雌虫寿命,而雌虫产卵量和卵孵化率在两种生殖方式间均无差异。子代各虫态的发育历期和死亡率以及子代单雌产卵量在两种生殖方式间均无差异,但子代成虫性比在两种生殖方式间存在显著差异,表现为孤雌生殖大多产雄性子代,而两性生殖大多产雌性子代。【结论】樟叶蜂的孤雌生殖延长了亲代雌虫的寿命,且为产雄孤雌生殖。这些研究结果表明,樟叶蜂的孤雌生殖不但具有自身建群的能力,同时在种群繁衍中可以提供大量的雄虫以弥补两性生殖后代雄性个体的不足。     

Experimental test of female black howler monkey (Alouatta Pigra) responses to loud calls from potentially infanticidal males: effects of numeric odds, vulnerable offspring, and companion behavior

During group defense, the contribution of female black howler monkeys (Alouatta pigra) may help deter male intruders; however, their involvement during natural intergroup encounters is facultative. Experimental playback trials simulating potentially infanticidal males were used to examine whether a female's reproductive investment and/or her group's relative fighting ability would influence her participation in loud call displays. Female howlers never responded to recordings without alpha male accompaniment, but their response patterns did not simply mimic his. For example, unlike alpha males, females with small, vulnerable offspring were no more likely than females without infants to participate in howling displays during playback trials. Further, although females without any small infants in their group got closer to speakers than females living in groups with small infants, males did not respond in the same way. To artificially simulate different "numeric odds" scenarios, recordings of one or three howling males (simulated intruders) were broadcast to females living in groups with 1-3 resident males. Responses were consistent with the hypothesis that females assessed intergroup fighting ability. As in alpha males, the weakest female responses occurred when the numeric odds were against their group. However, whereas alpha males participated most when numeric odds were in their favor, females had the most intense approach responses when the number of defending and intruding males was equal. Females appeared to use a cost-effective strategy, reserving their assistance for when their participation could have the greatest impact.     

Paternal investment in relation to size in the deathwatch beetle,Xestobium rufovillosum (Coleoptera: Anobiidae), and evidence for female selection for large mates

Male X. rufovillosumdonate on average 13.5% of their body weight to the female during copulation. The weight transferred is significantly greater in heavier males and declines in subsequent matings. When virgin females are offered a choice of several mates, they tend to mate with a heavy male. Females appear to be selective during courtship, refusing to mate with light males. Artificial weights attached to males increase the frequency of acceptance as mates by females, but not significantly. The evolutionary origins and significance of a large paternal investment and apparent female selection for heavy mates are discussed.     

Ants in their plants: Pseudomyrmex ants reduce primate,parrot and squirrel predation on Macrolobium acaciifolium (Fabaceae) seeds in Amazonian Brazil

Although plant‐inhabiting ants are known to act as effective deterrents to a variety of vertebrate and invertebrate herbivores, this has been reported only once before for primates, a group better known for their predation of ants. In the present study, we investigated the effects that colonies of Pseudomyrmex viduus ants living in individual Macrolobium acaciifolium (Fabaceae) trees have on the rates of visitation and fruit removal by four taxa of seed‐predating vertebrates: the primate Cacajao melanocephalus ouakary; macaws (Ara spp.); large parrots (Amazona spp.); and the Northern Amazonian red squirrel (Sciurus igniventris). We found that ant presence significantly reduced both rates of visitation and of fruit removal by C. m. ouakary. The same pattern of reduced fruit removal was also observed for other seed predators (parrots, macaws, and squirrels) but not for visitation rates (although this may be a result of the small sample size). This appears to be only the second‐known demonstration of the repellent effect of ants on primates and, indeed, the first for squirrels and psittacine birds. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 260–273.