The response of some prosimian primate mothers to their own anesthetized infants

Six lemur mothers of three different species and oneGalago crassicaudatus mother were observed in the presence of their own anesthetized infants. Two of the lemur mothers spent only very brief periods sitting near their infants and seldom groomed them; the other four spent over half of the infant immobility period in close proximity to their infants and groomed them frequently. Four lemur mothers groomed the ano-genital region of their infant at least once. None of the lemur mothers picked up or carried her immobilized infant, as has been reported for some higher primate mothers, although one lemur mother used her hands to pull the infant toward her ventrum while sitting on the floor. Five lemur mothers rejected their infants when the infants displayed disoriented behavior while emerging from anesthesia. The galago mother retrieved her anesthetized infant in her jaws but dropped the infant several times while attempting to groom it. These results suggest very tentatively that prosimian mothers lack the ability shown by mothers of some higher primate species to improvise protective ways of behaving toward helpless infants.     

Laterality in quadrupedal and bipedal prosimians: Reach and whole-body turn in the mouse lemur (Microcebus murinus) and the galago (Galago moholi)

Lateral preferences in food reaching and whole-body turning were assessed in 24 prosimian primates: 16 galagos (Galago moholi) and 8 mouse lemurs (Microcebus murinus). Reach and turn preference in the galago were examined using a single testing procedure; separate procedures were used to evaluate reach and turn preferences in the mouse lemur. The motoric requirements for both species were 1) reach into a Plexiglas container with a single hand for a food item and 2) execution of a whole-body rotation about the long axis of the body. Twenty-three of the subjects tested had a reach preference (15 right, 8 left preferent) and 22 a turn preference (1 right and 21 left preferent). No correlation between the direction of reach and turn preference was found for either species; however an association between right reach preference and female gender was found for the galagos. A species difference in the strength of lateralization was found, with the more bipedal species, the galago, more strongly lateralized in both measures. This result supports the hypothesis that the assumption of upright posture was an important factor in the phylogenetic development of primate lateralization.     

A case of infant swapping by wild northern muriquis (<Emphasis Type="Italic">Brachyteles hypoxanthus</Emphasis>)

Allo-parenting has been observed in a variety of female primates, and typically infants are reunited with their biological mothers assuming that their mothers are alive. We observed an exception to this pattern when two wild northern muriquis (Brachyteles hypoxanthus) exchanged infants of different sexes and then reared their adopted infants through weaning. The process of this exchange began when the infants were 4 and 8 days old, respectively. The mother of a 4-day old female carried and nursed her own daughter and the 8-day old son of a second female. The exchange ended when the second mother was first observed carrying the wrong infant 1.5 days later. This observation raises questions about the age and mechanisms of mother–infant recognition in this species, and about assumptions of mother–infant relatedness based on behavioral observations alone.     

Differentiation of vocalizations in bushbabies (Galaginae, Prosimiae, Primates) and the significance for assessing phylogenetic relationships

A comparative bioacustic analysis of vocalizations of the prosimian subfamily Galaginae revealed that morphologically similar sibling taxa within the main groups of the lesser galagos and the greater galagos can be reliably identified phenotypically on the basis of the acoustic structure of their loud call or advertisement call. Results confirm the separation of two distinct species of greater galagos, Galago crassicaudatus and Galago garnettii, and strongly suggest the discrimination of three distinct species from the senegalensis lesser bushbaby group, Galago senegalensis, Galago moholi and Galao zanzibaricus. An investigation of the ontogenetic development of the loud call indicated that it is derived from the infant's isolation call, displaying in all studied bushbaby taxa a fairly similar acoustic pattern. Shared acoustic characters of the loud call among the different taxa as well as the infant's isolation call were used to propose a hypothesis about the phylogenetic affinities in bushbabies. The results seem to be supported by recent fossil records.     

Cases of maternal cannibalism in wild bonobos (<Emphasis Type="Italic">Pan paniscus</Emphasis>) from two different field sites,Wamba and Kokolopori,Democratic Republic of the Congo

Maternal cannibalism, whereby a mother consumes her own offspring, occurs in various animal taxa and is commonly explained by nutritional stress or environmental pressures. It is rare in nonhuman primates and is considered an aberrant behavior only observed under high-stress conditions. It was therefore surprising when, in the first reported case of cannibalism in wild bonobos, a mother consumed part of the dead infant at LuiKotale. Here we report two more cases of maternal cannibalism by wild bonobos at two different study sites, Wamba and Kokolopori. The dead infants’ mothers participated in the cannibalism in both cases. At Kokolopori, although the mother did consume part of the carcass, it was held and shared by another dominant female. At Wamba, the mother was a dominant female within the community and was the primary consumer of the carcass. In both cases, cannibalism resembled other meat-eating events, with the dominant female controlling meat consumption. Infanticide was not observed in either case, but its occurrence could not be ruled out. Although rare, the occurrence of maternal cannibalism at three different study sites suggests that this may represent part of the behavioral repertoire of bonobos, rather than an aberrant behavior.     

Avoidance of post-coital cannibalism in the brachyurid paddle crab Ovalipes catharus

Sexual cannibalism was examined experimentally in the New Zealand paddle crab Ovalipes catharus, where it is the female that risks cannibalism during and after sexual activity. In this species copulation only occurs when the female is soft-shelled after moulting and she is most vulnerable to cannibalism. Male paddle crabs protect and copulate with the females until the females are no longer sexually receptive. Males appear able to identify a female with whom they have recently copulated. After a brief separation, significantly fewer females were cannibalized in cases where a female was returned to her original sexual partner than in those that had exchanged partners. The asymmetry, where females gain some protection during moulting but males receive no such advantage, may, at least partially, explain the skewed sex ratios which are sometimes found in samples of O. catharus from nature.     

Isolation of females prior to parturition reduces neonatal mortality in Galago

Eighteen years of birth records for three species of Galago at the Duke University Primate Center were examined to determine the effects of isolation of pregnant females on neonatal mortality rates. Isolation significantly decreased neonatal mortality rates in all three species over neonatal mortality rates in infants born to unisolated females. The frequency of cannibalism of infants did not differ between isolated and unisolated females. Secondary sex ratio differed significantly from 1:1 for all three species, but higher mortality in males in the first 10 days of life resulted in sex ratios that did not differ from 1:1 in G. garnettii and G. crassicaudatus.     

Reproduction in the slow loris (Nycticebus coucang)

The reproductive biology of the slow loris (Nycticebus coucang) is poorly documented because of infrequent captive breeding success and the absence of field studies of this species. Reproductive data were collected from a breeding colony of slow lorises held at the Duke University Primate Center for the past 10 years. Nineteen infants were born, with a sex ratio of 1:1 and a neonatal mortality rate of 15.8%. In all cases, litter size was one. Females born in the colony copulated for the first time between 18 and 24 months of age. A male that reached sexual maturity in the colony sired his first offspring at the age of 17 months. Estrous cycles ranged in duration from 29–45 days, with copulations usually occurring for 1 day of estrus. Gestation length averaged 192.2 days. Although a postpartum estrus was observed in three cases of infant death, no conceptions resulted. Lactation lasted approximately 6 months. A clear birth peak was observed, with 12 out of 19 births occurring in March, April, and May. The comparatively low basal metabolic rate of this species may account for the unusually low reproductive rate of the slow loris in comparison with other prosimian primates.     

Infant survival and litter size in primigravid and multigravid Galagos

Eighteen years of birth records for three species of Galago at the Duke University Primate Center were examined to determine the effect of gravidity status on neonatal mortality and litter size. Multiparous Galago senegalensis moholi and G crassicaudatus, but not G garnettii, had significantly higher infant survival rates. Gravidity status had no effect on the percentage of multiple births for any of the three species of Galago.     

Reproductive failure,possible maternal infanticide,and cannibalism in wild moustached tamarins, <Emphasis Type="Italic">Saguinus mystax</Emphasis>

Maternal infanticide in wild non-human primates has only been reported twice. In this paper, we report a possible new case of infanticide and cannibalism within a series of four successive reproductive failures in wild moustached tamarins, Saguinus mystax. Necropsy and genetic analyses of the corpses enabled us to rule out any pathology, and to determine paternity. The mother was seen biting and then eating the head of its own infant during a period when another female was pregnant and gave birth just 1 month later. Before that, the perpetrator had given birth to twins three times successfully when four to five adult and subadult males were present in the group. Although we do not know for certain that the infant was alive when the mother started biting it, our field observations preceding the event suggest it probably was. The possible infanticide case and the two cases of births and early death of the infants occurred while only two to three adult males were present in the group. This could be the second case of maternal infanticide reported in the genus Saguinus and the similar circumstances suggest a common pattern. We discuss these events in the light of the different functional explanations of infanticide and conclude that parental manipulation was the most likely: the mother could have terminated the investment in offspring that had low chances of survival in a group with low availability of helpers.     

Microhabitat segregation and cannibalism in an endangered freshwater isopod, Thermosphaeroma thermophilum

Intraspecific microhabitat segregation is expected to arise when there are age- or sex-specific differences in predation risk. The degree to which conspecific predation (cannibalism) can generate this risk, however, is poorly understood. In this paper, we examine microhabitat use, cannibalism, and individual responses to the presence of conspecifics in Thermosphaeroma thermophilum, an endangered isopod crustacean species that is endemic to a single, thermal spring in Socorro, N.M. USA. In samples from the natural habitat, juveniles (mancas) were found mainly on vegetation, whereas adults were found predominantly on bottom sediments. Females were found on vegetation more often than males. In laboratory containers without refuges, males cannibalized females, males and females cannibalized mancas, and mancas cannibalized each other, even in the presence of alternative food. When placed in containers provided with refuges, mancas actively avoided adults. We suggest, therefore, that cannibalism in T. thermophilum generates age-, size-, and sex-specific predation risks which are responsible for microhabitat segregation between mancas and adults, and between males and females. Since interspecific predation in the spring is negligible, cannibalism appears to play a significant role in population regulation and behavioral evolution in this species. We recommend, given the current “endangered” status of this species, that microhabitat heterogeneity be maintained in its native spring because it provides refuges from cannibalism and may support a larger and more viable natural population. Received: 28 June 1996 / Accepted: 24 February 1997     

The use of hair morphology in the classification of galagos (Primates, subfamily galagoninae)

The outer epidermal hair structure of bushbabies or galagos varies considerably between genera and species. Comparative morphology can therefore be useful in taxonomic studies, particularly when assessing the true status of newly nominated or misclassified species. Quantitative measurements of outer epidermal hair scales (scale frequency and scale complexity) were made for populations representing 13 taxa within the subfamily Galagoninae. Intraspecific variations in both measures of hair morphology were relatively minor. By contrast, significant interspecific differences were observed, even between closely related, well-established species (e.g. in the greater galagosOtolemur crassicaudatus andO. garnettii and lesser galagosGalago senegalensis andGalago moholi). Assessment of scale frequency resulted in the recognition of all species of the greater and needle-clawed galago genera and added support for nomination to species status of two former subspecies (O. argentatus andE. pallidus). Similar divisions were made in the lesser and dwarf galagos with respect to scale complexity. Possible explanations for the differences in outer epidermal hair scales are discussed. Characteristics of outer epidermal hair scales provide a useful guide to species identity in the subfamily Galagoninae, and the same may prove to be true for other groups of nocturnal mammals.     

Species differences in substrate use and diet between sympatric galagos in two Kenyan coastal forests

Two sympatric species of galago,Galago zanzibaricus andG. garnettii, differed significantly in diet (judged mainly by fecal analysis) and substrate use at each of two coastal forest sites in Kenya. The larger-bodiedG. garnettii tended to use branches of a bigger diameter and to be found higher in the canopy than the smallerG. zanzibaricus. The latter species spent most of its time in the thick undergrowth. The larger species ate more fruit than the smaller. There were differences between the species in the type of invertebrate prey remains found in the feces. It is suggested that the differences in habitat use were influenced by the different body sizes of the two galagos, which so enabled these closely related species to coexist. Order of authorship is alphabetical.     

Differential cannibalism and population dynamics in a host-parasitoid system

The effects of host cannibalism on a host-parasitoid system were explored through experiment and modelling. In individual encounters between parasitized and unparasitized Plodia interpunctella larvae, parasitized larvae were more likely to be cannibalized. Inclusion of this differential cannibalism into a simple Lotka-Volterra-type model of host-parasitoid population dynamics generates alternative stable states-including stable coexistence and extinction of the parasitoid — which depend on starting conditions. Possible mechanisms for differential cannibalism, and its implications for studies of host-parasitoid populations and biological control programmes are discussed.     

Precopulatory Sexual Cannibalism Causes Increase Egg Case Production,Hatching Success,and Female Attractiveness to Males

Precopulatory sexual cannibalism is an extreme form of sexual conflict that can entail significant costs to the cannibalized individual and a variety of costs and benefits to the cannibal itself. Characterizing these costs and benefits is fundamental to our understanding of how this behavior evolves. Using the spider Agelenopsis pennsylvanica, we tested the reproductive consequences of precopulatory sexual cannibalism by staging cannibalization events and comparing the performance of experimental cannibals against natural cannibals (i.e., those that cannibalized on their own) and non‐cannibals. We found two performance benefits associated with precopulatory sexual cannibalism: first, experimental cannibals were more likely to produce egg cases than non‐cannibals, and second, egg cases from experimental cannibals and natural cannibals were significantly more likely to hatch than those produced by non‐cannibals. We then tested whether males were more likely to approach the webs of experimental cannibals vs. non‐cannibalistic control females. Our data demonstrate that sexual cannibalism increases female attractiveness to males. Although this result seems counterintuitive, in fact, rates of precopulatory sexual cannibalism were much lower in females that had already cannibalized their first male: 38% of sexually naïve females engaged in precopulatory sexual cannibalism, whereas only 5% of females engaged in cannibalism a second time. Thus, males that approach cannibals receive two benefits: they are less likely to be cannibalized precopula, and they have the possibility of mating with females that have a higher probability of producing viable egg cases. Taken together, our data suggest that precopulatory sexual cannibalism affords females numerous benefits and may have a hand in shaping male mate choice decisions.     

Lactation and interbirth interval in the Senegal galago (Galago senegalensis moholi)

Five years of reproductive data on Galago senegalensis moholi at the Duke University Primate Center were examined to determine the effect of lactation on interbirth interval and its component phases, postpartum anovulatory interval and interval from onset of estrous cycles to conception. Females whose infants died within 3 weeks of birth had significantly shorter interbirth intervals and postpartum anovulatory intervals than did females who raised their infants until weaning.     

Comparison between wild-born mother-female infant interactions and laboratory-born mother-female infant interactions during the first 14 weeks after birth in individually caged cynomolgus macaques

In this study we compared mother-female infant interactions between primiparous and multiparous laboratory-born (F1) cynomolgus macaques (Macaca fascicularis) in individual cages at Tsukuba Primate Center (TPC), Japan, during the first 14 weeks of infant life. We also compared interactions between multiparousF1 mothers and their female infants with those between wild-born mothers and their female infants when mothers and their infants were housed in the same individual cages. PrimiparousF1 mothers showed significantly higher values for contact with and holding of their infants than multiparousF1 mothers. The primiparousF1 mothers also tended to behave aggressively toward their infants when the latter did not show any obviously irritating behaviors. Thus, the primiparousF1 mothers seemed to be inconsistent in terms of maternal behavior. Compared with multiparous wild-born mothers, multiparousF1 mothers moved more frequently, held their infants less frequently and acted aggressively toward their infants less frequently. However, infants ofF1 mothers, as well as infants of wild-born mothers, interacted with their mothers through approaching and playful contact with them. These findings indicate that the attitude of multiparousF1 mothers toward their infants was relatively passive. Possible reasons for the passive maternal style of multiparousF1 mothers are discussed.     

Maternal responses to dead and dying infants in wild troops of ring-tailed lemurs at the Berenty Reserve,Madagascar

We describe responses of seven mothers and other troop members to dead and dying infants in several troops of ring-tailed lemurs(Lemur catta) at the Berenty Reserve, Madagascar. In contrast to mothers in simian species, ring-tailed lemur mothers rarely carried their dying, immobile or dead infants. However, they sniffed, licked, and touched them even after they had died. While the dying infants were still peeping, their mothers remained near them, and 15 to 76 min after the infants ceased to peep, they were left by their mothers. Six of the seven mothers returned to their dead infants several times within the first few hours after they had left them. All seven mothers gave repeated calls, such as “mew” and “pyaa,” when they were separated from either their dead infants or other troop members or both. Thus, each mother exhibited some form of maternal behavior toward her dead infant for hours after its death. These results indicate that there may not be a great gap in terms of maternal affection between simian and prosimian mothers. We also discuss visuospatial memory ability in ring-tailed lemurs and the causes of the infants’ deaths.     

Individual identification of non-human primates using DNA fingerprinting

DNA fingerprints were studied in non-human primates including three species of Old World monkeys and one species of hominoid, using tandem repeats of a 28-base-pair sequence downstream of the human c-Ha-ras-1 oncogene as a probe. We observed Southern hybridization patterns consisting of multiple hypervariable DNA fragments, which were specific to each of the individuals examined. These results indicate that DNA fingerprinting is a powerful tool for identification of individuals among non-human primates, as is the case in man. On leave from the Department of Legal Medicine, Institute of Community Medicine, University of Tsukuba.