Stone-tool usage by Thai long-tailed macaques (Macaca fascicularis)

In January and March of 2005, we conducted surveys of long-tailed macaques at Piak Nam Yai Island, Laem Son National Park (9 degrees N 34-35', 98 degrees E 28'), Ranong Province, situated in southern Thailand. Two of the three troops of long-tailed macaques found on the island were observed using axe-shaped stones to crack rock oysters, detached gastropods (Thais tissoti, Petit, 1852), bivalves (Gafrarium divaricatum, Gmelin, 1791), and swimming crabs (Thalamita danae, Stimpson, 1858). They smashed the shells with stones that were held in either the left or right hand, while using the opposite hand to gather the oyster meat. Some monkeys used both hands to handle the stones. According to Matsuzawa's 1996 hierarchical classification of tool usage (levels 0-3), the tool usage by Thai long-tailed macaques could be characterized as either level 1 (cracking rock oysters with stones) or level 2 (cracking drifting mollusks and crabs with stones by placing them on a rock). Our discovery of stone-tool usage by Thai long-tailed macaques provides a new point of reference for discussions regarding the evolution of tool usage and the material culture of primates.     

Sex differences in the stone tool-use behavior of a wild population of burmese long-tailed macaques (Macaca fascicularis aurea)

We investigated sex differences in how Burmese long-tailed macaques (Macaca fascicularis aurea) used stone tools to open shelled food items along the shores of two islands in Laemson National Park, Thailand. Over a 2-week period in December 2009, we collected scan and focal samples on macaques when they were visible along the shores and mangroves. We found females used stones more often while feeding and used smaller tools than males. Females also processed sessile oysters more than males, whereas males processed unattached foods more than females. It was unclear which sex was overall more proficient at stone tool use, but males did perform significantly better at opening unattached food items with large pounding stones. Females also struck food items more times during tool-use bouts and at a faster rate, but no significant difference was found in average tool-use bout duration. Males processed foods slightly faster within a tool-use bout, but we were unable to detect a significant difference in the rate of food processing while foraging with tools. In summary females chipped open sessile oysters with an axing technique more than males, while males used larger stones to pound open unattached shelled food more often than females. Despite using pounding more than females, males also regularly utilized the axing technique on sessile oysters. Our results are the first assessment of sex differences in macaque stone tool use, providing a basis for comparison with tool use in other primates, and to nonfunctional forms of stone use in other macaques.     

Postdispersal nepotism in male long‐tailed macaques (Macaca fascicularis)

Cooperative behaviors are promoted by kin selection if the costs to the actor are smaller than the fitness benefits to the recipient, weighted by the coefficient of relatedness. In primates, cooperation occurs primarily among female dyads. Due to male dispersal before sexual maturity in many primate species, however, it is unknown whether there are sufficient opportunities for selective tolerance and occasional coalitionary support for kin selection to favor male nepotistic support. We studied the effect of the presence of male kin on correlates of male reproductive success (residence time, duration of high dominance rank) in non‐natal male long‐tailed macaques (Macaca fascicularis). We found that “related” (i.e., related at the half‐sibling level or higher) males in a group have a significantly higher probability to remain in the non‐natal group compared to males without relatives. Moreover, males stayed longer in a group when a relative was present at group entry or joined the same group within 3 months upon arrival. Males with co‐residing relatives also maintained a high rank for longer than those without. To our knowledge, this is the first demonstration of a potential nepotistic effect on residence and rank maintenance among non‐natal males in a social system without long‐term alliances.     

Affiliation Between Aggressors and Third Parties Following Conflicts in Long-Tailed Macaques (Macaca fascicularis)

Studies on cercopithecine monkeys have shown that soon after an agonistic conflict, victims have increased rates of affiliation with the agressor—reconciliation—but not with other group members. Postconflict affiliation is thought to function to restore disturbed relationships and to reduce social tension. This study on a captive group of long-tailed macaques (Macaca fascicularis) is focused on postconflict affiliative behavior of the aggressor. Increased rates of contact between female aggressors and kin of the victim occurred, as well as between female aggressors and their own kin. Furthermore, there were increased rates of contact between aggressors—males and females—and other group members. The increase in contacts with the victim's kin was selective, i.e., it could not be ascribed to the increased contact tendency with group members in general, and was not a side effect of the aggressor's proximity to the victim due to reconciliation. The increase in contacts with own kin was not selective. The fact that male aggressors do not have increased postconflict contacts with their kin or with kin of the victim is in agreement with the notion that males are less integrated in the nepotistic matrilineal network than females are. The fact that studies by others that focused on the victim evidence no increase in postconflict contacts with kin of the opponent or with other group members may be explained by the aggressor's larger influence over the postconflict situation: to reduce social tension, it might be more effective to affiliate with the aggressor than with the victim. Our findings emphasize that conflicts influence the behavior of other monkeys besides the direct contestants and, thus, indicate that the disturbance of social homeostasis is a matter of concern for all group members.     

The human-ABO blood groups of free-ranging long-tailed macaques (Macaca fascicularis) and parapatric rhesus macaques (M. mulatta) in Thailand

BACKGROUND: Long-tailed and rhesus macaques are widely used in biomedical research; therefore, the known blood group is important. METHODS: The human-type ABO blood group was determined in wild or semi-wild long-tailed and rhesus macaques in Thailand. A total of 729 long-tailed and 160 rhesus macaques from 20 localities were temporarily caught. RESULTS: The frequency profiles of blood groups, calculated by averaging the frequency of each troop in long-tailed and rhesus macaques, were AB > O > B > A at 29.6%, 27.4%, 27.2%, and 15.8%, and B > AB > A > O at 39.6%, 33.4%, 18.2%, and 8.8%, respectively. Irrespective of locality, the frequencies were AB > O > B > A of 29.6%, 28.0%, 24.4%, and 18.0%, and AB > B > A > O of 37.5%, 28.7%, 26.9%, and 6.9%, respectively, for all long-tailed and rhesus macaques. The frequency profile of blood groups in Thai rhesus macaques was somewhat similar to that in the parapatric long-tailed macaques; however, it was different from other rhesus populations where only group B was detected. CONCLUSIONS: Our data support the hypothesis that Indochinese rhesus macaques are hybrids between rhesus and long-tailed macaques in the past.     

Mitochondrial DNA variation within and among regional populations of longtail macaques (Macaca fascicularis) in relation to other species of the fascicularis group of macaques

An 835 base pair (bp) fragment of mitochondrial DNA (mtDNA) was sequenced to characterize genetic variation within and among 1,053 samples comprising five regional populations each of longtail macaques (Macaca fascicularis) and rhesus macaques (Macaca mulatta), and one sample each of Japanese (M. fuscata) and Taiwanese (M. cyclopis) macaques. The mtDNA haplotypes of longtail macaques clustered in two large highly structured clades (Fas1 and Fas2) of a neighbor-joining tree that were reciprocally monophyletic with respect to those representing rhesus macaques, Japanese macaques, and Taiwanese macaques. Both clades exhibited haplotypes of Indonesian and Malaysian longtail macaques widely dispersed throughout them; however, longtail macaques from Indochina, Philippines, and Mauritius each clustered in a separate well-defined clade together with one or a few Malaysian and/or Indonesian longtail macaques, suggesting origins on the Sunda shelf. Longtail macaques from Malaysia and Indonesia were far more genetically diverse, and those from Mauritius were far less diverse than any other population studied. Nucleotide diversity between mtDNA sequences of longtail macaques from different geographic regions is, in some cases, greater than that between Indian and Chinese rhesus macaques. Approximately equal amounts of genetic diversity are due to differences among animals in the same regional population, different regional populations, and different species. A greater proportion of genetic variance was explained by interspecies differences when Japanese and Taiwanese macaques were regarded as regional populations of rhesus macaques than when they were treated as separate species. Rhesus macaques from China were more closely related to both Taiwanese and Japanese macaques than to their own conspecifics from India.     

Reconciliation and relationship quality in Assamese macaques (Macaca assamensis)

A consistent conclusion in reconciliation research is that animals that reconcile are likely to have strong social bonds. This has led to the hypothesis that reconciliation occurs most often between valuable social partners. We tested this hypothesis in a group of Assamese macaques (Macaca assamensis) living near a temple in Assam, India. Using focal sample and ad libitum data collection, we recorded the occurrence of reconciliation, grooming, and agonistic aiding, and the outcomes of approach. We used matrix association methods (TauKr correlation) to correlate reconciliation with grooming, aiding, and approach outcome. Females reconciled more often with females with which they had stronger grooming and aiding relationships. The correlation between reconciliation and aiding was significant for support to the aggressor and the victim. In contrast, no such correlations with reconciliation were found for males. This study provides evidence that females reconcile most often with valuable and compatible social partners. The results do not support the relationship-quality hypothesis for males, and we suggest that future studies give more consideration to the possibility that males reconcile for reasons other than to repair relationships with valuable partners.     

A pilot study of the social correlates of levels of urinary cortisol,prolactin, and testosterone in wild long-tailed macaques (Macaca fascicularis)

Urine samples were collected from individuals in a wild population of Sumatran long-tailed macaques (Macaca fascicularis), and the levels of cortisol, immunoreactive prolactin, and (for males) testosterone were determined. The amount of foraging during the 2 hr preceding urine collection were found to affect the levels of urinary cortisol, but not those of the other hormones. Immigration into a new group and having one's infant kidnapped led to increased levels of cortisol. Levels of cortisol and testosterone were correlated both within and between individuals, whereas prolactin varied independently. The effects of age, reproductive status, and social rank on the mean values of individuals were also examined. Lactating females had higher prolactin levels than non-lactating ones; reproductive state interacted with the age effect on prolactin and possibly cortisol. No effects of social status were found in spite of a small, but consistent effect of rank on birth rate in this population. Among males, age and rank are strongly linked. The low ranking old males had increased levels of cortisol, even though the younger high-ranking males were involved in the fiercest conflicts.     

Urinary and fecal immunoglobulin A, cortisol and 11-17 dioxoandrostanes, and serum cortisol in metabolic cage housed female cynomolgus monkeys (Macaca fascicularis)

BACKGROUND AND METHODS: Quantitative enzyme-immunoassays of urinary and fecal immunoglobulin A (IgA), cortisol and 11-17-dioxoandrostanes (11,17-DOA), and serum cortisol in eight metabolic-cage-housed female cynomolgus monkeys were performed. The monkeys were divided into two groups, B and NB. Group B animals were blood sampled every 6 hours, whereas Group NB animals were not handled/blood sampled. RESULTS: No differences were recorded between the amounts of feces and urine excreted by the two groups. Group B animals excreted more urinary cortisol than did Group NB animals indicating that restraint-blood sampling resulted in a stress response. Excreted amounts of IgA and 11,17-DOA (urine and feces) did not differ between the groups. CONCLUSIONS: Urinary cortisol was a reliable marker of the stress associated with repeated blood sampling. Declining amounts of excreted urinary cortisol indicated that cynomolgus monkeys acclimated quickly to repeated blood sampling in metabolism cages. Within and between animal variation in amounts of feces voided demonstrated the importance of expressing fecal markers as 'amounts excreted per time unit per kg body weight' rather than just measuring the concentrations in fecal samples.     

Disproportionate participation by age/sex classes in aggressive interactions between long-tailed macaques (Macaca fascicularis) and human tourists at Padangtegal monkey forest, Bali, Indonesia

We observed 420 aggressive interactions between tourists and Macaca fascicularis at the Padangtegal Wanara Wana Temple forest site in Bali, Indonesia, during the months of June and July 2001. The data collected included patterns of aggression, presence or absence of food, and demographic information on resident macaques and human visitors. Analyses of the interactions suggest that macaques respond differentially to humans according to the age/sex classes involved. Additionally, adult and subadult male macaques participated in more aggressive behaviors than expected, while adult female macaques and immatures participated in such behaviors less than expected. These variations in interaction patterns between macaques and tourists may have substantial implications for management issues and the potential for pathogen transmission.     

The relationship of agonistic and affiliative behavior patterns to cellular immune function among cynomolgus monkeys (Macaca fascicularis) living in unstable social groups

Considerable recent interest has focused on the possibility that behavioral factors may influence immune competence, and hence, potentially, patterns of disease. We report here the relationship between the aggressive and affiliative behavior and the cellular immune responses of 30 adult male cynomolgus monkeys (Macaca fascicularis) living in small (n = 5) social groups whose members were periodically redistributed over 26 months. Animals also were subjected to behavioral observation, allowing them to be categorized as either high or low in aggressiveness and affiliation. At the end of the 26 months, lymphocyte proliferation tests were performed on blood samples from all monkeys, using both concanavalin A (ConA) and phytohemagglutinin (PHA) in concentrations of 1, 5, and 10 ug/ml. Two-by-two (Aggressiveness [high, low] X Affiliation [high, low]) analyses of variance performed on these data showed lymphocyte proliferation in response to both ConA and PHA to be greatest (at 1 ug/ml) among highly affiliative animals, albeit only if they were also low in aggressiveness (ConA: Affiliation x Aggression, P < 0.02; PHA: Affiliation x Aggression, P < 0.03). An additional finding was that natural killer cell activity (at an effector to target ratio of 100:1) was highest among highly affiliative animals, regardless of their aggressiveness (P < 0.05). These results indicate that immune competence may be enhanced among monkeys which, in response to a disrupted social environment, spend large amounts of time in affiliation with other animals. Social status, a phenomenon known to influence many aspects of nonhuman primate physiology, was unassociated with nonspecific lymphocyte blastogenesis or natural killer cell activity in this experiment.     

Tetanus antibody titers and duration of immunity to clinical tetanus infections in free-ranging rhesus monkeys (Macaca mulatta)

Prior to 1985 tetanus was a major cause of mortality in the free-ranging colony of rhesus monkeys on Cayo Santiago, accounting for almost a quarter of annual deaths. In 1985 and 1986 all animals (except infants) received primary and booster doses, respectively, of tetanus toxoid. In subsequent years primary immunizations were given to all yearlings, and boosters were administered to all 2-year-old animals during the annual capture of the colony. The main objectives of the tetanus immunization program were to reduce the pain and suffering caused by tetanus infections and to decrease mortality in the colony. Other objectives were to evaluate the efficacy of the two-dose tetanus toxoid immunization protocol and to determine whether additional boosters might be required to provide adequate long-term protection against tetanus infections. The immediate effect of the mass immunization program was the elimination of clinical tetanus infections in the population and a 42.2% reduction in the overall mortality rate. Since the immunization program began, no cases of tetanus have been observed in the colony, except in two unimmunized infants, and it has not been necessary to give tertiary injections of tetanus toxoid to maintain protection against infection. A sample collected in 2004 of the original cohort of monkeys immunized in 1985 and 1986 showed that 93.3% (14/15) had protective tetanus antibody titers (>0.01 IU/ml) at the ages of 20-23 years, which is close to the life expectancy of the Cayo Santiago rhesus macaques. Two intramuscular doses of tetanus toxoid provided long-term, if not lifelong, protection against tetanus for rhesus monkeys living in a tropical clime where tetanus is enzootic and the risk of infection is great.     

Seasonal dynamics of digestion in relation to diet quality and intake in European roe deer (Capreolus capreolus)

Three tame, hand-reared adult roe deer (Capreolus capreolus) were fed a low-quality diet (blueberry stems) or high-quality concentrate either restricted or ad libitum in summer and winter. Total mean retention time (TMRT) and rumen retention time (RRT) were significantly longer, indigestible fill was significantly higher and apparent digestibility and intake were significantly lower when fed blueberry stems compared to concentrate. The feeding regimes of concentrate did not affect the digesta kinetic estimates, except that total fill and apprent digestibility were significantly higher when deer were fed ad libitum than when they were fed a restricted ration. TMRT was significantly longer when they were fed a restricted ration of blueberry stems than for ad libitum intake, whereas all other estimates were equal. Intake was significantly higher and TMRT and RRT were significantly shorter in summer compared to winter when they were fed concentrate. These findings support the theory that roe deer, as small-bodied concentrate selectors, are adapted to high intake, rapid turnover, and rapid digestion when fed high-quality concentrate. When fed a low-quality diet the roe deer may be limited by rumen bulk. A strategy based on increased rumen retention accompanied by increased cell-wall digestion has therefore severe limitations in roe deer. This indicates that roe deer are dependent on a selective feeding strategy to enhance winter survival.     

Sex ratio in relation to season and host plant quality in a monogenous stem-galling midge (Diptera: Cecidomyiidae)

Abstract.  1. The sex determination mechanism in gall midges is little understood, although it is known that the females of several species primarily or exclusively produce unisexual broods throughout their lifetime.
2. The gall midge Izeniola obesula Dorchin is a multivoltine species, inducing multi-chambered stem galls on the salt-marsh plant Suaeda monoica . Each gall contains 5–70 individuals, all being the progeny of a single female. Sampling of more than 450 galls, from which adult midges were reared, suggested that I .  obesula exhibits strict monogeny, resulting in galls that contain either all female or all male progeny.
3. Characterisation of the growth pattern of young S .  monoica shoots revealed that shoots in apical positions grew more rapidly than shoots in more basal positions. Galls that were induced on such shoots were larger and yielded more adult midges.
4. No difference in the site of gall induction was found between male and female galls, with galls of either sex being mainly induced on more rapidly growing shoots. It is concluded that I .  obesula females cannot control the sex of their progeny, and that both female-producers and male-producers strive to maximise their reproductive success by choosing the faster-growing shoots for gall induction.
5. Female galls were larger and more abundant than male galls at almost all times. The sex ratio among galls fluctuated throughout the year, ranging from 4:1 in spring to 1:1 in winter. The skewed sex ratio among galls possibly results from greater mortality rates among male galls than among female galls, due to either primary or secondary factors. Alternatively, it is possible that the number or fitness of male-producers in the population is reduced relative to female-producers.     

Adrenocortical responses in zebra finches (Taeniopygia guttata): individual variation, repeatability, and relationship to phenotypic quality

Although individual variation is a key requirement for natural selection, little is known about the magnitude and patterns of individual variation in endocrine systems or the functional significance of that variation. Here we describe (1) the extent and repeatability of inter-individual variation in adrenocortical responses and (2) its relationship to sex-specific phenotypic quality, such as song duration and frequency and timing of egg laying. We measured adrenocortical responses to a standardized stressor in zebra finches (Taeniopygia guttata) at two life history stages: approximately day 16 (nestlings) and 3 months of age (sexually mature adults). Subsequently, we assessed phenotypic (reproductive) quality of all individuals as adults. Marked inter-individual variation in the adrenocortical response was seen in both sexes and ages, e.g., stress-induced corticosterone ranged from 2.2 to 62.5 ng/mL in nestlings and 5.0-64.0 ng/mL in adults. We found sex differences in (a) inter-individual variation in the adrenocortical response, (b) repeatability, and (c) relationships between corticosterone levels and phenotypic quality. In males, variation in nestling corticosterone was weakly but positively correlated with brood size and negatively correlated with nestling mass (though this relationship was dependent on one individual). There was no significant correlation of adrenocortical responses between two stages in males and adult phenotypic quality was significantly correlated only with adult corticosterone levels. In contrast, in females there was no relationship between nestling corticosterone and brood size or mass but adrenocortical response was repeatable between two stages (r2=0.413). Phenotypic quality of adult females was correlated with nestling baseline and adrenocortical response.