Radiographic evaluation of neonatal skeletal development in Callimico goeldii reveals closer similarity to Callithrix jacchus than to Saguinus oedipus

The phylogenetic affinities of the neotropical Goeldi's monkey (Callimico goeldii) have long been a matter of debate. Whereas most morphological evidence appears to place Callimico in a sister group position relative to the Callitrichidae, genetic studies place C. goeldii within the Callitrichidae and suggest that it is more closely related to marmosets than to tamarins. The present study presents the first radiographic analysis comparing the secondary limb bone ossification of newborn C. goeldii with representatives of the marmosets (Callithrix jacchus) and tamarins (Saguinus oedipus). The state of secondary ossification of the epiphysis and short bones is classified into three different ontogenetic stages. Our results reveal that in terms of the number of ossification centers, C. goeldii is significantly closer to C. jacchus than to S. oedipus. This is the first morphological study to support the findings of molecular studies, and the results suggest that C. goeldii is more closely related to marmosets than to tamarins.     

Social interaction with non-averse group-mates modifies a learned food aversion in single- and mixed-species groups of tamarins (Saguinus fuscicollis and S. labiatus)

For social species, being a member of a cohesive group and performing activities as a coordinated unit appear to provide a mechanism for the efficient transmission of information about food. Social learning about food palatability was investigated in two captive primates, Saguinus fuscicollis and S. labiatus, which form stable and cohesive mixed-species groups in the wild. We explored whether an induced food aversion toward a preferred food is modified during and after social interaction with non-averse conspecifics or congeners. Sets of intra- and interspecific pairs were presented with two foods, one of which was considered distasteful by one of the pairs (the other was palatable), and their behavior was compared pre-interaction, during interaction, and post-interaction. For the aversely-conditioned individuals of both species, the change in social context corresponded to a change in their preference for the food that they considered unpalatable, regardless of whether they had interacted with a conspecific or congeneric pair, and the change in food preference was maintained post-interaction. In a control condition, in which averse individuals did not have the opportunity to interact with non-averse animals, S. fuscicollis sampled the preferred food, but not as quickly as when given the opportunity to interact. We conclude that the social learning demonstrated here may allow individual tamarins to track environmental change, such as fruit ripening, more efficiently than asocial learning alone, because social learners can more quickly and safely focus on appropriate behavior by sharing up-to-date foraging information. Furthermore, since the behavior of congeners, as well as conspecifics, acts to influence food choice in a more adaptive direction, social learning about food palatability may be an advantage of mixed-species group formation to tamarins of both species.     

Urinary endocrine monitoring of the ovarian cycle and pregnancy in Goeldi's monkey (Callimico goeldii)

A non-invasive study of urinary hormones in 6 captive female Goeldi's monkeys provided accurate information on reproductive function. Conjugated oestrone accounted for 80-85% of the urinary oestrone and oestradiol measured. Radioimmunoassay measurements of conjugated oestrone provided a reliable indicator of cyclic ovarian function (mean cycle length: 24.1 +/- 0.9 days; n = 9) and pregnancy (gestation: 145, 155 days; n = 2). Measurements of urinary progesterone and pregnanediol glucuronide were only reliable as indicators of ovarian cyclicity. Elevations in urinary conjugated oestrone coincided with luteal-phase elevations of urinary progesterone and pregnanediol glucuronide. Urinary LH concentrations provided no indication of pituitary activity. However, the frequencies of female sexual solicitations of males were maximal when oestrone conjugate concentrations rose, suggesting a peri-ovulatory period. Ovulation was suppressed in 1 of 3 subordinate females housed in male-female-female trios.     

Monitoring fecal samples for estrogen excretion across the ovarian cycle in Goeldi's monkey (Callimico goeldii)

In captive Goeldi's monkeys, estrogen concentration was determined in fecal samples collected from 4 cycling/unmated females and 4 postpartum/mated females in order to ascertain the potential of fecal estrogen monitoring for providing basic information about reproductive status in this endangered Amazonian monkey. Subjects were fed an omnivorous diet and first-void feces were collected in the home cage at 1–3-day intervals for 30–50 days from the cycling females, and at 6–14-day intervals around the estimated time of the postpartum ovulation in each of the 4 mated females. Estimates for the duration of ovarian cycles (22–26 days) and the timing of ovulation were based on cyclic profiles of either blood progesterone or urinary pregnanediol-3α-glucuronide. Fecal estrogen values were normalized using these plasma or urinary profiles. HPLC analysis of estrogen from postpartum fecal samples demonstrated the presence of unconjugated estrone and estradiol-17β (“unconjugated estrogen”). Unconjugated estrogen was extracted and its fecal concentration estimated via EIA. The correlation (r) between plasma estrone conjugates and fecal unconjugated estrogen across nonconception ovarian cycles was 0.65 and measurement of the latter generated cyclic profiles. A range of 4–36-ng unconjugated estrogen g^?1 feces was identified for follicular phases of nonconception cycles. Fecal unconjugated estrogen first exceeded the concentration range of the follicular phase 2–5 days after ovulation; the range was 49–402 ng g^?1 feces in samples collected during the remainder of these nonconception luteal phases. Luteal phase concentrations were on average 10-fold higher than follicular phase concentrations. Each of the 4 mated females conceived at its postpartum ovulation; concentrations of fecal unconjugated estrogen excreted by 3 of these females demonstrated a marked postovulatory increase. This study demonstrates that fecal unconjugated estrogen can be applied to monitor ovarian cyclicity in Goeldi's monkey. © 1994 Wiley-Liss, Inc.     

Resting energy metabolism of Goeldi's monkey (Callimico goeldii) is similar to that of other callitrichids

The resting metabolic rates (RMRs) of six adult Goeldi's monkeys (Callimico goeldii) were measured using standard methods of open circuit respirometry during both the active (daytime) and inactive (nighttime) circadian phases for this species. One subject was measured both while she was pregnant and after she delivered a full-term, stillborn infant. Inactive-phase RMR within thermal neutrality (above 27.5 degrees C) averaged 288.5 +/- 30.8 ml O2/hr; active-phase RMR within thermal neutrality averaged 416.3 +/- 60.9 ml O2/hr. These values are 74.6% and 107.6%, respectively, of the mammalian expected for animals of this body mass. During the inactive phase, metabolic rate increased an estimated 4.3% for every degree decline in temperature below 27.5 degrees C. The RMR in Goeldi's monkey is similar quantitatively and qualitatively to those of other captive callitrichids that have been studied, with active-phase RMR being at or slightly above the mammalian expected, and inactive-phase RMR being significantly reduced. We propose that this circadian pattern of RMR is a consequence of small body size, and is not a specific metabolic adaptation within the Callitrichidae. Thus we predict that metabolic studies measuring both circadian phases in other small primates will also find this pattern of reduced RMR during the inactive phase. The inactive-phase RMR within thermal neutrality of the pregnant female was not different from that measured after the stillbirth, despite an almost 15% difference in body mass. During pregnancy, however, the female was more metabolically responsive to temperature below thermal neutrality, and had a lower upper critical temperature (i.e., was less tolerant of heat).     

A field study of the socio-ecology of the Goeldi's monkey (Callimico goeldii) in northern Bolivia

A 5-month field study on both the distribution and ecology of Callimico goeldii was carried out in the seasonally dry rain forest of north-western Bolivia. The species was found to be very sparsely distributed (approximately one group per 4 km2) in isolated groups of about 6 animals throughout the study area. Callimico was found to associate a great deal with two species of Saguinus that inhabit the same region in greater densities. It appears to be a habitat specialist, preferring low-lying and damp, but well-drained, bamboo forest and spending nearly all its time within 3 m of ground level, travelling mainly by vertical clinging and leaping. We believe that this ecological specialisation accounts for the species' discontinuous micro-distribution, and that this in turn is related to Callimico's distinctive pattern of social organisation.     

Urinary excretion of oestrone conjugates and gonadotrophins during pregnancy in the Goeldi's monkey (Callimico goeldii)

Oestrone conjugate and LH/CG were measured in the urine of 4 Goeldi's monkeys during 6 pregnancies. The gestational length was a mean of 148.8 days from the post-partum LH/CG peak to parturition. CG was first detected a mean of 18.8 days after the LH/CG peak and values remained elevated for a mean of 44.8 days. Three different gonadotrophin assays were used to detect LH/CG: the mouse in-vitro interstitial cell bioassay, a mixed heterologous LH RIA, and a monkey CG RIA. The mouse in-vitro interstitial cell bioassay was useful for measuring both the LH peak which occurred post partum and the CG concentrations during pregnancy. However, both immunoassays were inconsistent in measuring LH due to poor cross-reactivity or lack of specificity; CG concentrations were measurable. Oestrone conjugates became elevated at the time of the LH/CG peak and concentrations continued to increase throughout pregnancy, reaching peak levels before parturition. The postpartum interval, pregnancy and parturition can therefore be monitored in the Goeldi's monkey by the use of urinary assays: those for bioactive LH and immunoreactive oestrone conjugates to determine the post-partum LH peak and those for immunoreactive LH/CG and immunoreactive oestrone conjugates to follow pregnancy and parturition.     

Mothers, not fathers, determine the delayed onset of male carrying in Goeldi's monkey (Callimico goeldii)

In biparental species, females are thought to accept and even to seek male assistance in rearing of the young. In this study, we present data that suggests that Goeldi's monkey females (Callimico goeldii) actually reject male parental care for a certain period. In Callimico, which have biparental care, mothers carry the infant exclusively for the first three weeks despite the fact that fathers are interested in their infants directly after birth. Fathers initiated significantly more body contact with their mates when newborn infants were present and retrieved one-day-old infants that were experimentally presented to them. The onset of paternal carrying in our colony was 27.5 days compared to 11.5 days (medians) observed in the field. However, presentation of a live potential predator induced earlier onset of paternal carrying by about 10 days. Additional costs to maternal carrying such as foraging and predator avoidance are likely factors influencing the decision of the mother as to when to share the cost of infant carrying with the father. We conclude that Goeldi's monkey fathers start carrying their infants so late because they do not get them earlier from the mother. We suggest that one ultimate explanation for that delay might be increased infant mortality when infant transfer starts at an earlier stage.     

An investigation into the socioendocrinology of infant care and postpartum fertility in Goeldi’s monkey (Callimico goeldii)

We investigated the existence of interaction between the major behavioral and endocrine events that occur in breeding pairs of Callimicoduring the postpartum period: the reduction in maternal care, the onset of maternal aggression, the onset of paternal care, and the resumption of female fertility. While the frequency of nursing remained constant throughout the 6-week observation period, decreasing amount of time spent nursing generally preceded the onset of paternal carriage. Decreasing nursing duration was not associated with the occurrence of postpartum ovulation. Some mothers frequently acted aggressively toward the infant during the period of first mother-to-father transfer of the infant, while other mothers did not. There is no correlation between the interval to the first transfer and the period to postpartum ovulation. We validated urinary cortisol as a measure of stress and defined the duration of its poststress elevation as approximately 3 hr. There is no consistent relationship between female behavior and endocrine state, or male cortisol values and the onset of infant carrying by fathers. During the peritransfer phase, no significant change in cortisol concentration occurred, while the pre-, peri-, and postovulatory phases appeared to be reflected in urinary cortisol output by some males. Based on these results, we propose an explanatory model for the causal dynamics of infant care in pairs of Callimico.The model stresses the importance of a high reproductive rate to male and female reproductive strategies.     

Response to novel food and the role of social influences in common marmosets (Callithrix jacchus) and Goeldi's monkeys (Callimico goeldii)

Neophobia, defined as showing caution toward novel features of the environment, is widespread in birds and mammals; it can be affected by ecology, early experience, and social context. In this study, we aimed to (i) investigate the response to novel food in adult common marmosets and Goeldi's monkeys and (ii) assess the role of social influences. We used an experimental paradigm employed previously with capuchin monkeys and children, in which a subject (observer) was presented with a novel food under three conditions: (i) Presence: group members did not have food; (ii) Different color: group members received familiar food whose color differed from that of the observer's novel food; (iii) Same color: group members received familiar food of the same color as the observer's novel food. Although most common marmosets tasted and/or ate the novel food, none of the Goeldi's monkeys ate it and only two sampled it. Differences in home range size and early social experience might explain the divergent behavior of the two species. Observers of both species similarly attended to group members and their visual attention increased with the number of group members eating, especially when the observer's and group members' foods were perceptually similar. However, we observed social influences on explorative behavior in Goeldi's monkeys but not on explorative or eating behavior in common marmosets. This result might be explained by the different pattern of response to novel food observed in the two species. Moreover, social influences on Goeldi's monkeys' behavior were nonspecific, i.e. they were not based on an appreciation that the food is safe because eaten by group members.     

Foraging behavior of a tamarin group (Saguinus fuscicollis weddelli) and interactions with marmosets (Callithrix emiliae)

We present data on aspects of the behavioral ecology of a free- ranging group of Saguinus fuscicollis weddelliat a site in Brazilian Amazonia where a second callitrichid, Callithrix emiliae,is syntopic. Diet, activity patterns, and ranging behavior are broadly similar to those of S. fuscicollisfrom sites in Bolivia, Brazil, and Perú, though significant seasonal changes include an extreme and atypical form of ranging behavior in which they foraged in central-place fashion around a source of exudate—Parkia pendula. S. f. weddelliwas active at relatively low levels in the forest both in absolute terms and relative to C.emiliae, which appears to be an important factor in their niche partitioning. Association between the two species appeared to be less systematic overall than those observed between S. fuscicollisand congeners at other sites, though this may be partly a result of observation conditions. During the period of central-place foraging, the two species exhibited a high degree of association. Other characteristics of the behavior of S. f. weddelliat the study site include the frequent use of tree holes as sleeping sites.     

Status and ecology of the golden monkey (Cercopithecus mitis kandti) in Mgahinga Gorilla National Park, Uganda

Given the degree to which tropical ecosystems are currently being disturbed by human activities, it is essential to set priorities for conservation and thus it becomes important to consider how best to set these priorities. From this perspective, this study provides the first detailed investigations of Cercopithecus mitis kandti, the golden monkey, focusing on the population in Mgahinga Gorilla National Park (MGNP), Uganda. Specifically, we (1) establish the current status of the golden monkey in terms of population size and distribution within the park in relation to vegetation types and altitude, and (2) investigate the golden monkey's feeding ecology. A total of 67 censuses of 4+ km transects were conducted along a cumulative distance of 299 km and 132 social groups were encountered. Densities were estimated to have increased by 1.6 times since a census 8 years ago, and the total population in the park is estimated to be between 3164 and 5059 individuals. The average size of golden monkey groups in MGNP is 30 individuals (range 3–62). This is similar to that of other subspecies in neighbouring forests. In contrast, the census conducted 8 years before estimated average group size to be eight individuals. Golden monkeys were observed to eat 21 plant species and they were inferred to eat an additional eleven from signs left behind and reports. Both study groups relied upon leaves (primarily young leaves), fruits and invertebrates for food, but the amount of time they fed on these different types of foods varied between the groups. Given the apparent increase in density since the census 8 years ago, the golden monkeys of MGNP appear to be doing well. However, given the number of snares and the extent of illegal extraction of bamboo found during the census, conservation efforts should be increased.     

The ecology of the introduced patas monkey (Erythrocebus patas) population of Southwestern Puerto Rico

This paper presents the results of a study on the introduced, free-ranging patas monkey population of Southwestern Puerto Rico (SWPR). It describes information on the population size, social group composition, diet, daily ranging patterns, and patas home range during a 3 year period. The patas monkey population in the study area consisted of approximately 120 individuals in four heterosexual groups and several all-male bands. Within their home ranges (26.8 km²), the population density was 4.47 individuals/km². Home range size among the population's four heterosexual groups varied from 3.72 km² to 15.39 km², and minimum daily distance traveled ranged from 0.8–2.0 km. In general, the social structure and mating system of this population parallels what has been described for African populations. However, habitat use, ranging behavior, and the quality of intergroup interactions suggests that patas of this population exhibit territorial behavior. Am. J. Primatol. 45:351–365, 1998. © 1998 Wiley-Liss, Inc.     

Home range dynamics of the yellow‐footed rock‐wallaby (Petrogale xanthopus celeris) in central‐western Queensland

Analyses of the interspecific differences in macropod home range size suggest that habitat productivity exerts a greater influence on range size than does body mass. This relationship is also apparent within the rock‐wallaby genus. Lim reported that yellow‐footed rock‐wallabies (Petrogale xanthopus xanthopus) inhabiting the semi‐arid Flinders Ranges (South Australia) had a mean home range of 170 ha. While consistent with the hypothesis that species inhabiting less productive habitats will require larger ranges to fulfil their energetic requirements, the ranges reported by Lim were considerably larger than those observed for heavier sympatric macropods. The aim of the current study was to document the home range dynamics of P. x. celeris in central‐western Queensland and undertake a comparison with those reported for their southern counterparts. Wallaby movements were monitored at Idalia National Park, between winter 1992 and winter 1994. Male foraging ranges (95% fixed kernel; 15.4 ha, SD = ±7.8 ha) were found to be significantly larger than those of female wallabies (11.3 ha, SD = ±4.9 ha). Because of varying distances to the wallabies' favoured foraging ground (i.e. an adjacent herb field), the direction in which the wallabies moved to forage also significantly affected range size. Mean home range size was estimated to be 23.5 ha (SD = ±15.2 ha; 95% fixed kernel) and 67.5 ha (SD = ±22.4 ha; 100% minimum convex polygon). The discrepancy between these two estimates resulted from the exclusion of locations, from the 95% kernel estimates, when the wallabies moved to a water source 1.5 km distant from the colony site. The observed foraging and home ranges approximated those that could be expected for a macropod inhabiting the semi‐arid zone (i.e. 2.4 times larger‐than‐predicted from body mass alone). Possible reasons for the disparity between the current study and that of Lim are examined.     

The invasion and potential impact of the Asian House Gecko (Hemidactylus frenatus) in Australia

Hemidactylus frenatus is an Asian gecko that has spread pantropically to become one the world's most widespread reptiles. It has been established in Australia for approximately 50 years, but the last two decades have seen massive range expansion across settled areas of northern and eastern Australia; and this spread continues at pace. Disturbingly, H. frenatus is increasingly being detected in natural habitats in Australia, in some cases at high densities. Despite rampant spread, there has been little concern regarding the potential impact of this species on native geckos or natural systems more broadly. This is surprising given that Australia is a centre of gecko origin and diversity, and that H. frenatus has had well documented detrimental impacts on geckos in other parts of its introduced range. Here I review the biology and global distribution of H. frenatus, plot its spread in Australia over the five decades since establishment, and review the research on invasive populations of this species overseas and in Australia to assess potential impacts. I argue that Australia should be more concerned about H. Frenatus because: (i) it is spreading rapidly across northern, eastern and central Australia; (ii) it can invade natural habitats; (iii) it is a very strong competitor and may out‐compete Australian geckos in some situations; and (iv) it carries novel parasites that may impact native reptile species. Hemidactylus frenatus is here to stay and represents a potential threat to Australia's diversity and ecology. A key question is the degree to which it will invade natural habitats and what its impacts will be in these. Research is required to assess the current and potential impacts of H. frenatus in Australia so as to determine how these can be managed and the level of investment warranted.     

The effects of prey,habitat heterogeneity and fire on the spatial ecology of peninsular Diamond Pythons (Morelia spilota spilota: Pythonidae)

Understanding an organism's home range is an important component of effective wildlife management. However, home ranges can vary spatially and temporally within and between populations. Landscape ecology theory can provide a framework for understanding spatio‐temporal variability in animal traits. We used radio‐telemetry in a population of diamond python Morelia spilota spilota Lacépède (Pythonidae) from a biologically rich and structurally heterogeneous reserve in eastern Australia to explore the relationship between home range size, optimal foraging theory and vegetation mosaic theory. Twelve adult snakes were tracked between September 2004 and February 2008. Male home ranges were significantly larger (P < 0.05) and more variable (41 ± 30 ha) than female home ranges (23 ± 5 ha), and males moved further between observations (123 m c.f. 65 m). Core activity centres varied significantly among habitat (P < 0.05) with larger home ranges observed in heathland, a vegetation community which supported comparatively low mammal diversity. No other variables examined including number of fixes, body length, prey abundance, vegetation heterogeneity or fire history explained home range variability. In this system, relatively high mammalian prey diversity and rapid post‐fire vegetation succession may limit prey availability and fire effects as being significant determinants of home range variability in M. spilota.