Within‐group vigilance in red colobus and redtail monkeys

In theory, animals are expected to relax vigilance in the safety of large groups. Four controlled studies of primates have failed to detect relaxed vigilance as group size increases. The counter‐intuitive behavior of primates might arise if another component of vigilance increases with group size, masking any decrease in outward, anti‐predator vigilance. Surveillance of associates is a major component of primate vigilance and might be expected to increase with group size due to an increase in competitive interactions. The present analysis uses data on glances toward associates to determine if within‐group surveillance is related to group size in wild red colobus and redtail monkeys of Uganda. Although males glance at associates more frequently during mating periods and females glance at associates more often when infants are young or out of contact, there was no evidence of a group‐size effect on within‐group surveillance. As with previous studies, primate vigilance patterns reflect reproductive strategies such as infant protection and mate defense. This study joins several others that indicate that primate vigilance is unresponsive to group size. New models that take into account association patterns below the level of the group may be needed. Am. J. Primatol. 48:113–126, 1999. © 1999 Wiley‐Liss, Inc.     

Temporal dynamics of nutrition, parasitism, and stress in colobus monkeys: implications for population regulation and conservation

The need to develop conservation plans calls for the ability to identify ecological factors that influence population density. Because stress is known to affect fecundity and mortality, increasing stress may provide a warning of potential population declines. We examined the effects of temporal variation in nutrition and parasitism on stress in endangered red colobus monkeys in Kibale National Park, Uganda. First, we tested the hypothesis that parasitism and nutrition would individually affect stress levels. We found that periods of poor-quality diet corresponded with an increase in cortisol. Similarly, increases in parasite infections were associated with increased cortisol. Next, we predicted that a poor-quality diet would facilitate increased parasite infections, and that together, they would lead to amplified stress. However, we found no support for such amplification, likely because the quality of the diet had little effect on parasite infections. Third, we tested whether individuals in a larger group were subject to food stress due to greater within-group competition, which would intensify nutritional stress and parasitism, and lead to reduced reproduction. Although we found no evidence to support a group size effect on parasites, cortisol levels in the large group tended to be higher than those in the small group, and the large group had fewer infants per female. The results suggest that parasitism and poor nutrition lead to increased stress which, because they are known to be associated with reduced fecundity and increased mortality, may lead to population declines.     

Killing of a pearl-spotted owlet (Glaucidium perlatum) by male red colobus monkeys (Procolobus tephrosceles) in a forest fragment near Kibale National Park, Uganda

Adult male red colobus (Procolobus tephrosceles) were observed capturing and killing an owl (Glaucidium perlatum) in the Rurama forest fragment near Kibale National Park in western Uganda. The owl was not subsequently eaten by the colobus, their conspecifics, or the other primates present during the attack. Because the incident was preceded by an agonistic encounter with a raptor, the event is best interpreted as a misdirected antipredator behavior. Although antipredator behaviors are not unknown in red colobus, this is the first such incident directed against a raptor to be documented.     

Interactions between overlapping multimale groups of black and white colobus monkeys (Colobus guereza) in the Kakamega Forest,Kenya

Sixteen out of 18 groups of black and white colobus monkeys, or guerezas (Colobus guereza), observed in the Kakamega Forest, Kenya, included more than one adult male. Each group overlapped in its home range with 4–7 other groups, and no group appeared to have exclusive access to any part of its home range. Groups were engaged in intergroup encounters one-quarter of observation time. Encounters often occurred around preferred feeding sites as different groups were attracted to such sites in their overlapping home ranges. Wins and losses during encounters were not dependent on location and a null model suggested that groups were not increasing their encounter rate to defend boundaries, further demonstrating a lack of territoriality. Although guerezas have repeatedly been described as a territorial species living in one-male groups, nonterritorial multimale groups are common in continuous forests. Territorial one-male groups may be usual in narrow riparian forests where resources are limiting, groups are small, and defendability is high, but such organization cannot be regarded as typical of the species. Habitat affects group size, as well as the potential for territoriality, and group size determines the number of adult males per group; therefore, classifying groups as one-male or multimale appears to be an artificial dichotomy. © 1996 Wiley-Liss, Inc.     

Life on the edge: gastrointestinal parasites from the forest edge and interior primate groups

Humans are responsible for massive changes to primate habitats, and one unanticipated consequence of these alterations may be changes in host-parasite interactions. Edges are a ubiquitous aspect of human disturbance to forest landscapes. Here we examine how changes associated with the creation of edges in Kibale National Park, Uganda, alter the parasite community that is supported by two species of African colobines: the endangered red colobus (Piliocolobus tephrosceles) and the black-and-white colobus (Colobus guereza). An analysis of 822 fecal samples from edge and forest interior groups revealed no difference in the richness of parasite communities (i.e., the number of parasite species recovered from the host's fecal sample). However, for both species the proportion of individuals with multiple infections was greater in edge than forest interior groups. The prevalence of specific parasites also varied between edge and forest interior groups. Oesophagostomum sp., a potentially deleterious parasite, was 7.4 times more prevalent in red colobus on the edge than in those in the forest interior, and Entamoeba coli was four times more prevalent in red colobus on the edge than in animals from the forest interior. Environmental contamination with parasites (measured as parasite eggs/gm feces) by red colobus from the edge and forest interior differed in a similar fashion to prevalence for red colobus, but it did not differ for black-and-white colobus. For example, egg counts of Oesophagostomum sp. were 10 times higher in red colobus from the edge than in those from the interior. The less severe infections in the black-and-white colobus relative to the red colobus may reflect the fact that black-and-white colobus raid agricultural crops while red colobus do not. This nutritional gain may facilitate a more effective immune response to parasites by the black-and-white colobus. The fact that animals on the edge are likely not nutritionally stressed raises an intriguing question as to what facilitates the elevated infections in edge animals. We speculate that interactions with humans may be linked to the observed patterns of infections, and hence that understanding the ecology of infectious diseases in nonhuman primates is of paramount importance for conservation and potentially for human-health planning.     

Vigilance in ursine black and white colobus monkeys (Colobus vellerosus): an examination of the effects of conspecific threat and predation

Vigilance is thought to have evolved as an antipredator defense but, in primates, conspecific threat often better explains this behavior. We examined vigilance in one group of Colobus vellerosus inhabiting the Boabeng‐Fiema Monkey Sanctuary in Ghana. We aimed to (1) describe factors affecting vigilance in this population, and (2) examine the importance of predation avoidance and conspecific threat in explaining vigilance patterns. Because of a male takeover preceding the study, our focal group (B2) consisted of six adult males and three adult females. We collected 490 10‐min focal samples (82 hr) from all adults in the group (N=9) from July to November, 2001. To avoid predators, individuals should be more vigilant (i) with fewer neighbors, and (ii) in areas of the canopy with higher predation risks. Conspecific threats can be divided into extra‐ and intra‐group threats. Extra‐group threats should lead to higher vigilance levels (iii) during intergroup encounters, and (iv) in areas where the home range overlaps with other groups of colobus. Intra‐group threats should lead to greater vigilance (v) in the presence of neighbors and (vi) while feeding or occupying food patches (if resources are limiting). Our results best support the hypothesis that vigilance functions primarily to detect extra‐group, conspecific threats. Individuals were most vigilant during intergroup encounters and in areas of range overlap, and monthly vigilance rates were associated with monthly encounter rates. Individuals tended to scan less in proximity to familiar vs. unfamiliar group mates, suggesting that relationship quality may affect colobus vigilance. Finally, predation pressures or anthropogenic disturbances might have influenced vigilance, as individuals were more vigilant low in the canopy. However, this last result could also be due to the lower visibility because of dense foliage or to the fact that the monkeys have access to fewer escape routes when ranging lower in the canopy. Am. J. Primatol. 71:919–927, 2009. © 2009 Wiley‐Liss, Inc.     

Parasites in bloom: flowers aid dispersal and transmission of pollinator parasites within and between bee species

The dispersal of parasites is critical for epidemiology, and the interspecific vectoring of parasites when species share resources may play an underappreciated role in parasite dispersal. One of the best examples of such a situation is the shared use of flowers by pollinators, but the importance of flowers and interspecific vectoring in the dispersal of pollinator parasites is poorly understood and frequently overlooked. Here, we use an experimental approach to show that during even short foraging periods of 3 h, three bumblebee parasites and two honeybee parasites were dispersed effectively onto flowers by their hosts, and then vectored readily between flowers by non-host pollinator species. The results suggest that flowers are likely to be hotspots for the transmission of pollinator parasites and that considering potential vector, as well as host, species will be of general importance for understanding the distribution and transmission of parasites in the environment and between pollinators.     

Stress in Yucatan spider monkeys: effects of environmental conditions on fecal cortisol levels in wild and captive populations

In the Yucatán Peninsula, spider monkeys Ateles geoffroyi yucatanensis are generally found in two contrasting conditions: large tracts of conserved forest or small fragments surrounded by human populations. In the present study, we analyzed fecal cortisol levels of spider monkeys to investigate whether environmental conditions have an influence on stress; specifically, we compared fecal cortisol across individuals living in conserved forests, fragmented forests and captive conditions (zoos and pets). Radioimmunoanalysis of fecal samples from 121 individuals indicated significant differences in mean cortisol for A. g. yucatanensis based on habitat type, with the lowest levels found in the conserved forest condition. The higher cortisol levels in both fragmented forest populations and in captive individuals may be the result of metabolic and behavioral stress. The mean male fecal cortisol concentration was significantly higher than that of females, and the fecal cortisol concentration was higher in the dry season compared with the wet season in a conserved habitat. Therefore, we emphasize the importance of considering sex and seasonality when monitoring fecal cortisol concentrations of spider monkeys, and more generally of frugivores, as they face a seasonal variation in food availability. Finally, our results suggest that forest fragmentation may create long-term stressors for spider monkeys, affecting the viability of populations living under such conditions.     

Shuttlebox avoidance in rhesus monkeys: effects on plasma cortisol and beta-endorphin

Groups of monkeys either extensively pretrained to avoid shocks in a shuttlebox or with minimal prior experience were compared for plasma cortisol and beta-endorphin levels immediately following: (1) an exposure to the box with no shock, (2) the box providing repeated inescapable shocks or (3) a re-exposure to the box, again with no shock presentation. Mere exposure to the unfamiliar box elevated plasma cortisol just as much as exposure + shock did when inexperienced monkeys were tested. However, animals with a history of previously successful shock avoidance showed smaller elevations when exposed to the box alone, than they did when inescapable shock was received. Plasma beta-endorphin levels following shuttlebox exposure showed only a sporadic pattern of elevations in either inexperienced or pretrained monkeys. However, levels of beta-endorphin as determined under control conditions in the home cage were lower in pretrained animals, as were plasma levels of cortisol. The results indicate that behavioral factors may effect plasma cortisol and beta-endorphin following both acute and chronic shuttlebox experience.     

Inbred women in a small and isolated Swiss village have fewer children

Despite overwhelming evidence for a negative effect of inbreeding on fitness in plants and nonhuman animals, the exact nature of its effect in humans remains subject to debate. To obtain a better understanding of the effects of inbreeding on reproductive success in humans, we reconstructed the genealogies of the current inhabitants of a small and isolated Swiss village and used these to estimate the level of inbreeding of both members of all married couples, as well as their relatedness (i.e. the level of inbreeding of their offspring). Although there was no effect of parental relatedness on the number of children a couple had, we found that inbred mothers, but not inbred fathers, had significantly fewer children. Thus, although related couples did not have fewer children themselves, their inbred daughters did leave them with fewer grandchildren. Thereby, we provide evidence for the existence of inbreeding depression in human fertility, also in relatively outbred and egalitarian communities.     

Aggression and social support predict long‐term cortisol levels in captive tufted capuchin monkeys (Cebus [Sapajus] apella)

Many nonhuman primates live in complex social groups in which they regularly encounter both social stressors such as aggression and social support such as that provided by long‐term affiliative relationships. Repeated exposure to social stressors may result in chronically elevated cortisol levels that can have deleterious physical effects such as impaired immune function, cardiovascular disease, and reduced brain function. In contrast, affiliative social relationships may act as a buffer, dampening the release of cortisol in response to acute and chronic stressors. Understanding how social stressors and social support predict cortisol levels is therefore essential to understanding how social situations relate to health and welfare. We studied this relationship in 16 socially housed captive brown capuchin monkeys (Cebus [Sapajus] apella) by comparing long‐term hair cortisol levels with behavioral measures of social stress (dominance rank, rank certainty, and amount of aggression received) and social support (amount of affiliation and centrality in the affiliative social network of the group). Dominance rank, rank certainty, amount of affiliation, and age were not significant predictors of long‐term cortisol levels in this population. Instead, long‐term cortisol levels were positively related to the amount of aggression received and negatively related to centrality in the affiliative social network of the group. This pattern may be attributed to the species’ socially tolerant dominance system and to the availability of social support across the dominance hierarchy.     

Individual and seasonal variation in fecal testosterone and cortisol levels of wild male tufted capuchin monkeys, Cebus apella nigritus

This study tested the "challenge hypothesis" and rank-based predictions for temporal steroid production in male tufted capuchin monkeys, Cebus apella. Fecal samples (n = 209) collected from six wild males were analyzed for testosterone and cortisol concentration by enzyme immunoassay. The temporal pattern in male steroid production was compared to female sexual activity and rates of male aggression. The top-ranking adult male did not differ from other adult males in testosterone or cortisol concentration. Mean adult testosterone was significantly higher than mean subadult testosterone throughout the year. There was a clear elevation of testosterone and cortisol in both adult and subadult males during the peak of adult female sexual activity after the birth season. In fact, the magnitude of increase in testosterone was higher than predicted for a species with low male-male aggression. However, there was no difference between nonbreeding baseline testosterone levels during the birth season, and the "breeding" baseline of testosterone in males found during asynchronous female sexual activity. Of all behavioral indices examined, the distribution of female-maintained consortships was the best predictor of mean adult male testosterone concentrations. Although in many species, elevated testosterone coincides with increased male-male aggression, in the present study, the sustained high-magnitude increase in steroids during the peak of adult female sexual activity was associated with a relatively low rate of male-male intragroup aggression.     

Poststress levels of lysozyme and cortisol in adult rainbow trout: heritabilities and genetic correlations

Lysozyme response in stressed rainbow trout was compared with measurements of poststress cortisol activity. Estimates of heritability of lysozyme and cortisol were both moderate-to-high and both traits displayed positive genetic correlations in pair-wise comparisons of stress exposures. Genetic correlations between lysozyme and cortisol in stressed rainbow trout tended to be negative, although insignificant. Neither lysozyme, nor cortisol exhibited significant correlations with serum haemolytic activity. It is concluded that the data do not confirm earlier suggestions that lysozyme should be superior to cortisol in consistency of stress response in rainbow trout.     

The radiation of red colobus monkeys (Primates,Colobinae): morphological evolution in a clade of endangered African primates

Red colobus monkeys are a group of African monkeys that include some of the most endangered primate populations. Despite urgently needing to understand the importance of particular populations for preserving the biodiversity of this lineage, their evolutionary relationships remain poorly understood, and their taxonomy is unstable, and often enigmatic. Data on behaviour, ecology, genetics, and morphology are thus strongly needed to address taxonomic issues that are not only relevant for primatologists, but also for conservation biologists. In this study, we investigated the morphological diversity and evolution of red colobus by examining the cranial variation of 369 individuals from most living populations. Crania were measured using a set of 64 anatomical landmarks, and were analysed using geometric morphometric methods for the study of three‐dimensional landmark coordinates. We found significant differences among most of the populations traditionally described on the basis of pelage colour and geographic distribution. However, differences tended to be smaller within biogeographic assemblages, which might be related to mountain refugia during periods of forest contraction in the Pleistocene.We also found a tendency towards large taxonomic distances, which suggested that populations might have originated earlier than has been traditionally thought, a result congruent with a recent molecular phylogenetic analysis. However, the distinctive forms of East African relict populations might be related to an acceleration of morphological evolution in small peripheral isolates, under strong selective pressures. This indicates that small and isolated populations, which are also the most endangered ones, might indeed be unique representatives of the red colobus radiation, and hence contribute to its biodiversity significantly. However, in‐ depth morphological studies of red colobus, particularly those in peripheral populations that tend to be rare in the wild, as well as in museum collections, is hampered by a paucity of data. In these cases, populations might be extinct before primatologists and conservationsts can even appreciate what was lost.     

The influence of a magnesium-rich marine extract on behaviour,salivary cortisol levels and skin lesions in growing pigs

Growing pigs can display undesirable behaviours, reflecting or causing poor welfare. Addition of magnesium (Mg) to the diet could reduce these, as Mg supplementation has been associated with improved coping ability in response to stress. This study examined the effect of supplementation with a Mg-rich marine extract-based product (Supplement) on the behaviour, skin and tail lesion scores and salivary cortisol concentrations of growing pigs. At weaning (28 days), 448 piglets were assigned to either Control or Supplement (0.05%) diets in single-sex groups of 14. Four weeks later (c. 17 kg), pigs were blocked according to weight and back test scores. Seven piglets from each pen were mixed with seven from another pen of the same sex and dietary treatment to yield the following groups: control male, Supplement male, control female and Supplement female (n = 4 of each). This marked the start of the 9-week experimental period. Instances of the following behaviours were recorded in each pen for 8 × 2 min periods 1 day/week: aggression (fight, head-knock and bite); harmful (tail-in-mouth, ear-chewing and belly-nosing); and sexual/mounting behaviour. Four focal pigs were selected from each pen, and their behaviour was continuously recorded for 2 × 5 min periods on the same day. Saliva was collected once per week at 1000 h by allowing pigs to chew on a cotton bud for c. 1 min. Salivary cortisol was analysed in duplicate by an enzyme immunoassay. Skin and tail lesions were scored according to severity 1 day/week. There were fewer aggressive incidents in Supplement pens (P < 0.01), and mounting behaviour (performed only by males) was almost three times lower in Supplement than in control pens (P < 0.01). However, there was no effect of Supplement on the incidence of each of the harmful behaviours. Behaviour of the focal pigs showed no treatment effect on the duration or incidence of aggressive behaviour. However, Supplement pigs spent less time performing harmful behaviours compared with control pigs (P < 0.001). Supplement had no effect on the occurrence or severity of tail-biting outbreaks or on tail lesion scores. However, Supplement females had lower skin lesion scores, in particular in the ears and shoulders (P < 0.01). Finally, Supplement pigs had lower salivary cortisol concentrations (P < 0.01). Mounting is a major welfare concern in uncastrated pigs, and therefore this represents an important welfare benefit of Supplement. Reduced salivary cortisol, in conjunction with reduced skin lesion scores in supplemented females, suggests that addition of a Mg-rich marine extract improved pig welfare in this system.