Capture,immobilization, and Global Positioning System collaring of olive baboons (Papio anubis) and vervets (Chlorocebus pygerythrus): Lessons learned and suggested best practices

As the value of Global Positioning System (GPS) technology in addressing primatological questions becomes more obvious, more studies will include capturing and collaring primates, with concomitant increased risk of adverse consequences to primate subjects. Here we detail our experiences in capturing, immobilizing, and placing GPS collars on six olive baboons (Papio anubis) in four groups and 12 vervet monkeys (Chlorocebus pygerythrus) in five groups in Kenya. We captured baboons with cage traps and vervets with box traps, immobilized them, and attached GPS collars that were to be worn for 1 year. Adverse consequences from the trapping effort included incidental death of two nonsubjects (an adult female and her dependent infant), temporary rectal prolapse in one baboon, superficial wounds on the crown of the head in two vervets, and failure to recapture/remove collars from two baboons and two vervets. Obvious negative effects from wearing collars were limited to abrasions around the neck of one vervet. A possible, and if so, serious, adverse effect was greater mortality for collared adult female vervets compared with known uncollared adult female vervets, largely due to leopard (Panthera pardus) predation. Collared animals could be more vulnerable to predation because trapping favors bolder individuals, who may also be more vulnerable to predation, or because collars could slow them down or make them more noticeable to predators. Along with recommendations made by others, we suggest that future studies diversify trapping bait to minimize the risk of rectal prolapse, avoid capturing the first individuals to enter traps, test the movement speeds of collared versus noncollared animals, include a release system on the collars to avoid retrapping failure, and publish both positive and negative effects of capturing, immobilizing, and collaring.     

Response of fecal cortisol to stress in captive chimpanzees (Pan troglodytes)

This study examined whether fecal cortisol could be used as an index of stress responses. The stress responsiveness of fecal cortisol was tested with a stressor known to stimulate adrenal activity, the stress of anesthesia. Daily fecal and urine samples were collected from four captive chimpanzees (Pan troglodytes) before and after anesthetizations with Telazol^®/Ketasat^®. Tests of assay validity indicated that cortisol was measurable in chimpanzee fecal extracts. Fecal cortisol concentrations were significantly elevated 2 days after anesthetization, with elevations in seven of the eight treatments. The posttreatment peak was significantly greater than baseline values in three of the four subjects. Both fecal concentrations and proportionate increases in response to stress were significantly correlated with the corresponding values in urinary cortisol, confirming the stressfulness of these procedures and the stress responsiveness of fecal cortisol. These findings provide evidence for the application of fecal cortisol as a noninvasive index of physiologic stress in nonhuman primates. Am. J. Primatol. 44:57–69, 1998. © 1998 Wiley-Liss, Inc.     

Capture, anesthesia, and disturbance of free-ranging brown bears (Ursus arctos) during hibernation

We conducted thirteen immobilizations of previously collared hibernating two- to four-year-old brown bears (Ursus arctos) weighing 21-66 kg in central Sweden in winter 2010 and 2011 for comparative physiology research. Here we report, for the first time, an effective protocol for the capture and anesthesia of free-ranging brown bears during hibernation and an assessment of the disturbance the captures caused. Bears were darted in anthill, soil, or uprooted tree dens on eleven occasions, but two bears in rock dens fled and were darted outside the den. We used medetomidine at 0.02-0.06 mg/kg and zolazepam-tiletamine at 0.9-2.8 mg/kg for anesthesia. In addition, ketamine at 1.5 mg/kg was hand-injected intramuscularly in four bears and in six it was included in the dart at 1.1-3.0 mg/kg. Once anesthetized, bears were removed from the dens. In nine bears, arterial blood samples were analyzed immediately with a portable blood gas analyzer. We corrected hypoxemia in seven bears (PaO(2) 57-74 mmHg) with supplemental oxygen. We placed the bears back into the dens and antagonized the effect of medetomidine with atipamezole. Capturing bears in the den significantly increased the risk of den abandonment. One of twelve collared bears that were captured remained at the original den until spring, and eleven, left their dens (mean ± standard deviation) 3.2±3.6 (range 0.5-10.5) days after capture. They used 1.9±0.9 intermediate resting sites, during 6.2±7.8 days before entering a new permanent den. The eleven new permanent dens were located 730±589 m from the original dens. We documented that it was feasible and safe to capture hibernating brown bears, although they behaved differently than black bears. When doing so, researchers should use 25% of the doses used for helicopter darting during the active period and should consider increased energetic costs associated with den abandonment.     

Differences between domesticated Eurasian and Japanese indigenous strains of the common carp (Cyprinus carpio) in cortisol release following acute stress

To understand the differences in the stress sensitivities between domesticated Eurasian and Japanese indigenous strains of common carp (Cyprinus carpio Linnaeus 1758), we compared concentrations of cortisol released into the water in response to handling of the two types of strains. At 0.5 and 2 h after the handling treatment, the cortisol emission was greater from the Eurasian strain than from the Japanese strain. There were no differences between the strains in the cortisol levels after 4 to 24 h. We found that Eurasian strains exposed to the unnatural stressor (i.e., handling) exhibited a higher cortisol response than the Japanese strain.     

The cortisol stress response in male round goby (Neogobius melanostomus): effects of living in polluted environments?

Acute exposure to contaminants frequently induces stress, but prolonged exposures, such as those experienced by individuals in wild populations, can impair the capacity to mount a stress response. Using the round goby (Neogobius melanostomus), a small benthic fish and potential sentinel species for habitat contamination in the Great Lakes, we explored the impacts of living in highly polluted areas. Round goby were collected from highly contaminated and less contaminated areas of Hamilton Harbour (a well-known site of polycyclic aromatic hydrocarbon (PAH) and heavy metal contamination). The cortisol stress responses of fish from sites of high and low contamination were compared using an EIA assay on blood collected (n?=?112) either prior to or 0, 10, 30, 60, 240 min and 24 h following the application of a 4-min confined air exposure stressor. Plasma cortisol levels were elevated at 10 and 30 min post-stressor (100.3 and 87.5 ng/mL), and returned to levels similar to baseline (22.3 ng/mL) 1 h after the stressor. In contrast to predictions, round goby from areas of high and low contamination had similar cortisol levels at all timepoints. We also monitored stress responses immediately after a chasing stressor (n?=?19). During the chasing stressor, contaminated-site round goby exhausted faster than individuals from a less contaminated site, although they had similar levels of plasma cortisol (23.5 versus 20.9 ng/mL) and lactate (2.53 versus 1.98 mmol/L). Our results indicate that not all fishes may demonstrate impaired stress responses, even in highly contaminated habitats; however, such animals may still have increased vulnerability to predation.     

Reproductive tactics influence cortisol levels in individual male gray-cheeked mangabeys (Lophocebus albigena)

Concentration of the hormone cortisol is often used as an indicator of stress, and chronically high cortisol levels are often associated with poor health. Among group living animals that compete for resources, agonistic social interactions can be expected to contribute to variation in cortisol levels within and among individuals over time. Reproductive tactics of males can change with individual quality, relatedness, and social structure, and affect cortisol levels. In gray-cheeked mangabey (Lophocebus albigena) groups, male rank is an important factor in social interactions, and males also move between groups while actively competing for females or sneaking copulations. During a 20-month study we observed the social behavior and collected 461 fecal samples from 24 adult male gray-cheeked mangabeys from five groups in Kibale National Park, Uganda. Aggressive interactions and the presence of females at the peak of sexual swelling were associated with elevated cortisol concentrations in all males. Independently, dominant (i.e., highest-ranking) males within groups had higher cortisol concentrations than subordinate males, and immigrant males had higher cortisol concentrations than dominant males.     

Taking the sting out of darting: Risks,restraint drugs and procedures for the chemical restraint of Southern Hemisphere otariids

The need to manage otariid populations has necessitated the development of a wide range of capture methods. Chemical restraint by remote drug delivery (i.e., darting) is a highly selective method that can be used to facilitate otariid capture in a range of scenarios, when other methods may be impracticable. However, the risks associated with darting otariids are not widely known and guidelines necessary to promote and refine best practice do not exist. We review the risks associated with darting and in light of our findings, develop darting guidelines to help practitioners assess and minimize risks during capture, anesthesia and recovery. Published studies reveal that mortalities associated with darting predominantly result from complications during anesthetic maintenance (e.g., prolonged respiratory depression, apnea, or hyperthermia), rather than from complications during capture or recovery. In addition to monitoring vital signs and proper intervention, the risk of irreversible complications during anesthesia can be reduced by administering drug doses that are sufficient to enable the capture and masking of animals, after which anesthetic depth can be regulated using gas anesthesia.     

Digestive capacity, growth and social stress in newly-metamorphosed Japanese flounder (Paralichthys olivaceus)

Hierarchies readily appear when rearing flounders through metamorphosis in space-limited conditions. In this experiment, subordinate fish were stressed, as suggested by their elevated cortisol level compared to dominant fish. Subordinate fish, although of smaller size than the dominant fish, showed no suppressed digestive capacity. By separating the two hierarchical groups into different tanks at low density, the cortisol level of the subordinate fish substantially decreased. The removal of the stressor also resulted in an increase in digestive function and improved coloration. Also, compensatory growth in length but not in weight was observed in the subordinate group, suggesting that the subordinate fish devoted their energy to increase their length. These results imply that the climax of flounder metamorphosis (i.e. the settlement stage) is a highly sensitive period, where social interactions may induce high levels of stress. However, Japanese flounder early juveniles prove to have a high recovery capacity from stress and show to allocate energy preferentially to growth in length. This seems to be an adaptation to diminish the probability of death by predation.     

Psychosocial stressor effects on cortisol and ghrelin in emotional and non-emotional eaters: Influence of anger and shame

Food consumption in stressful situations vary as a function of individual difference factors (e.g., emotional vs. non-emotional eating), and may be related to hormonal responses elicited by the stressful event. These hormonal responses may be tied to specific emotions elicited by the stressful event. The present investigation examined the emotional and hormonal (cortisol, ghrelin) responses of high and low emotional eaters following a laboratory stressor (Trier Social Stress Test; TSST). Women (n = 48) either high or low in emotional eating status were tested in a TSST or served as controls during which blood samples were taken for analysis of cortisol and ghrelin, both of which have been implicated in eating and in response to stressors. The TSST promoted elevated cortisol levels, being somewhat more pronounced in emotional than in non-emotional eaters. Both shame and anger were provoked by the TSST, and although both these emotions were correlated with cortisol levels, only anger significantly mediated the relationship between the stressor and cortisol levels. As well, baseline ghrelin levels in low emotional eaters exceeded that of high emotional eaters, and increased moderately in response to the stressor situation, irrespective of emotional eating status. Interestingly, when provided with food, ghrelin levels declined in the non-emotional eaters, but not in emotional eaters. The possibility is offered that the lack of a decline of ghrelin in emotional eaters may sustain eating in these individuals.     

Darting and marking techniques for an arboreal forest monkey,Cercopithecus ascanius

Techniques are described for capturing and marking redtail monkeys (Cercopithecus ascanius). An air-powered darting rifle and syringe darts loaded with a Ketamine-Rompun mixture were used for capture. Ketamine was used for maintaining anesthesia. Monkeys were darted 48 times and captured 27 times. In 24 of the 27 captures, the monkeys were released unharmed. Adult males were marked with radiotransmitters attached to collars of nylon webbing. Females received nylon webbing collars with colorcoded plastic washers for identification.     

Measuring Hair Cortisol Concentrations to Assess the Effect of Anthropogenic Impacts on Wild Chimpanzees (Pan troglodytes)

Non-human primates face major environmental changes due to increased human impacts all over the world. Although some species are able to survive in certain landscapes with anthropogenic impact, their long-term viability and fitness may be decreased due to chronic stress. Here we assessed long-term stress levels through cortisol analysis in chimpanzee hair obtained from sleeping nests in northwestern Uganda, in order to estimate welfare in the context of ecotourism, forest fragmentation with human-wildlife conflicts, and illegal logging with hunting activity (albeit not of primates), compared with a control without human contact or conflict. Concerning methodological issues, season [F(2,129) = 37.4, p < 0.0001, r² = 0.18] and the age of nests [F(2,178) = 20.3, p < 0.0001, r² = 0.11] significantly predicted hair cortisol concentrations (HCC). With regard to effects of anthropogenic impacts, our results neither showed elevation of HCC due to ecotourism, nor due to illegal logging compared to their control groups. We did, however, find significantly increased HCC in the fragment group compared to chimpanzees living in a nearby intact forest [F(1,88) = 5.0, p = 0.03, r² = 0.20]. In conclusion, our results suggest that hair cortisol analysis is a powerful tool that can help understanding the impact of anthropogenic disturbances on chimpanzee well-being and could be applied to other great ape species.     

Do Nematode Infections of Red Colobus (Procolobus rufomitratus) and Black-and-White Colobus (Colobus guereza) on Humanized Forest Edges Differ from Those on Nonhumanized Forest Edges?

Forested edges, especially those that border humanized landscapes, provide opportunities for nonhuman primates and people to interact, and such interactions are predicted to alter disease dynamics. Given the rapid expansion of edge habitats globally, understanding changes occurring on edges is important in evaluating primate behavioral ecology and developing conservation plans. Our research investigates predictions concerning how gastrointestinal parasite and stress levels (cortisol) in red colobus and black-and-white colobus (Procolobus rufomitratus; Colobus guereza) in Kibale National Park, Uganda, differ between humanized and nonhumanized forest edges. We found Trichuris sp., an unidentified strongyle, and Strongyloides sp. in the fecal samples. Results did not generally support our expectation that humanized forest edges increase parasite infection and, counter to what we predicted, fecal cortisol did not differ between habitats, suggesting that proximity to edges and/or to humans did not result in increased stress. We conclude that broad habitat classifications, e.g., “humanized,” may be too general to identify consistent differences in parasite infection, as other factors, specific to the parasite (e.g., life cycled), host (e.g., immune systems strength), or environment (e.g., moisture level), likely also play important roles.     

Physiological stress responses of two species of coral trout (Plectropomus leopardus and Plectropomus maculatus)

The physiological responses of two species of coral trout (Plectropomus maculatus and Plectropomus leopardus) to capture, shallow water and low salinity stressors were investigated. The responses of P. maculatus and P. leopardus to capture stress were characterised by rapid and transient increases in glucose, haemoglobin, haematocrit and lactate, as well as an equally dramatic but delayed increase in cortisol levels that persisted for at least 72 h. The magnitude and duration of the response to capture stress was very similar in both species. In contrast, the levels of cortisol, glucose, lactate, haemoglobin and haematocrit were generally elevated sooner and to higher levels in P. maculatus than in P. leopardus after exposure to shallow water stress. Coral trout exposed to reduced salinity showed minimal changes in cortisol, glucose, lactate, haemoglobin and haematocrit, but such changes were not characteristic of a non-specific response to stress. Thus, the physiological stress responses of coral trouts are species-specific and dependent on the nature of the stressor. This observation probably reflects different cortical processes in the brains of P. maculatus and P. leopardus-a result that may be related to the differential variability of the respective environments in which the two species habit.     

Prey selection and the functional response of sea stars (Asterias vulgaris Verrill) and rock crabs (Cancer irroratus Say) preying on juvenile sea scallops (Placopecten magellanicus (Gmelin)) and blue mussels (Mytilus edulis Linnaeus)

Predators in nature include an array of prey types in their diet, and often select certain types over others. We examined (i) prey selection by sea stars (Asterias vulgaris) and rock crabs (Cancer irroratus) when offered two prey types, juvenile sea scallops (Placopecten magellanicus) and blue mussels (Mytilus edulis), and (ii) the effect of prey density on predation, prey selection, and component behaviours. We quantified predation rates, behavioural components (proportion of time spent searching for prey, encounter probabilities) and various prey characteristics (shell strength, energy content per prey, handling time per prey) to identify mechanisms underlying predation patterns and to assess the contribution of active and passive prey selection to observed selection of prey. Sea stars strongly selected mussels over scallops, resulting from both active and passive selection. Active selection was associated with the probability of attack upon encounter; it was higher on mussels than on scallops. The probability of capture upon attack, associated with passive selection, was higher for mussels than for scallops, since mussels can not swim to escape predators. Sea stars consumed few scallops when mussels were present, and so did not have a functional response on scallops (the target prey). Rock crabs exhibited prey switching: they selected mussels when scallop density was very low, did not select a certain prey type when scallop density was intermediate, and selected scallops when scallop density was high relative to mussel density. The interplay between encounter rate (associated with passive selection) and probability of consumption upon capture (associated with both active and passive selection) explained observed selection by crabs. Scallops were encountered by crabs relatively more often and/or mussels less often than expected from random movements of animals at all scallop densities. However, the probability of consumption varied with scallop density: it was lower for scallops than mussels at low and intermediate scallop densities, but tended to be higher for scallops than mussels at high scallop densities. When mussels were absent, crabs did not have a functional response on scallops, but rather were at the plateau of the response. When mussels were present with scallops at relatively low density, crabs exhibited a type II functional response on scallops. Our results have implications for the provision of protective refuges for species of interest (i.e., scallops) released onto the sea bed, such as in population enhancement operations and bottom aquaculture.     

Acutely Elevated Cortisol in Response to Stressor Is Associated with Attentional Bias Toward Depression-Related Stimuli but Is Not Associated with Attentional Function

Cortisol induces attentional bias toward a negative stimulus and impaired attentional function. Depressed individuals have high levels of cortisol, and exhibit an attentional bias toward a depression-related stimulus and impaired processing speed and executive attention, which are components of attentional function. Therefore, the study tested the hypotheses that an acute increase in cortisol in response to a stressor is associated with attentional bias toward a depression-related stimulus and impaired processing speed and executive attention. Thirty-six participants were administered the dot-probe task for the measurement of attentional bias toward a depression-related stimulus and the Trail Making Test A and B for the measurement of processing speed and executive attention before and after a mental arithmetic task. It was revealed that attentional bias toward a depression-related stimulus following the stressor was observed only among the responders (i.e., participants with cortisol elevation in response to a stressor). On the other hand, no differences in the performance of processing speed and executive attention were noted between the responders and non-responders. The results indicate that acutely elevated cortisol is related to attentional bias, but is not related to processing speed and executive attention. The results have an implication for the etiology of depression.     

The effects of capture, handling, confinement and ectoparasite load on plasma levels of cortisol, glucose and lactate in the coral reef fish Hemigymnus melapterus

Tropical labrids Hemigymnus melapterus sampled underwater had low plasma levels of cortisol, glucose, and lactate. Plasma cortisol levels were elevated by capture stress within 5–6 min, while glucose and lactate levels were not. Plasmalevels of cortisol and glucose increased after 2–4 h of handling and transport to the laboratory. Levels of cortisol and glucose fell with laboratory acclimation back to values similar to those found in wild fish. Parasitism by gnathiid isopods across an order of magnitude of isopod numbers had no effect on plasma levels of cortisol or glucose. Thus, H. melapterus has a stress response similar to that shown by temperate species, and relatively high parasite loads are not apparently stressful to fish in the wild. This may be related to the counterproductive effects of physiological stress responses on the immune system or behaviour-modulated processes that counter parasitic invasion.     

Costs and Benefits of Radio-collaring on the Behavior,Demography, and Conservation of Owl Monkeys (<Emphasis Type="Italic">Aotus azarai</Emphasis>) in Formosa,Argentina

The benefits to researchers of capturing and collaring free-ranging primates are numerous, but so are the actual and potential costs to the individuals. We aimed to 1) evaluate quantitatively the possible demographic long-term costs of radio-collaring a free-ranging primate species, and 2) evaluate qualitatively the costs to the subjects and the overall benefits to the research program that results from monitoring a large number of groups with collared individuals during many years. Between 2000 and 2009, we captured, recaptured, and radio-collared 146 owl monkeys (Aotus azarai) to study the behavior, demography, and genetics of the species. To evaluate the potential long-term costs of the collaring procedures on the population, we compared the demographic composition of groups (n = 20) in our core study area with those of undisturbed groups (n = 20) in a control area within the same forest. Groups in both areas ranged in size between 2 and 5 individuals. Surprisingly, group size tended to be larger among the study groups owing to more infants and juveniles in those groups than in the control groups. The benefits to the research program have included, among others, the reliable identification of individuals, increased sample sizes, the recovery of specimens, studies of dispersal, outreach activities, and conservation education. Still, some of the benefits will become tangible only when the project persists on time; is fully approved and supported by local authorities; and has broad community participation, as well as conservation and education goals. Thus, any serious initiative to capture and collar individuals should be the result of an extremely careful evaluation of benefits and costs.     

Interspecies transmission of simian foamy virus in a natural predator-prey system

Simian foamy viruses (SFV) are ancient retroviruses of primates and have coevolved with their host species for as many as 30 million years. Although humans are not naturally infected with foamy virus, infection is occasionally acquired through interspecies transmission from nonhuman primates. We show that interspecies transmissions occur in a natural hunter-prey system, i.e., between wild chimpanzees and colobus monkeys, both of which harbor their own species-specific strains of SFV. Chimpanzees infected with chimpanzee SFV strains were shown to be coinfected with SFV from colobus monkeys, indicating that apes are susceptible to SFV superinfection, including highly divergent strains from other primate species.     

Insect Seed Predators in Erythrina falcata (Fabaceae): Identification of Predatory Species and Ecological Consequences of Asynchronous Flowering

Seed predation by insects exerts negative effects on plant reproduction by limiting the supply of seeds and preventing germination. Seed predators of the family Fabaceae are usually generalists, which increases the rate of predation. One strategy to minimize seed predation, developed by plants from temperate regions, is “escape in time,” i.e., flowering before or after the peak of predation. For tropical species, few studies have investigated the strategies used by plants to minimize seed predation. Here, using Erythrina falcata, a tropical species of Fabaceae, we test three main hypotheses: (i) escape in time is a mechanism used by E. falcata to minimize seed predation, (ii) the predators of E. falcata seeds are generalists, and (iii) the biometric variables of the pods can influence seed predation. In order to test these hypotheses, we determined the flowering time of E. falcata, rate of seed predation, the predators insects, and biometric variables of the pods. The analyzed trees were grouped into three classes: “early,” “peak,” and “late” flowering. The average seed predation rates on trees in the early and late classes were 65% and 50%, respectively, and in the peak class, 80%; thus, our first hypothesis can be accepted. Three species of Lepidoptera and two of Coleoptera were found preying on E. falcata seeds. These species were observed to be generalist predators; thus, our second hypothesis can be accepted. The biometric variables of the pods cannot influence seed predation rate. The ecological consequences of asynchronous flowering on plants and insects are discussed.     

Aquaculture implications of growth variation in the African catfish: Heterobranchus longifilis (Val.) reared under controlled conditions

Individual (mass) selection experiments were undertaken on different batches of Heterobranchus longifilis siblings to investigate factors such as significant size variation among larvae and juveniles that influence the darting (shooting) phenomenon. Darting was studied by subjecting treatment groups of fish larvae to (1) different feeding levels: 3% and 10% of body weight, and continuously at equal stocking rate. (2) different stocking rates: 600, 300 and 150 fish/30 L at the same feeding level. (3) effects of introduction of shelter under similar stocking and feeding levels and regime. A darting (shooting) event was registered when fish darted abruptly over a length of approximately three times the estimated total body length. The study concluded that food and density were the critical epigenetic factors responsible for size variation in juvenile H. longifilis.