When Northern Pigtailed Macaques (Macaca leonina) Cannot Select for Ideal Sleeping Sites in a Degraded Habitat

International Journal of Primatology - Primates must select sleeping sites carefully to maximize fitness. In habitats with diminished quality and availability of resources, sleeping site selection...     

Influence of Food Resources on the Ranging Pattern of Northern Pig-tailed Macaques (Macaca leonina)

Food availability may influence primates’ home range size and use. Understanding this relationship may facilitate the design of conservation strategies. We aimed to determine how fruit availability influences the ranging patterns of a group of northern pig-tailed macaques (Macaca leonina) living around the visitor center of Khao Yai National Park, Thailand. We predicted that macaques would increase their range during low fruit abundance periods to gather high-quality food and that they would go where there are more fruits or more fruits of particular species. We also predicted that human food, linked to human presence, would attract the macaques. We followed the macaques and recorded their diet and movements within their home range. We superimposed a grid on kernels defining the monthly home range surface to compare spatially macaques’ travel and the availability of fruits measured on botanical transects. Our results showed that the macaques increased their monthly home range in March, probably to obtain newly available fruits. During high fruit abundance seasons, they spent more time near particular fruit species. In August and September, although fruits became rare again, macaques kept their home range large, perhaps to find enough fruits as supplies dwindled. Finally, from October to February, they decreased their monthly home range size while consuming human food, a high-quality item. In conclusion, the macaques used several ranging strategies according to fruit availability. However, we think that, without human food, macaques would tend to increase their range during low fruit abundance periods, as predicted.     

Frugivory and Seed Dispersal by Brown Lemurs in a Malagasy Tropical Dry Forest

In the Ankarafantsika tropical dry forest (northwestern Madagascar), the common brown lemur (Eulemur fulvus fulvus) is the largest frugivore and probably the sole disperser of large‐seeded plants (seed diameter > 10 mm). To investigate seed dispersal by this primate, I recorded the feeding activities of a troop; also conducted fecal analyses, germination trials on defecated seeds, and a vegetation survey over 1 yr (beginning Dec 2006). Brown lemurs mostly consumed fruit (68%). The fruit of Vitex beraviensis was the most exploited resource (21% of total feeding time). Among dung samples, 1126 contained intact seeds of 70 plant species, with a median of six seeds and two species per sample. These data indicate that the brown lemur population dispersed approximately 9854 seeds/km²/d. Although the number of annually defecated seeds was overwhelmingly the largest in Grewia triflora, many of the small seeds were often clumped in dung piles. In contrast, large seeds of V. beraviensis occurred in the largest number of dung samples. The rate and time of seed germination in V. beraviensis were improved by passage through brown lemur guts. Therefore, V. beraviensis may readily establish seedlings in sites of brown lemur fecal deposition. Vitex beraviensis and brown lemurs are probably involved in a strong mutualism. Twenty‐three large‐seeded plants were probably dependent on brown lemurs for seed dispersal and some of these species were common trees in the forest. Maintenance of these key plant–animal interactions will probably contribute to the conservation of species diversity and intact regeneration of the Ankarafantsika forest.     

Frugivory and Seed Dispersal by the Lowland Tapir Tapirus terrestris in the Peruvian Amazon

The lowland tapir Tapirus terrestris is the largest herbivore in the Neotropics and feeds on a large quantity of fruits, often ingesting the seeds and defecating them intact. Seed dispersal by the lowland tapir in the southwestern Amazon was studied by examining seeds from 135 dung samples collected between 2005 and 2007. Seeds of a total of 122 plant species were identified, representing 68 genera and 33 families. The species accumulation curve showed that more species can be expected with further sampling. Many species (45%) were only encountered once, and only 10 percent of all species were found in >10 samples, indicating that the lowland tapir is an opportunistic forager. Seed diversity showed a clear seasonal pattern and was highly correlated with fruit availability. Seed diameter ranged from <1 to 25 mm with 81 percent <10 mm diam. The size distribution of seeds found in lowland tapir dung generally followed that of seeds found in the forest, but had a lower proportion of seeds in the smallest size class (<2.5 mm) and a larger proportion found in the largest size class (20–25 mm). The diversity of seeds encountered in dung of the lowland tapir in this study was much higher than in previous studies. We conclude that the lowland tapir is a potential disperser for a large number of plant species, including many that previously have been thought to be dispersed only by large primates.     

Simian Varicella Virus in Pigtailed Macaques (Macaca nemestrina): Clinical, Pathologic, and Virologic Features

Simian varicella virus (SVV; Cercopithecine herpesvirus 9) is a naturally occurring herpesvirus of nonhuman primates. Here we present the clinical, pathologic, and virologic findings from 2 cases of SVV in adult female pigtailed macaques (Macaca nemestrina). The initial case presented with hyperthermia and a diffuse inguinal rash which spread centripetally, progressing to vesiculoulcerative dermatitis of the trunk, face, and extremities. At 96 h after presentation, the animal was anorexic and lethargic and had oral and glossal ulcerations. Euthanasia was elected in light of the macaque''s failure to respond to clinical treatment. Seven days after the first case was identified, a second macaque presented with a vesicular rash and was euthanized. Gross necropsy lesions for both cases included vesicular, ulcerative dermatitis with mucocutaneous extension and hepatic necrosis; the initial case also demonstrated necrohemorrhagic gastroenterocolitis and multifocal splenic necrosis. Histology confirmed herpetic viral infection with abundant intranuclear inclusion bodies. Immunofluorescence assays detected antibodies specific for SVV. PCR assays of vesicular fluid, tissue, and blood confirmed SVV and excluded varicella–zoster virus (Human herpesvirus 3). Serology for Macacine herpesvirus 1 (formerly Cercopithecine herpesvirus 1), poxvirus (monkeypox), and rubella was negative. Banked serum samples confirmed SVV exposure and seroconversion. Investigation into the epidemiology of the seroconversion demonstrated a SVV colony prevalence of 20%. The described cases occurred in animals with reconstituted immune systems (after total-body irradiation) and demonstrate the clinical effects of infection with an endemic infectious agent in animals with a questionable immune status.Abbreviations: IFA, immunofluorescence assay; SVV, simian varicella virus; TBI, total body irradiation; WaNPRC, Washington National Primate Research Center; VZV, varicella–zoster virus; McHv1, Macacine herpesvuris 1; SRV-2, Simian retrovirus 2 (type D)Simian varicella virus (SVV; Cercopithecine herpesvirus 9) is a naturally occurring herpesvirus of Old World primates responsible for sporadic epizootics in biomedical research facilities.² Signs of infection include fever, vesicular skin lesions, hemorrhagic ulceration throughout the gastrointestinal tract, and multifocal hemorrhagic necrosis of the liver, spleen, lymph nodes, and endocrine organs.^6,7,8 Other names for SVV include Delta herpesvirus, Liverpool vervet virus, patas herpesvirus, and Medical Lake macaque virus.^{16, 20-23} Like many other herpesviruses, SVV establishes persistent lifelong infections, with viral DNA detectable in neural ganglia.¹² Infection with SVV does not necessarily lead to lifelong latency, and periodic reactivation of SVV may occur.³ SVV is genetically and antigenically similar to Human herpesvirus 3,² commonly known as varicela–zoster virus (VZV), the etiologic agent of chickenpox and shingles in humans. SVV in macaques and VZV in man present with similar clinical signs; SVV has been proposed as an animal model of VZV disease in man.²⁴ Rarely, VZV may occur in higher primates (Gorilla).¹⁸ The 2 viruses must be distinguished from one another through molecular techniques.^1,410,11 Both viral infections are usually mild and self-limiting in immunocompetent hosts,^4,8 reactivation and viral shedding may occur during times of stress or immunosupression.^80,21,22A recent review of SVV in Old World Monkeys⁸ focused on SVV as a disease of nonhuman primates. This case report expands on the 2 most recent cases of SVV mentioned in that review.⁸ The animals described were housed in accordance with the regulations of the Animal Welfare Act and the recommendations of the Guide for the Care and Use of Laboratory Animals¹¹ at the Washington National Primate Research Center (WaNPRC) facility in Seattle. The Institutional Animal Care and Use Committee of the University of Washington approved all aspects of the study to which the animals were assigned. The 2 clinical cases described in this report originated at the WaNPR–Seattle facility; contact animals described originated at the WaNPR–Tulane facility. When animals are relocated between the 2 facilities, they are processed through a domestic quarantine consisting of isolation for 30 d, during which time 3 tuberculin skin tests, 2 physical examinations, and 1 complete blood count and serological panel are performed. The WaNPRC–Tulane facility houses a breeding colony founded by animals relocated to Louisiana from the WaNPRC–Medical Lake facility in 1996.     

Frugivory and Seed Dispersal by Four Species of Primates in Madagascar's Eastern Rain Forest1

In the unique faunal assemblage of the Malagasy rain forest, lemurs appear to play particularly important roles as seed-dispersing frugivores. A three-month study of feeding ecology and seed dispersal by four species of lemurs in Madagascar's eastern rain forest found that three species, Eulemur rubriventer, Eulemur fulvus, and Varecia variegata were seed dispersers, and the fourth, Propithecus diadema, was a seed predator. In germination trials, seeds passed by lemurs sprouted significantly faster and in greater numbers than those not passed by lemurs. Analysis of fruit morphologies of 69 local plant taxa producing fleshy fruits during the study period found that these fruits fell into two well-defined color categories that correlated significantly with fruit size. Seventy seven percent of fleshy fruits greater than 10 mm in diameter were colored green, brown, tan, purplish, or black, while all fruits less than 10 mm in diameter were colored red, yellow, orange, pink, blue, or white. Three introduced exotic plant species provided exceptions to this pattern, producing fruits which were larger than 10 mm and pink or orange. Fruits chosen by the primates in this study were usually larger than 10 mm in diameter and were in nearly all cases colored green, brown, tan, purplish, red, or some combination of these colors. Morphological traits shared by fruits of multiple plant taxa in the diets of seed-dispersing lemurs suggest possible coevolved relationships between Malagasy rain forest plants and lemurs.     

Craniodental variation among Macaques (Macaca), nonhuman primates

Background  

In terms of structure and function, the skull is one of the most complicated organs in the body. It is also one of the most important parts in terms of developmental and evolutionary origins. This complexity makes it difficult to obtain evolutionary assessments if, as is usually the case with fossils, only part of the skull is available. For this reason this study involves a set of comparisons whereby the smallest functional units are studied first, and these built up, through a triple-nested hierarchical design, into more complex anatomical regions and eventually into the skull-as-a-whole. This design has been applied to macaques (Macaca) in order to reveal patterns of variation at the different levels. The profiles of such variation have been obtained both within and between species. This has lead to a search for the skull parts that have undergone similar selection pressures during evolution and comparable development patterns in both ontogeny and phylogeny.     

Macaques as Seed Dispersal Agents in Asian Forests: A Review

The role of primates in seed dispersal is well recognized. Macaques (Macaca spp.) are major primate seed dispersers in Asia, and recent studies have revealed their role as seed dispersal agents in this region. Here, we review present knowledge of the traits that define the role of macaques as seed dispersers. The size of seeds in fruit influences whether macaques swallow (0.5–17.1 mm; median: 3.0), spit (1–37 mm; median: 7.6), or drop (8.2–57.7 mm; median: 20.5) them. Dispersal distances via defecation are several hundreds of meters (median: 259 m, range: 0–1300 m), shorter than those achieved by some mammals and birds in tropical and temperate regions. However, macaques disperse seeds by defecation at comparable distances to omnivorous carnivores, and further than passerines. Seed dispersal distance by spitting is much shorter (median: 20 m, range: 0–405 m) than by defecation. Among Asian primates, seed dispersal distances resulting from macaque defecation are shorter than those for gibbons and longer than those for langurs. The effects of seed ingestion on the percentage and speed of germination vary among both plant and macaque species. The degree of frugivory, fruit/seed handling methods, seed dispersal distance, microhabitats of dispersed seeds, and effects of dispersal on seed germination vary seasonally and interannually, and long-term studies of the ecological role of macaques are needed. Researchers have begun to assess the effectiveness of seed dispersal by macaques, secondary dispersal of seeds originally dispersed by macaques, and the effects of provisioning on seed dispersal. Future studies should also test the effects of social factors (such as age and rank), which have received little attention in studies of seed dispersal.     

A Meta-Analysis of Rhesus Macaques (Macaca mulatta), Cynomolgus Macaques (Macaca fascicularis), African green monkeys (Chlorocebus aethiops), and Ferrets (Mustela putorius furo) as Large Animal Models for COVID-19

Animal models are at the forefront of biomedical research for studies of viral transmission, vaccines, and pathogenesis, yet the need for an ideal large animal model for COVID-19 remains. We used a meta-analysis to evaluate published data relevant to this need. Our literature survey contained 22 studies with data relevant to the incidence of common COVID-19 symptoms in rhesus macaques (Macaca mulatta), cynomolgus macaques (Macaca fascicularis), African green monkeys (Chlorocebus aethiops), and ferrets (Mustela putorius furo). Rhesus macaques had leukocytosis on Day 1 after inoculation and pneumonia on Days 7 and 14 after inoculation in frequencies that were similar enough to humans to reject the null hypothesis of a Fisher exact test. However, the differences in overall presentation of disease were too different from that of humans to successfully identify any of these 4 species as an ideal large animal of COVID-19. The greatest limitation to the current study is a lack of standardization in experimentation and reporting. To expand our understanding of the pathology of COVID-19 and evaluate vaccine immunogenicity, we must extend the unprecedented collaboration that has arisen in the study of COVID-19 to include standardization of animal-based research in an effort to find the optimal animal model.

Human research of disease presents a number of ethical dilemmas, prompting scientists to use animal models in their research with the primary goal of enhancing the understanding of a human disease or phenomenon. Animal models have been instrumental to our understanding of pathologies, the assessment of novel vaccines, and the testing of acute therapies. Of the past 222 Nobel prizes awarded in the physiology and medicine categories since 1901, all but 36 have been a direct result of animal-based research.³¹Insects, nematodes, fish, amphibians, and numerous mammals have enabled some of the most important advances in physiology and medicine since their introduction in disease research. Through genetic modification, surgical adaptation, xenografts, chemical induction, and infection models, these animals have been used to model human phenomena.³¹ However, although particular animal species are often chosen based on their ability to meet specific criteria in line with the research question, their size remains an important factor.^26,31Small animals are often preferred in laboratory settings for their ease of use, shorter life cycle, easier handling and care, and short gestation.⁵ Rodents are the most commonly used animal for the study of human diseases for these very reasons, although they frequently fail to fully mimic the clinical signs and significant pathologic hallmarks of human diseases.^11,18 For this reason, some researchers use large animal models. Nonhuman primates (NHPs), in particular, have been extremely useful in reproducing the clinical signs of human diseases due to their close phylogenetic relationship to humans and resulting genetic, behavioral, and biochemical similarities.¹⁴On March 11, 2020, the World Health Organization declared a SARS-CoV-2 pandemic. SARS-CoV-2 is a novel coronavirus causing symptoms similar to, but distinct from, those found in individuals infected with SARS-CoV, the coronavirus that caused the 2003 SARS pandemic. As of September 10, 2021, this coronavirus has infected 219 million individuals with the COVID-19 disease.¹⁰ Although vaccines have been developed and approved in record time, we still need to better understand the pathogenesis of the disease and the long-term implications of infections. To do this, and to increase our understanding of the immunogenicity of current vaccines, finding an animal that replicates the manifestation of COVID-19 in humans is imperative.Much of the research on COVID-19 thus far has been aided by previous SARS research. In both SARS-CoV and SARS-CoV-2 studies, mice^33,45 and hamsters^19,34 were small animal models of choice. Large animals such as ferrets, cats, pigs, chickens, dogs, and nonhuman primates have also been tested for their reproducibility of COVID-19, with varying degrees of success.^27,41,49 While a perfect animal model of this viral infection is unlikely, the need remains to identify at least one large animal species as a frontrunner in reproducibility of the human clinical signs and significant pathologies of SARS-CoV-2 infection.The need for a large animal model to study COVID-19 does not imply a replacement for murine models, but rather an adjunct. The closer phylogenetic relationship of humans to NHPs makes them excellent candidates for the study of this disease. Vaccine trials have already shown that the responses of NHPs are closer to those of humans than are those of mice.²³ This difference may be due to species differences in IgG antibody and T helper type 1 cell responses that influence virus-immune system interactions, which make small animal models problematic for studying SARS-CoV-2 infection and vaccine performance in humans.¹⁵ NHPs have potential high value as a model due to their homology to the human angiotensin‐converting enzyme‐2, which is the SARS-CoV-2 binding site.^23,28 After the outbreak, the World Health Organization (WHO) formed the WHO COVID-19 modelling ad-hoc expert grouping. The working group identified various NHP models, including rhesus macaques, cynomolgus macaques and African green monkeys, in addition to ferrets as being susceptible to SARS Co-V-2 isolates that would result in reproducible infection, with mild to moderate disease.⁵² Therefore, the present article is focused on summarizing the results of multiple studies on rhesus macaque, cynomolgus macaque, African green monkey, and ferret infection with SARS-CoV-2. To highlight the species that best replicate the human clinical and laboratory findings of COVID-19, we synthesized the results of 22 animal studies to provide a comprehensive analysis of what is known about their infections to date.     

Oral Squamous Cell Carcinoma in a Pigtailed Macaque (Macaca nemestrina)

An adult, gravid, female pigtailed macaque (Macaca nemestrina) presented for facial swelling centered on the left mandible that was approximately 5 cm wide. Differential diagnoses included infectious, inflammatory, and neoplastic origins. Definitive antemortem diagnosis was not possible, and the macaque''s condition worsened despite supportive care. Necropsy findings included a mandibular mass that was locally invasive and expansile, encompassing approximately 80% of the left mandibular bone. The mass replaced portions of the soft palate, hard palate, sinuses, ear canal, and the caudal–rostral calvarium and masseter muscle. Histologically, the mass was a neoplasm that was poorly circumscribed, unencapsulated, and infiltrative invading regional bone and soft tissue. The mass consisted of polygonal squamous epithelial cells with intercellular bridging that breached the epithelial basement membrane and formed invasive nests, cords, and trabeculae. The mitotic rate averaged 3 per 400× field of view, with occasional bizarre mitotic figures. Epithelial cells often exhibited dyskeratosis, and the nests often contained compact lamellated keratin (keratin pearls). The neoplasm was positive via immunohistochemistry for pancytokeratin, variably positive for S100, and negative for vimentin, smooth muscle actin, and desmin. The gross, histologic, and immunohistochemical findings were consistent with an aggressive oral squamous cell carcinoma. The neoplasm was negative via PCR for papilloma virus. In general, neoplasia in macaques is rare. Although squamous cell carcinomas are one of the most common oral neoplasia in many species, to our knowledge this case represents the first reported oral squamous cell carcinoma in a pigtailed macaque.Abbreviation: SCC, squamous cell carcinomaSquamous cell carcinomas (SCC) are one of the most commonly reported oral tumors. They are characterized as firm, nodular to irregular, soft-tissue masses that are often ulcerated.⁶ These tumors are frequently highly invasive to local bone and muscle and occasionally metastasize to local and regional lymph nodes.⁶ Histologically, SCC are characterized by keratin pearls, intercellular bridges, and positive cytokeratin staining on immunohistochemistry.^6,18 SCC have been associated with carcinogen exposure (such as bracken fern toxicosis in cattle), actinic radiation, and rarely with papillomatosis.⁸In general, neoplastic diseases are rare in nonhuman primates, and SCC and lymphoma are the 2 most commonly reported oral neoplasms in these species.³ SCC have most commonly been reported in rhesus macaques (Macaca mullata) and baboons (Papio spp.) among nonhuman primate species.⁹ In rhesus macaques, SCC has occurred in the oral cavity,⁹ integument,^9,22 esophagus,⁹ stomach,²¹ lung,^9,13 prepuce–penis,¹⁰ cervix,⁹ uterus,⁹ and eye.⁹ These neoplasms have also been reported to occur in cynomolgus macaques,^14,15,17,19 marmosets, squirrel monkeys, tree shrews, capuchins, tamarins, black spider monkeys, sooty mangabies, a spectacled langur, and an orangutan.⁹ No report describing SCC in a pig-tailed macaque has been published previously. The oral cavity is the most common site of SCC in nonhuman primates, and metastasis occurs in approximately 23% of cases.⁹ The average age at diagnosis of oral SCC in rhesus macaques is 17.6 y.²² In baboons, SCC is the third most common neoplasm, after intestinal adenocarcinoma and lymphosarcoma.⁴ The following case report describes an oral SCC in a pregnant pig-tailed macaque.     

Phylogenetic Relationships of the Macaques (Cercopithecidae: Macaca), Inferred from Mitochondrial DNA Sequences

To study the phylogenetic relationships of the macaques, five gene fragments were sequenced from 40 individuals of eight species: Macaca mulatta, M. cyclopis, M. fascicularis, M. arctoides, M. assamensis, M. thibetana, M. silenus, and M. leonina. In addition, sequences of M. sylvanus were obtained from Genbank. A baboon was used as the outgroup. The phylogenetic trees were constructed using maximum-parsimony and Bayesian methods. Because five gene fragments were from the mitochondrial genome and were inherited as a single entity without recombination, we combined the five genes into a single analysis. The parsimony bootstrap proportions we obtained were higher than those from earlier studies based on the combined mtDNA dataset. Excluding M. arctoides, our results are generally consistent with the classification of Delson (1980). Our phylogenetic analyses agree with earlier studies suggesting that the mitochondrial lineages of M. arctoides share a close evolutionary relationship with the mitochondrial lineages of the fascicularis group of macaques (and M. fascicularis, specifically). M. mulatta (with respect to M. cyclopis), M. assamensis assamensis (with respect to M. thibetana), and M. leonina (with respect to M. silenus) are paraphyletic based on our analysis of mitochondrial genes.     

Group Fission in Moor Macaques (Macaca maurus)

This is the first report of group fission in a wild group of Moor macaques (Macaca maurus) in South Sulawesi, Indonesia. The subject group, which has been observed on the basis of individual identification since 1988, showed no sign of fission in April 1999. In August 1999, the group had split in two, with the same number of mature females in each new group. For the most part, mothers and their offspring joined the same groups. Dominance relations and association patterns established during the previous year among adult females did not strongly affect new group membership. The difference in female reproductive state between the two branch groups was a prominent characteristic. The -male of the original group visited both groups at the first stage of group fission, even though otherwise the compositions of the new groups were stable. After the division, six adult males from outside the original group immigrated exclusively into the group that did not contain the -male of the original group. Severe intergroup encounters occurred between the two groups. We discuss the process of the fission and the resultant pattern in relation to the egalitarian dominance style among females, lack of seasonality in reproduction, and resemblance to one-male type social organization.     

Post-conflict Behaviour in Long-tailed Macaques (Macaca fascicularis)

After being the victim of an agonistic conflict, long-tailed macaques increased the rate of tension-related activities such as scratching, body-shake and selfgrooming. This increase indicates that they experienced physiological changes preparing them to cope with the uncertainty of the post-conflict situation. Indeed, victims of agonistic conflict experienced a higher risk of renewed attacks. However, victims were also involved in social interactions characteristic of post-conflict situations, namely reconciliation and redirection. These two post-conflict social events reduced the rate of scratching, body-shake and selfgrooming. This suggests a faster termination of the stress response. Indeed, the two social events also decreased the likelihood of renewed attacks, one of the causes of the state of uncertainty. Reconciliation is more effective than redirection in this process probably because the restoration of the relationship with the former aggressor allows the victim to resume control of the situation.     

Extraintestinal Campylobacteriosis in Rhesus Macaques (Macaca mulatta)

Two cases of clinical disease associated with extraintestinal Campylobacter infection were recently encountered in rhesus macaques (Macaca mulatta). The first case was that of a 3-y-old, male, rhesus macaque experimentally infected with SIV, who presented with abdominal pain and a midabdominal mass and was euthanized. Pathology findings included an abscess within the median liver lobe, fibrinopurulent peritonitis, and intestinal serositis with isolation of Campylobacter fetus from the blood, liver, and the hepatic abscess. The second case was that of a 1-mo-old, female, rhesus macaque who died with no apparent history of illness. Gross pathology findings included thin body condition and diarrheic staining of the perineum; histologically, acute multifocal hepatitis with intralesional bacteria was noted. Campylobacter coli was isolated from the liver and colon. Extraintestinal Campylobacter infection is uncommon in humans, usually occurring in immunocompromised subjects and most commonly manifesting as bacteremia. Extraintestinal Campylobacter infections in animals are rare but have been associated with bacteremia and cholecystitis. The macaques presented here were either immunocompromised due to SIV infection (case 1) or more vulnerable due to young age (case 2). These factors likely contributed to the extraintestinal spread of Campylobacter.Campylobacter spp. are curved or spiral, gram-negative, microaerobic, typically motile bacteria with a single flagellum at one or both ends of the cell.²⁵ Campylobacter is one of the most common bacterial causes of gastroenteritis in humans worldwide.³ The Centers for Disease Control and Prevention estimate it to affect more than 1.3 million people in the United States each year.¹¹ Campylobacter spp. colonize the intestinal tract of primates, other mammals, birds, reptiles, and shellfish, but infection is not always associated with clinical signs of disease.^2,23 Contaminated or undercooked poultry represents the largest potential source of human infection.²² Campylobacteriosis is a zoonosis, and other significant sources of human infection include livestock, wildlife, pets, and contaminated water.²² The species most commonly isolated from humans and nonhuman primates are C. jejuni and C. coli; other species like C. fetus are less commonly found.^2,4,9,23 Extraintestinal campylobacteriosis in humans usually occurs in immunocompromised or elderly persons with underlying medical problems and most commonly manifests as bacteremia.²³ There have been a few reports of extraintestinal Campylobacter infections in animals, including bacteremia and cholecystitis in 2 dogs.^17,30     

Maternal Anxiety in Rhesus Macaques (Macaca mulatta)

Visual monitoring and scratching were used as behavioral indicators of maternal and social anxiety in small captive groups of rhesus macaques. Young infants were especially at risk from other group members during the first weeks of locomotion away from their mothers. Mothers received aggression from other individuals irrespective of their infants' presence or absence. The rate at which mothers scratched themselves increased significantly when their infants moved away from them and when the infants approached or were approached by individuals who frequently harassed them. The rate of maternal scratching and the rate of glancing at the infant and at other individuals when the infant was away decreased as infants grew older and became less vulnerable to harassment. In contrast, the rate of maternal scratching and visual monitoring of other individuals when the infant was in contact remained stable across the first 12 wk of lactation. The rate of maternal scratching increased when the mother-infant pair was in spatial proximity to the adult male or higher ranking adult females. Although visual monitoring and scratching showed a similar sensitivity to social variables, it is speculated that they might reflect different components of anxiety, namely, anticipation of danger and uncertainty due to motivational conflict. The results of this investigation indicate that a macaque mother's emotional reactivity to a perceived danger for herself and her infant can be measured quite accurately using the rates of visual monitoring and scratching and that the latter represent reliable tools to investigate the emotional correlates of maternal behavior in nonhuman primates.     

Snake Species Discrimination by Wild Bonnet Macaques (Macaca radiata)

Wild bonnet macaques (Macaca radiata) were studied in southern India to assess their ability to discriminate non‐venomous, venomous and predatory snakes. Realistic snake models were presented to eight troops of bonnet macaques at feeding stations and their behavior was video‐recorded 3 min before and 3 min after snake exposure. Snakes presented were: (1) venomous Indian cobra (Naja naja) displaying an open hood with ‘eyespots’; (2) venomous common Indian krait (Bungarus caeruleus); (3) non‐venomous green keelback (Macropisthodan plumbicolor); (4) non‐venomous rat snake (Ptyas mucosus); and (5) Indian python (Python molurus) which preys on macaques. Latencies to detect and react to the snakes were evaluated to determine initial responsiveness. Longer‐term assessment was measured as the percentage of time individuals looked at the snakes and monitored the activity of nearby individuals before and after snake detection. All snake models engendered caution and maintenance of a safe distance. Alarm calling occurred only during python presentations. The cobra engendered a startle response or running in the largest percentage of individuals after its detection, whereas the rat snake and python elicited bipedal standing or ambulating to monitor the snakes. We also examined the influence of age on snake recognition. Juveniles and subadults looked at the cobra, krait, and python for a larger percentage of time than adults did; albeit, adults looked at the python substantially longer than at the other snakes. Age differences in behavior suggest that, with the exception of the python, repeated experience with snakes in the wild moderates excitability, consistent with the likely threat of envenomation.