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4 Infant male Alouatta pigra resting on a hammock (photo by Rosalia Pastor-Nieto) 

4 Infant male Alouatta pigra resting on a hammock (photo by Rosalia Pastor-Nieto) 

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Among platyrrhines, howler monkeys are commonly traded illegally as pets in Central and South America, resulting in the high mortality of specimens. Many of these animals end up in long-term captive situations in zoos and rehabilita-tion centers, where adaptation may be diffi cult. Careful husbandry planning, taking into account the animals' behavi...

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... religiosa, Ficus thonningii, Hibiscus, Morus alba, Tecomaria capensis, and Tipuana tipu. Some of these plant species have been successfully fed to primates in North American zoo collections. A more extensive list of nontoxic browse fed to primates in zoos is also provided by Tresz ( 2003 ) ( Table 12.1 , Fig. 12.3 ). In general terms, the total daily amount of food is divided into two or more portions. This is to keep the animals busy by prolonging feeding times and simulating wild conditions. Although each portion may be balanced to meet the nutritional needs of all animals in a group, high-ranking individuals tend to achieve preferential access to high quality foods (Wolfensohn and Honess 2005 ). Hierarchy sometimes deters subordinates from climbing to feeding platforms (pers obs); therefore, it is crucial to verify that low-ranking individuals are also provided with a balanced portion of the diet. Mixed exhibits with two or more species of howler monkeys are not recommended. Size differences, such as those seen between Alouatta pigra and A. palliata may result in intimidation of the smaller A. palliata, forcing them to climb to less optimal feeding stations (pers obs). Captivity provides a very static environment compared to wild habitats, often resulting in reduction in animal attention, propensity to seek, problem solving, and reduced interests in novel items. Environmental poverty , defi ned as “inappropriate social and physical environments in relation to the basic needs of primates” (Hosey et al. 2009 ), may trigger a series of nonadaptive responses, such as increased aggressiveness, abnormal behaviors (such as coprophagy, lethargy, auto-mutilation), stereotypic behaviors, inappropriate sexual behaviors (inappropriate mounts, hyper- sexuality or abnormal postures), inadequate immune response, disease, parasitism, and poor reproductive performance (Meyer-Holtzapfel 1968 ; Harlow and Suomi 1971 ; Mason 1991 ; Sapolsky 1993 ; Boere 2001 ; Hosey et al. 2009 ; Behie et al. 2010 ). Insuffi cient space and isolation are the most important characteristics of an impoverished environment (Hosey et al. 2009 ). Conversely, environmental enrichment consists of a series of measures to modify these impoverished environments, with the goal of improving the physical and social potential of the animals, and therefore improving their quality of life by meeting their ethological needs (Hosey et al. 2009 ). Basic aspects of behavioral enrichment include minimal clinical interventions, minimizing and/or eradicating animal suffering, providing proper nutrition, adequate enclosure design and dimensions, promoting proper social conditions, and shaping novel and interesting environments by creating occupational therapies. Some examples of occupational therapies are food seeking on substrate, foraging plant species within the enclosure, nest-boxes, perches and refuges, promoting three-dimensional locomotion with ropes, tree trunks and/or branches, elevated feeding trays, and group housing (Novak and Suomi 1988 ; Woolverton et al. 1989 ; Boere 2001 ). Moreover, enclosure design is not only linked to psychological well being but also to health. Considering that howler monkeys are tropical primates, housing has to take into account ambient temperature (optimal room temperature should be between 20 and 26 ° C), or an additional heat source should be provided. Another relevant, yet commonly overlooked, enclosure design is the position and location of feeding trays. Howler monkeys are arboreal primates adapted to feed and move on trees, and for this reason it is highly likely that they lack natural immunity to many terrestrial pathogens. Placing feeding trays on elevated platforms can aid in preventing further stress and disease. Enclosures for captive howlers should be designed to meet the needs of arboreal primates. Most zoos that hold howler monkeys include perches, nests, hammocks, and natural foraging vegetation within their facilities. Howler monkeys should be able to move in an elevated, three- dimensional environment (Hosey et al. 2009 ) (Fig. 12.4 ). In captivity, there is a tendency towards inactivity and a lack of use of the prehensile tail. Promoting natural feeding behaviors through enrichment activities, by varying the presentation of the diet encourages activity and use of the tail. Finally, enclosures should be designed with external and indoor sections and a heat source when low temperatures are expected to occur. Aberrant behaviors are sometimes observed, like in Alouatta clamitans as described by Dada ( 2009 ). Among the most common pathologic behaviors are circle locomotion, head and body swinging, back hitting with tail, tongue fl icking to observers, self-mutilation, fl exing and stretching limbs, sexually directed behaviors, and aberrant eating. In this study, singled housed animals showed higher rates of stereotypic behaviors, among which locomotion in circles was observed in highest frequencies, especially before feeding hours, suggesting increased anxiety levels before feeding. Dividing the diet into a number of smaller portions and hiding them in different parts of the enclosure are good strategies to reduce levels of anxiety. Social interactions with familiar conspecifi cs are essential for howler monkeys in captivity (Farmer et al. 2011 ). Other social events such as separation from the mother, a sibling or nursery peer, a cage partner, or a roommate are detrimental for howlers and may result in chronic stress and illness (pers obs). Another factor, possibly associated with captivity stress in some primate species is the visitor effect (Hosey et al. 2009 ), but its responses have not been yet evaluated in howler monkeys in captivity. Conditions associated with overcrowding, lack of behavioral enrichment, and improper enclosure design may lead to otherwise avoidable animal injuries. In many cases, an increase in aggression is observed in overcrowded conditions, when a male sex-biased group is housed together, and when animals are maintained in improper facilities. The most common injuries include lacerations of ears, face, and fi ngers as a consequence of fi ghting. It is worthwhile mentioning that good knowledge of the behavioral characteristics of howler monkeys is essential to prevent injuries caused by fi ghts, aggression, and infanticide (Crockett and Janson 2000 ). Captive howler managers should consider specifi c behavioral traits, such as signs of psychological well being. Factors such as group structure, hierarchy, and age are important factors to take into account to prevent aggressive behavior (Hosey et al. 2009 ). General physical examination in howler monkeys includes dental examination, weighing, blood and stool samples, and rectal swabs for bacteriological cultures. It is also important to evaluate systolic arterial pressure and cardiac frequency, and to check for their coordination (Chagas et al. 2010 ). The pulse can be monitored at the lateral metatarsal area or at the femoral-inguinal region. The recorded clinical parameters are heart rate at 151–194 (bounce/min.), respiratory frequency of 19–25 breaths/min, systolic blood pressure at 154–163 mmHg, and rectal temperature ranging between 37.5 and 39 ° C. Oral and dental examinations are essential to discover oral lesions and dentition problems. The fur and skin of newly acquired howler monkeys should be checked for external parasites, miasis and bacterial infections, especially if suspected to be wild caught. Abdominal palpation is important for checking liver and kidney size, as well as the consistency of intestines and bladder palpation. Flexion and extension of the limbs to check for range of motion and articular fl exibility can be crucial in cases of contracture and arthritis due to captive conditions. Venipuncture for blood samples is in the femoral vein, located in the femoral triangle. The use of a vacutainer is usually recommended to avoid excessive handling of primate blood. Reference hematological values for Alouatta are reported elsewhere (Canales et al. this volume). To perform a thorough medical examination, improved immobilization techniques have made the restraint of monkeys much safer. Before manually restraining a howler monkey, there are several factors to consider, such as the animals’ physical and health condition, temperament, duration of restraint, and the handler’s experience (Ølberg 2007 ). Other important factors involved in successful animal handling are enclosure design and careful planning. It is very important that captive howler monkeys are housed under conditions that allow for safe handling without anesthesia. This may be accomplished by a combination of properly designed facilities and management practices allowing selective movement of animals (Bush 1996 ). The common capture and restraint techniques for howler monkeys are netting and holding the arms and neck while wearing leather gloves. If chemical restraint is used, ketamine hydrochloride is generally a safe drug that has been widely used with excellent results ...

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... In captivity, these primates are often restricted to the floor of the enclosure, which increases the chances of contact with specific agents responsible for the development of infectious diseases. 5,9 Indeed, bacterial diseases were the second major cause of death in primates in this investigation, and bacterial pneumonia was the main condition diagnosed. ...
Article
Background Anthropogenic disturbances are the main threats to nonhuman primates conservation, and infectious diseases may also play a key role in primate population decline. This study aimed to determine the main causes of death in neotropical primates. Methods A retrospective study of post-mortem examinations was conducted on 146 neotropical primates between January 2000 and December 2018. Results Conclusive diagnoses were obtained in 68.5% of the cases, of which 59 corresponded to non-infectious causes and 41 to infectious diseases. Trauma was the main cause of death (54/100), with anthropogenic stressors caused by blunt force trauma injuries (collision with vehicles) and puncture wound injuries associated with interspecific aggression (dog predation) were the most common factors. Other causes of death included bacterial diseases (27%), followed by parasitic diseases (12%), neoplasms (2%), and viral diseases (2%). Conclusions Free-ranging primates were mostly affected by non-infectious causes, while captive primates were by infectious conditions.
... El estudio de los primates en México tiene una tradición que data de la década de 1970, por lo que las tres especies han sido estudiadas ampliamente en diferentes aspectos (Estrada, 1984); siendo los monos araña los más explorados a nivel cognitivo, ya que los monos aulladores presentan diferentes problemas para ser mantenidos por largos periodos en cautiverio (Pastor-Nieto, 2015), además de presentar tasas bajas de actividad a lo largo del día (Cristóbal-Azkarate, & Arroyo- Rodríguez, 2007). ...
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La memoria es un proceso donde los animales pueden mantener información del pasado para usarla en el futuro. En los estudios de esta habilidad, los primates han sido ampliamente usados, sin embargo, muchas especies no han sido estudiadas, lo que abre la posibilidad de extender nuestra compresión de la memoria a otras especies. El presente trabajo tuvo como objetivo probar los efectos del tiempo y la cantidad de información en la memoria de monos araña (Ateles geoffroyi vellerosus). La primera serie de tres experimentos evaluó el efecto de la memoria sobre las decisiones de forrajeo, observándose que los monos araña recuerdan donde se alimentaron y cuanto alimento consumieron allí, incluso por 24 h. Los siguientes dos experimentos probaron la curva de olvido y los resultados indicaron que, a mayor demora y a mayor número de posiciones espaciales donde se puede esconder una recompensa, mayores fueron los errores y estos se dispersaban cada vez más lejos. Finalmente, el ultimo experimento evaluó la memoria de reconocimiento visual y determinó que los monos araña son capaces de reconocer una imagen que vieron en el pasado, pero este reconocimiento dependió de la cantidad de imágenes, el orden en que se presentaron y la demora que debían esperar para reconocer una imagen. Todos estos resultados indicaron que los monos araña son una especie que se puede emplear para investigar características psicológicas y al igual que otras especies la demora y la cantidad de información afecta el recuerdo de información.
... Although A. pigra may harbor different GI parasites, such as trematodes that inhabit the bile ducts (Kowalzik et al., 2010;Pastor-Nieto, 2015), it is also frequently infected by GI nematodes of the genus Trypanoxyuris (Nematoda: Oxyuridae), which are found in the large intestine (Hugot et al., 1996;Solórzano-García & Pérez-Ponce de León, 2017;Solórzano-García et al., 2016). This feature makes Trypanoxyuris a suitable model to explore associations between parasite infection and gut bacterial community composition. ...
Article
Gut bacteria may coexist with other groups of organisms, such as nematode parasites, that inhabit the gastrointestinal tract of primates; however, the possible effects of endoparasites on bacterial communities are frequently overlooked. Here we explored whether infection with Trypanoxyuris, an oxyurid gastrointestinal parasite, is associated with changes in the gut bacterial community of wild black howler monkeys (Alouatta pigra), by comparing gut bacterial communities of consistently infected individuals and individuals that never tested positive for Trypanoxyuris throughout different months across the year. We additionally controlled for other sources of variation reported to influence the primate microbiome including individual identity, social group, and seasonality. Trypanoxyuris infection was not related to differences in gut bacterial alpha diversity, but was weakly associated with differences in gut bacterial community structure. In contrast, among the covariates considered, both individual identity and social group were more strongly associated with variation in the howler gut bacterial community. Our results suggest that gastrointestinal parasites may be associated, to some extent, with shifts in the gut bacterial communities hosted by free-ranging primates, although a causal link still needs to be established. Further studies of wild primate hosts infected with parasite species with different pathogenicity are needed to better elucidate health-related consequences from the parasite-microbiome interplay. Research highlights • 1. Pinworm (Trypanoxyuris) infection was associated with slight shifts in the gut bacterial community of black howler monkeys. • 2. The individual ID and social group played a stronger role shaping bacterial communities in this Alouatta pigra population. • 3. Bacterial taxa associated with colonic inflammation were increased in parasite-infected individuals.
... Monkeys were also most reported with the same condition (Table 2). It has been mentioned that some captive monkeys are provided with diets low either in calcium or vitamin D3 which results in MBD (19). On the other hand, hedgehogs were most reported with urinary problems in our study, which is known as one of the five most common health conditions in this creature (20). ...
Article
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In recent decades, exotic pets are increasingly invited to homes with a wide range of variation in species and requirements that are more specialized. During a one-year period, 2408 exotic animals admitted to the Small Animal Veterinary Hospital, University of Tehran were assessed. Rabbits, hamsters, squirrels, turtles/tortoises, guinea pigs, lizards, hedgehogs, reindeer, monkeys, and snakes were referred, respectively. Owner referral cause and their gender in addition to the disease diagnosis were analyzed. While no statistical significance (P>0.05) was observed in the total number of men and women presenting these animals, gender-based preferences were spotted for owning specific types of animal species in this study (P<0.05). Furthermore, analysis showed that snakes and rabbits were more commonly (P<0.05) presented for checkup; while chelonians, lizards, hedgehogs, and monkeys were more presented with health problems (P<0.05). Other animals’ results did not show statistically significant difference for admission reasons (P>0.05). The health record assessment included 1587 animals with complete health files. The most common diseases diagnosed in most of these animals were metabolic bone disease/musculoskeletal problems and dental problems. In addition, eye problems in chelonians and urinary problems in hedgehogs were the most common diagnosis of those species. In conclusion, since the most common health problems of most participating animals were associated with mismanagement and inappropriate diet, it is highly recommended that owners be thoroughly educated by veterinarians to reduce the possibility of such conditions in exotic captive animals
... According to the International Union for the Conservation of Nature and Natural Resources (IUCN) assessment, proboscis monkey belongs to endangered species [5]. The decrease of the primate population is mainly caused by deforestation and illegal trading [3,6]. Deforestation also allows the hunter to provide primates illegal trading [6]. ...
... The decrease of the primate population is mainly caused by deforestation and illegal trading [3,6]. Deforestation also allows the hunter to provide primates illegal trading [6]. The decrease of population is also expected as the main cause of the change of distribution pattern of the primate population in a certain area [7]. ...
... However, for marmosets, even though coprophagy has been described in animals on a protein-deficient diet [60], other observations do not suggest that coprophagy is a typical part of their behavioural repertoire [72]. For howler monkeys, coprophagy was not mentioned in four digesta passage studies [49,[73][74][75], was specifically mentioned as "not observed" in the passage study of Espinosa-Gómez, Gómez-Rosales [24], but is mentioned as a possible abnormal behaviour in captive animals [76]. While all this does not represent conclusive evidence that howler monkeys do not practice some kind of cecotrophy, it makes cecotrophy as a regular strategy in this species unlikely. ...
Article
The digestive tract of animals, and the patterns how passage markers are excreted from them, have been fruitfully compared to chemical reactor models from engineering science. An important characteristic of idealized reactor models is the smoothness of the curves plotting marker concentrations in outflow (i.e., faeces) over time, which is the result of the assumed complete mixing of the marker with the reactor contents. Published excretion patterns from passage experiments in non-primate mammals appear to indicate a high degree of digesta mixing. In order to assess whether marker excretion graphs from primates differ from ideal outflow graphs, we performed passage experiments in eight individuals of three foregut-fermenting species (Pygathrix nemaeus, Trachypithecus auratus and Semnopithecus vetulus), and added them to available marker excretion curves from the literature. In the resulting collection, 23 out of a total of 25 patterns in foregut fermenters (21 individuals of 10 species from 7 studies), and 13 out of 15 in hindgut fermenters (9 individuals of 2 species from 2 studies), showed an irregular, ‘spiky’ pattern. We consider this proportion to be too high to be explained by experimental errors, and suggest that this may indicate a taxon-wide characteristic of particularly incomplete digesta mixing, acknowledging that further data from less related primate species are required for corroboration. Our hypothesis is in accordance with previous findings of a comparatively low degree of ‘digesta washing’ (differential retention of particulate and fluid digesta) in primates. Together with literature findings that suggest a low chewing efficiency in primates compared to other mammals, these observations indicate that in contrast to other herbivores, the success of the primate order is not derived from particularly elaborate adaptations of their ingestive and digestive physiology.
... Pavelka, Kutz, & Behie, 2010), but it remains unclear whether these parasites have detrimental effects on howler health (Pastor-Nieto, 2015). Our study suggests that the endocrine changes experienced by female howlers during an energetically demanding reproductive phase (i.e., early lactation) are an additional factor that increases susceptibil- ity to C. biliophilus infections. ...
Article
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Parasitic infections in wildlife are shaped by host-related traits including individual reproductive condition. It has been argued that female primates are more susceptible to infectious diseases during pregnancy due to short-term changes in immune function that result in reduced ability to combat infections. Likewise, lactation, which is the most energetically expensive state, may affect immunity and infection risk due to tradeoffs between milk production and maintenance of immune function. Here, we examine the degree to which parasite prevalence and parasite richness are affected by female reproductive condition and stress levels in wild female black howler monkeys (Alouatta pigra). Over the course of one year, we collected fresh fecal samples from 15 adult females belonging to seven black howler groups living in Escárcega, Mexico. Fecal samples were used for parasitological analysis and for measuring fecal glucocorticoid metabolites (i.e., stress biomarker). We found that the prevalence of intestinal parasites and parasite richness did not differ among non-pregnant, pregnant, and lactating females. Fecal glucocorticoid metabolite levels increased significantly during pregnancy and during the first month of lactation, and positively predicted the probability of Controrchis biliophilus infection. Parasite prevalence and richness decreased during the months of increased rainfall. We conclude that reproductive physiology has limited consequences on intestinal parasitic infection risk in female black howler monkeys and that seasonal environmental fluctuations have greater effects. K E Y W O R D S gastrointestinal parasites, glucocorticoids, immune system, Mexico, pregnancy
... Howlers require a wide dietary variety of fruits and leaves for survival and a delicate microbiomic balance for proper food digestion (Milton 1980); improper diet can lead to gastric dilation, a common cause of death in captive mantled howlers (Varela et al. 2005). In addition, veterinary options are limited; for example, great care must be used when providing antibiotic therapy to howlers, as a reduction in normal gut microflora can lead to the proliferation of harmful bacteria and ultimately cause death (Pastor-Nieto 2015). Indeed, the International Species Information Service (ISIS) indicates that there are no mantled howlers kept in captivity in any of the 911 zoos and aquaria across 85 countries present in their database (ISIS 2015). ...
Article
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Wildlife rehabilitation presents many challenges, especially when anthropogenic threats yield large numbers of naive juvenile animals. In particular, many primates obtain survival skills such as the identification of palatable foods, avoidance of unsafe substrates, and antipredatory behaviors from conspecifics, and require prerelease training by humans in the absence of opportunities for social learning. Nonetheless, few primate rehabilitation programs quantitatively evaluate the success of prerelease training programs, making the establishment of best practices for many species difficult. Here, we quantitatively assess whether three juvenile mantled howlers (Alouatta palliata) gained independence from humans and increased their frequencies of naturalistic behaviors while participating in a rehabilitation program in Panama that consisted of daily “bush outings” with an operant conditioning component. We evaluated the role of rehabilitating animals in groups in particular, by determining whether the three rehabilitants were more likely to exhibit naturalistic behaviors when in closer proximity to conspecifics. Across the 54-day study period, all three rehabilitants improved significantly in at least two out of the three tested metrics (approaching humans less frequently, traveling higher into the canopy, and spending more time foraging for forest foods). Individuals were more likely to venture into trees and less likely to approach humans when in close proximity to conspecifics, suggesting that group rehabilitation positively impacts the acquisition of naturalistic behaviors by this species. Our results support previous notions of prerelease training as a crucial rehabilitation tool, and highlight the importance of group rehabilitation in programs targeting social animals, even when naturalistic group compositions cannot be approximated.
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The healthy function of the gastrointestinal system is influenced by changes in the microbiota and the adaptability of the host to different habitat conditions and food availability. We isolated and identified 64 bacterial morphospecies from rectal swabs from five captive black howler monkeys (CM) and 15 wild individuals (WM) from groups living in fragments with different compositions and vegetation structures (height, density, canopy width) in flooded and non-flooded areas. Low microbial diversity in CM and WM from the flooded area was observed while in WM from the non-flooded area, there was a higher microbial diversity and evenness. Free-ranging monkeys from different areas showed a significant difference in the replacement of morphospecies of gut microbiota (p = 0.0006); however, the bacterial communities are not differentiated as particular entities. The intestinal microbial community can be an indicator of howler monkeys’ health and habitat quality. The change in the composition of the plant community into small landscape scales, as well as fragmentation and natural heterogeneity of the landscape, can affect the intestinal microbial community of howler monkeys.