Monkeying around with venom: an increased resistance to α-neurotoxins supports an evolutionary arms race between Afro-Asian primates and sympatric cobras.

BACKGROUND: Snakes and primates have a multi-layered coevolutionary history as predators, prey, and competitors with each other. Previous work has explored the Snake Detection Theory (SDT), which focuses on the role of snakes as predators of primates and argues that snakes have exerted a selection pressure for the origin of primates' visual systems, a trait that sets primates apart from other mammals. However, primates also attack and kill snakes and so snakes must simultaneously avoid primates. This factor has been recently highlighted in regard to the movement of hominins into new geographic ranges potentially exerting a selection pressure leading to the evolution of spitting in cobras on three independent occasions. RESULTS: Here, we provide further evidence of coevolution between primates and snakes, whereby through frequent encounters and reciprocal antagonism with large, diurnally active neurotoxic elapid snakes, Afro-Asian primates have evolved an increased resistance to α-neurotoxins, which are toxins that target the nicotinic acetylcholine receptors. In contrast, such resistance is not found in Lemuriformes in Madagascar, where venomous snakes are absent, or in Platyrrhini in the Americas, where encounters with neurotoxic elapids are unlikely since they are relatively small, fossorial, and nocturnal. Within the Afro-Asian primates, the increased resistance toward the neurotoxins was significantly amplified in the last common ancestor of chimpanzees, gorillas, and humans (clade Homininae). Comparative testing of venoms from Afro-Asian and American elapid snakes revealed an increase in α-neurotoxin resistance across Afro-Asian primates, which was likely selected against cobra venoms. Through structure-activity studies using native and mutant mimotopes of the α-1 nAChR receptor orthosteric site (loop C), we identified the specific amino acids responsible for conferring this increased level of resistance in hominine primates to the α-neurotoxins in cobra venom. CONCLUSION: We have discovered a pattern of primate susceptibility toward α-neurotoxins that supports the theory of a reciprocal coevolutionary arms-race between venomous snakes and primates.

Cognitive maps in the wild: revealing the use of metric information in black howler monkey route navigation.

When navigating, wild animals rely on internal representations of the external world - called 'cognitive maps' - to take movement decisions. Generally, flexible navigation is hypothesized to be supported by sophisticated spatial skills (i.e. Euclidean cognitive maps); however, constrained movements along habitual routes are the most commonly reported navigation strategy. Even though incorporating metric information (i.e. distances and angles between locations) in route-based cognitive maps would likely enhance an animal's navigation efficiency, there has been no evidence of this strategy reported for non-human animals to date. Here, we examined the properties of the cognitive map used by a wild population of primates by testing a series of cognitive hypotheses against spatially explicit movement simulations. We collected 3104 h of ranging and behavioural data on five groups of black howler monkeys (Alouatta pigra) at Palenque National Park, Mexico, from September 2016 through August 2017. We simulated correlated random walks mimicking the ranging behaviour of the study subjects and tested for differences between observed and simulated movement patterns. Our results indicated that black howler monkeys engaged in constrained movement patterns characterized by a high path recursion tendency, which limited their capacity to travel in straight lines and approach feeding trees from multiple directions. In addition, we found that the structure of observed route networks was more complex and efficient than simulated route networks, suggesting that black howler monkeys incorporate metric information into their cognitive map. Our findings not only expand the use of metric information during route navigation to non-human animals, but also highlight the importance of considering efficient route-based navigation as a cognitively demanding mechanism.

Illegal trade in wild cats and its link to Chinese-led development in Central and South America.

Seizures of hundreds of jaguar heads and canines in Central and South America from 2014 to 2018 resulted in worldwide media coverage suggesting that wildlife traffickers are trading jaguar body parts as substitutes for tiger parts to satisfy the demand for traditional Asian medicine. We compiled a data set of >1000 seized wild cats (jaguar [Panthera onca], puma [Puma concolor], and ocelot [Leopardus pardalis]) from 19 Central and South American countries and China. We ran generalized additive mixed models to detect trends in wild-cat seizures from 2012 to 2018 and assess the effects of socioeconomic factors of source countries and between those countries and China on the number of wild cats seized. Jaguar seizures increased over time, and most of the seized jaguar pieces were canines (1991 of 2117). Around 34% (32 of 93) of the jaguar-part seizure reports were linked with China, and these seizures contained 14-fold more individuals than those intended for domestic markets. Source countries with relatively high levels of corruption and Chinese private investment and low income per capita had 10-50 times more jaguar seizures than the remaining sampled countries. The number of Chinese residents in Central and South America was not significantly related to the number of jaguars seized. No socioeconomic factors influenced the seizures of puma and ocelots. Legal market chains may provide structure for the illegal chain; thus, the influx of illegal jaguar products is potentially a side effect of the economic partnership between Central and South American countries and China. Poverty and high levels of corruption in the source countries may motivate local people to engage in illegal activities and contribute to the growth of this trade. Supply-side interventions to curb this threat to Neotropical wild cats may include improved training for officials and promotion of governance and the value of protecting these animals to local people.

Mercado Ilegal de Felinos Silvestres y su Conexión al Desarrollo Encabezado por China en América Central y América del Sur Resumen La incautación de cientos de cabezas y colmillos de jaguar en América Central y América del Sur entre 2014 y 2018 resultó en una cobertura mediática mundial que sugirió que los traficantes de fauna están comerciando con partes de jaguar como sustituto de las partes de tigre para satisfacer la demanda de la medicina tradicional asiática. Recopilamos un conjunto de datos de más de mil felinos silvestres incautados (jaguar [Panthera onca], puma [Puma concolor], ocelote [Leopardus pardalis]) en 19 países de América Central y América del Sur y en China. Corrimos modelos aditivos mixtos generalizados para detectar las tendencias en las incautaciones de felinos silvestres entre 2012 y 2018 y para evaluar los efectos de los factores socioeconómicos de los países de origen y entre esos países y China sobre el número de felinos silvestres incautados. La incautación de artículos de jaguar incrementó con el tiempo y la mayoría de ellos fueron colmillos (1991 de 2117). Alrededor del 34% (32 de 93) de los reportes de incautación estuvieron vinculados a China y estas incautaciones tenían 14 veces más individuos que las incautaciones de artículos dirigidos al mercado doméstico. Los países de origen con niveles relativamente altos de corrupción y con inversión privada proveniente de China y con un bajo ingreso per cápita tuvieron de 10 a 50 veces más incautaciones de artículos de jaguar que los demás países muestreados. El número de residentes chinos en América Central y en América del Sur no tuvo una relación significativa con el número de jaguares incautados. Ningún factor socioeconómico influyó sobre las incautaciones de pumas y ocelotes. Las cadenas de mercado legales pueden proporcionar una estructura para la cadena ilegal; por lo tanto, la afluencia de productos ilegales de jaguar es potencialmente un efecto colateral de la colaboración económica entre China y los países de América Central y América del Sur. La pobreza y los altos niveles de corrupción en los países de origen pueden motivar a los habitantes locales a participar en actividades ilegales y a contribuir al crecimiento de este mercado. Las intervenciones del lado del suministro para disminuir esta amenaza para los felinos silvestres neotropicales pueden incluir mejoras al entrenamiento para los oficiales y el fomento entre los locatarios de la gestión y el valor de proteger a estos animales.

A giant among dwarfs: a new species of galago (Primates: Galagidae) from Angola.

OBJECTIVES: Based on vocalization recordings of an unknown galago species, our main objectives were to compare morphology and call structure with known closely-related taxa and describe a new species of galago. MATERIALS AND METHODS: We conducted field surveys in three forest habitats along the escarpment region in western Angola (Kumbira Forest, Bimbe Area, and Northern Scarp Forest), and examined galago specimens from museums worldwide. We digitized and analyzed calls using Avisoft SASLab Pro software. We also compared museum specimens from Angola with other Galago and Galagoides specimens, and conducted comparative analyses (ANOVA and between group principle component analysis) based on a set of twelve linear measurements of skulls and teeth. RESULTS: We describe the new species to which we give the name Angolan dwarf galago, Galagoides kumbirensis sp. nov. The new species has a loud and characteristic crescendo call, used by other Galagoides spp. (sensu stricto) in West Africa to attract companions and repel rivals. However, this call shows species-typical differences from its closest relatives. Galagoides kumbirensis sp. nov. is also distinguished by differences in the skull morphology, pelage color and facial markings, as well as a larger body size, similar to that of Galago moholi, which is not known to be sympatric. CONCLUSION: This discovery points to the importance of Angolan forests as refuges for endemic biodiversity. These forests are under severe threat from overexploitation, and there is an urgent need to establish conservation measures and designate protected areas.

The largest relative testis size among primates and aseasonal reproduction in a nocturnal lemur, Mirza zaza.

OBJECTIVES: Testis size is an indirect indicator of a species' mating system, along with sexual size and canine dimorphism, existence and usage of mating and advertisement calls as well as the spatial distribution of males and females ready to mate in solitary species. Upon its recent discovery, the northern giant mouse lemur Mirza zaza was suggested to have a polygynandrous mating system and to exhibit seasonal breeding. We tested these predictions in a field study in Sahamalaza National Park, NW Madagascar. MATERIALS AND METHODS: We caught 12 M. zaza, before and during the suggested mating period and obtained standard field morphometric measurements, including testes size. RESULTS: We show that M. zaza has the highest relative testis volume among primates, indicating strong sperm competition and polygynandrous mating. In addition, based on inferred age of captured animals, observed mating behavior, a female caught in met-estrus and data from captivity, we suggest M. zaza to be one of the few lemurs that breed aseasonally. DISCUSSION: Future field work on this endangered species is required to illuminate the causes and consequences of intense promiscuity and aseasonal breeding despite strong habitat seasonality, which distinguish M. zaza from most other nocturnal lemurs.

Proteins from shrews' venom glands play a role in gland functioning and venom production.

Venom production has evolved independently many times in the animal kingdom, although it is rare among mammals. Venomous shrews produce venom in their submandibular salivary glands and use it for food acquisition. Only a few toxins have been identified in shrew venoms thus far, and their modes of action require investigation. The biological and molecular processes relating to venom production and gland functioning also remain unknown. To address this gap, we investigated protein content in extracts from venom glands of two shrew species, Neomys fodiens and Sorex araneus, and interpreted their biological functions. Applying a proteomic approach coupled with Gene Ontology enrichment analysis, we identified 313 and 187 putative proteins in venom glands of N. fodiens and S. araneus, respectively. A search of the UniProt database revealed that most of the proteins found in both shrew species were involved in metabolic processes and stress response, while GO enrichment analysis revealed more stress-related proteins in the glands of S. araneus. Molecules that regulate molecule synthesis, cell cycles, and cell divisions are necessary to enable venom regeneration and ensure its effectiveness in predation and food hoarding. The presence of proteins involved in stress response may be the result of shrews' high metabolic rate and the costs of venom replenishment. Some proteins are likely to promote toxin spreading during envenomation and, due to their proteolytic action, reinforce venom toxicity. Finally, finding numerous proteins involved in immune response suggests a potential role of shrew venom gland secretions in protection against pathogens. These findings open up new perspectives for studying biological functions of molecules from shrew venom glands and extend our knowledge on the functioning of eulipotyphlan venom systems. Because the majority of existing and putative venomous mammals use oral venom systems to inject venom into target species, the methods presented here provide a promising avenue for confirming or discovering new taxa of venomous mammals.

Correction: Blair et al. Molecular Phylogenetic Relationships and Unveiling Novel Genetic Diversity among Slow and Pygmy Lorises, including Resurrection of Xanthonycticebus intermedius. Genes 2023, 14, 643.

In the original publication [...].

Slowly Making Sense: A Review of the Two-Step Venom System within Slow (Nycticebus spp.) and Pygmy Lorises (Xanthonycticebus spp.).

Since the early 2000s, studies of the evolution of venom within animals have rapidly expanded, offering new revelations on the origins and development of venom within various species. The venomous mammals represent excellent opportunities to study venom evolution due to the varying functional usages, the unusual distribution of venom across unrelated mammals and the diverse variety of delivery systems. A group of mammals that excellently represents a combination of these traits are the slow (Nycticebus spp.) and pygmy lorises (Xanthonycticebus spp.) of south-east Asia, which possess the only confirmed two-step venom system. These taxa also present one of the most intriguing mixes of toxic symptoms (cytotoxicity and immunotoxicity) and functional usages (intraspecific competition and ectoparasitic defence) seen in extant animals. We still lack many pieces of the puzzle in understanding how this venom system works, why it evolved what is involved in the venom system and what triggers the toxic components to work. Here, we review available data building upon a decade of research on this topic, focusing especially on why and how this venom system may have evolved. We discuss that research now suggests that venom in slow lorises has a sophisticated set of multiple uses in both intraspecific competition and the potential to disrupt the immune system of targets; we suggest that an exudate diet reveals several toxic plants consumed by slow and pygmy lorises that could be sequestered into their venom and which may help heal venomous bite wounds; we provide the most up-to-date visual model of the brachial gland exudate secretion protein (BGEsp); and we discuss research on a complement component 1r (C1R) protein in saliva that may solve the mystery of what activates the toxicity of slow and pygmy loris venom. We conclude that the slow and pygmy lorises possess amongst the most complex venom system in extant animals, and while we have still a lot more to understand about their venom system, we are close to a breakthrough, particularly with current technological advances.

Molecular Phylogenetic Relationships and Unveiling Novel Genetic Diversity among Slow and Pygmy Lorises, including Resurrection of Xanthonycticebus intermedius.

Genetic analysis of historical museum collections presents an opportunity to clarify the evolutionary history of understudied primate groups, improve taxonomic inferences, and inform conservation efforts. Among the most understudied primate groups, slow and pygmy lorises (genera Nycticebus and Xanthonycticebus) are nocturnal strepsirrhines found in South and Southeast Asia. Previous molecular studies have supported five species, but studies using morphological data suggest the existence of at least nine species. We sequenced four mitochondrial loci, CO1, cytb, d-loop, and ND4, for a total of 3324 aligned characters per sample from 41 historical museum specimens for the most comprehensive geographic coverage to date for these genera. We then combined these sequences with a larger dataset composed of samples collected in Vietnam as well as previously published sequences (total sample size N = 62). We inferred phylogenetic relationships using Bayesian inference and maximum likelihood methods based on data from each locus and on concatenated sequences. We also inferred divergence dates for the most recent common ancestors of major lineages using a BEAST analysis. Consistent with previous studies, we found support for Xanthonycticebus pygmaeus as a basal taxon to the others in the group. We also confirmed the separation between lineages of X. pygmaeus from northern Vietnam/Laos/China and southern Vietnam/Cambodia and included a taxonomic revision recognizing a second taxon of pygmy loris, X. intermedius. Our results found support for multiple reciprocally monophyletic taxa within Borneo and possibly Java. The study will help inform conservation management of these trade-targeted animals as part of a genetic reference database for determining the taxonomic unit and provenance of slow and pygmy lorises confiscated from illegal wildlife trade activities.

The Fast and the Furriest: Investigating the Rate of Selection on Mammalian Toxins.

The evolution of venom and the selection pressures that act on toxins have been increasingly researched within toxinology in the last two decades, in part due to the exceptionally high rates of diversifying selection observed in animal toxins. In 2015, Sungar and Moran proposed the 'two-speed' model of toxin evolution linking evolutionary age of a group to the rates of selection acting on toxins but due to a lack of data, mammals were not included as less than 30 species of venomous mammal have been recorded, represented by elusive species which produce small amounts of venom. Due to advances in genomics and transcriptomics, the availability of toxin sequences from venomous mammals has been increasing. Using branch- and site-specific selection models, we present the rates of both episodic and pervasive selection acting upon venomous mammal toxins as a group for the first time. We identified seven toxin groups present within venomous mammals, representing Chiroptera, Eulipotyphla and Monotremata: KLK1, Plasminogen Activator, Desmallipins, PACAP, CRiSP, Kunitz Domain One and Kunitz Domain Two. All but one group (KLK1) was identified by our results to be evolving under both episodic and pervasive diversifying selection with four toxin groups having sites that were implicated in the fitness of the animal by TreeSAAP (Selection on Amino Acid Properties). Our results suggest that venomous mammal ecology, behaviour or genomic evolution are the main drivers of selection, although evolutionary age may still be a factor. Our conclusion from these results indicates that mammalian toxins are following the two-speed model of selection, evolving predominately under diversifying selection, fitting in with other younger venomous taxa like snakes and cone snails-with high amounts of accumulating mutations, leading to more novel adaptions in their toxins.

Training in the Dark: Using Target Training for Non-Invasive Application and Validation of Accelerometer Devices for an Endangered Primate (Nycticebus bengalensis).

Accelerometers offer unique opportunities to study the behaviour of cryptic animals but require validation to show their accuracy in identifying behaviours. This validation is often undertaken in captivity before use in the wild. While zoos provide important opportunities for trial field techniques, they must consider the welfare and health of the individuals in their care and researchers must opt for the least invasive techniques. We used positive reinforcement training to attach and detach a collar with an accelerometer to an individual Bengal slow loris (Nycticebus bengalensis) at the Shaldon Wildlife Trust, U.K. This allowed us to collect accelerometer data at different periods between January-June 2020 and January-February 2021, totalling 42 h of data with corresponding video for validation. Of these data, we selected 54 min where ten behaviours were present and ran a random forest model. We needed 39 15-min sessions to train the animal to wear/remove the collar. The accelerometer data had an accuracy of 80.7 ± SD 9.9% in predicting the behaviours, with 99.8% accuracy in predicting resting, and a lower accuracy (but still >75% for all of them apart from suspensory walk) for the different types of locomotion and feeding behaviours. This training and validation technique can be used in similar species and shows the importance of working with zoos for in situ conservation (e.g., validation of field techniques).

Risk of Viral Infectious Diseases from Live Bats, Primates, Rodents and Carnivores for Sale in Indonesian Wildlife Markets.

Southeast Asia is considered a global hotspot of emerging zoonotic diseases. There, wildlife is commonly traded under poor sanitary conditions in open markets; these markets have been considered 'the perfect storm' for zoonotic disease transmission. We assessed the potential of wildlife trade in spreading viral diseases by quantifying the number of wild animals of four mammalian orders (Rodentia, Chiroptera, Carnivora and Primates) on sale in 14 Indonesian wildlife markets and identifying zoonotic viruses potentially hosted by these animals. We constructed a network analysis to visualize the animals that are traded alongside each other that may carry similar viruses. We recorded 6725 wild animals of at least 15 species on sale. Cities and markets with larger human population and number of stalls, respectively, offered more individuals for sale. Eight out of 15 animal taxa recorded are hosts of 17 zoonotic virus species, nine of which can infect more than one species as a host. The network analysis showed that long-tailed macaque has the greatest potential for spreading viral diseases, since it is simultaneously the most traded species, sold in 13/14 markets, and a potential host for nine viruses. It is traded alongside pig-tailed macaques in three markets, with which it shares six viruses in common (Cowpox, Dengue, Hepatitis E, Herpes B, Simian foamy, and Simian retrovirus type D). Short-nosed fruit bats and large flying foxes are potential hosts of Nipah virus and are also sold in large quantities in 10/14 markets. This study highlights the need for better surveillance and sanitary conditions to avoid the negative health impacts of unregulated wildlife markets.

Aposematic signaling and seasonal variation in dorsal pelage in a venomous mammal.

In mammals, colouration patterns are often related to concealment, intraspecific communication, including aposematic signals, and physiological adaptations. Slow lorises (Nycticebus spp.) are arboreal primates native to Southeast Asia that display stark colour contrast, are highly territorial, regularly enter torpor, and are notably one of only seven mammal taxa that possess venom. All slow loris species display a contrasting stripe that runs cranial-caudally along the median sagittal plane of the dorsum. We examine whether these dorsal markings facilitate background matching, seasonal adaptations, and intraspecific signaling. We analyzed 195 images of the dorsal region of 60 Javan slow loris individuals (Nycticebus javanicus) from Java, Indonesia. We extracted greyscale RGB values from dorsal pelage using ImageJ software and calculated contrast ratios between dorsal stripe and adjacent pelage in eight regions. We assessed through generalized linear mixed models if the contrast ratio varied with sex, age, and seasonality. We also examined whether higher contrast was related to more aggressive behavior or increased terrestrial movement. We found that the dorsal stripe of N. javanicus changed seasonally, being longer and more contrasting in the wet season, during which time lorises significantly increased their ground use. Stripes were most contrasting in younger individuals of dispersal age that were also the most aggressive during capture. The dorsal stripe became less contrasting as a loris aged. A longer stripe when ground use is more frequent can be related to disruptive colouration. A darker anterior region by younger lorises with less fighting experience may allow them to appear larger and fiercer. We provide evidence that the dorsum of a cryptic species can have multimodal signals related to concealment, intraspecific communication, and physiological adaptations.

The Role of the Songbird Trade as an Anthropogenic Vector in the Spread of Invasive Non-Native Mynas in Indonesia.

The wildlife trade has facilitated the introduction of invasive non-native species, which may compete with native species for resources and alter ecosystems. Some of these species have great potential to become invasive if released or escaped from captivity. Here we studied the pet trade in a group of open countryside birds, the mynas (Acridotheres spp.) in Indonesia, and identified the areas that are at high risk of facing the establishment of these species. Mynas are among the most invasive birds in Southeast Asia. Once established in a new area, they are almost impossible to eradicate and can have strong negative impacts on the ecosystem. Preventing their introduction is therefore essential. Yet, invasive non-native mynas continue to be traded openly. We present data on the trade in seven species of mynas on Java, Bali and Lombok, with three species being native to parts of one or two of these islands, but not to the remainder, and four that are non-native to the region. From 2016 to 2021 we conducted 255 surveys of 30 animal markets. We recorded over 6000 mynas that were offered for sale outside their native range. Areas most at risk because of their high prevalence in specific animal markets, are Greater Jakarta, eastern Java, Bali and Lombok. The number of invasive non-native mynas recorded was positively related to the size of the animal market. Indonesia is signatory to several international agreements (CBD, ASEAN) that have policies and guidelines to prevent the introduction of invasive non-native species, but compliancy is weak. Annually hundreds and possibly thousands of invasive non-native mynas are released by Indonesian conservation authorities in regions that are outside their native range. Effective management of, and regulation of trade in, potential invasive non-native birds in Indonesia falls short and inadvertently greatly aids both their introduction and establishment.

Density estimates of Panamanian owl monkeys (Aotus zonalis) in three habitat types.

The resolution of the ambiguity surrounding the taxonomy of Aotus means data on newly classified species are urgently needed for conservation efforts. We conducted a study on the Panamanian owl monkey (Aotus zonalis) between May and July 2008 at three localities in Chagres National Park, located east of the Panama Canal, using the line transect method to quantify abundance and distribution. Vegetation surveys were also conducted to provide a baseline quantification of the three habitat types. We observed 33 individuals within 16 groups in two out of the three sites. Population density was highest in Campo Chagres with 19.7 individuals/km(2) and intermediate densities of 14.3 individuals/km(2) were observed at Cerro Azul. In la Llana A. zonalis was not found to be present. The presence of A. zonalis in Chagres National Park, albeit at seemingly low abundance, is encouraging. A longer-term study will be necessary to validate the further abundance estimates gained in this pilot study in order to make conservation policy decisions.

The Toxicological Intersection between Allergen and Toxin: A Structural Comparison of the Cat Dander Allergenic Protein Fel d1 and the Slow Loris Brachial Gland Secretion Protein.

Slow lorises are enigmatic animal that represent the only venomous primate lineage. Their defensive secretions have received little attention. In this study we determined the full length sequence of the protein secreted by their unique brachial glands. The full length sequences displayed homology to the main allergenic protein present in cat dander. We thus compared the molecular features of the slow loris brachial gland protein and the cat dander allergen protein, showing remarkable similarities between them. Thus we postulate that allergenic proteins play a role in the slow loris defensive arsenal. These results shed light on these neglected, novel animals.

Arboreal route navigation in a Neotropical mammal: energetic implications associated with tree monitoring and landscape attributes.

BACKGROUND: Although navigating along a network of routes might constrain animal movement flexibility, it may be an energetically efficient strategy. Routinely using the same route allows for visually monitoring of food resources, which might reduce the cognitive load and as such facilitate the process of movement decision-making. Similarly, locating routes in areas that avoid costly landscape attributes will enhance their overall energy balance. In this study we determined the benefits of route navigation in an energy minimiser arboreal primate, the black howler monkey (Alouatta pigra). METHODS: We monitored five neighbouring groups of black howler monkeys at Palenque National Park, Mexico from September 2016 through August 2017. We recorded the location of the focal group every 20 m and mapped all travel paths to establish a route network (N = 1528 travel bouts). We constructed linear mixed models to assess the influence of food resource distribution (N = 931 trees) and landscape attributes (slope, elevation and presence of canopy gaps) on the location of routes within a route network. RESULTS: The number of food trees that fell within the visual detection distance from the route network was higher (mean: 156.1 ± SD 44.9) than randomly simulated locations (mean: 121.9 ± SD 46.4). Similarly, the number of food trees found within the monkey's visual range per meter travelled increased, on overage, 0.35 ± SE 0.04 trees/m with increasing use of the route. In addition, route segments used at least twice were more likely to occur with increasing density of food resources and decreasing presence of canopy gaps. Route segments used at least four times were more likely to occur in elevated areas within the home ranges but only under conditions of reduced visual access to food resources. CONCLUSIONS: Route navigation emerged as an efficient movement strategy in a group-living arboreal primate. Highly used route segments potentially increased visual access to food resources while avoiding energetically costly landscape features securing foraging success in a tropical rainforest.

Venom in Furs: Facial Masks as Aposematic Signals in a Venomous Mammal.

The function of colouration in animals includes concealment, communication and signaling, such as the use of aposematism as a warning signal. Aposematism is unusual in mammals, and exceptions help us to understand its ecology and evolution. The Javan slow loris is a highly territorial venomous mammal that has a distinctive facial mask and monochromatic vision. To help understand if they use aposematism to advertise their venom to conspecifics or predators with different visual systems, we studied a population in Java, Indonesia. Using ImageJ, we selected colours from the facial masks of 58 individuals, converted RBG colours into monochromatic, dichromatic and trichromatic modes, and created a contrast index. During 290 captures, we recorded venom secretion and aggressiveness. Using Non-metric Multidimensional Scaling and generalised additive models for location, scale and shape, we found that young slow lorises differ significantly from adults, being both more contrasting and more aggressive, with aggressive animals showing fewer wounds. We suggest aposematic facial masks serve multiple purposes in slow lorises based on age. Change in colouration through development may play a role in intraspecific competition, and advertise toxicity or aggressiveness to competitors and/or predators in juveniles. Aposematic signals combined with intraspecific competition may provide clues to new venomous taxa among mammals.

Environment shapes sleep patterns in a wild nocturnal primate.

Among primates, the suborder Haplorhini is considered to have evolved a consolidated monophasic sleep pattern, with diurnal species requiring a shorter sleep duration than nocturnal species. Only a few primate species have been systematically studied in their natural habitat where environmental variables, including temperature and light, have a major influence on sleep and activity patterns. Here we report the first sleep study on a nocturnal primate performed in the wild. We fitted seven wild Javan slow lorises (Nycticebus javanicus) in West Java, Indonesia with accelerometers that collected activity data, and installed climate loggers in each individual's home range to collect ambient temperature readings (over 321 days in total). All individuals showed a strictly nocturnal pattern of activity and displayed a striking synchronisation of onset and cessation of activity in relation to sunset and sunrise. The longest consolidated rest episodes were typically clustered near the beginning and towards the end of the light period, and this pattern was inversely related to daily fluctuations of the ambient temperature. The striking relationship between daily activity patterns, light levels and temperature suggests a major role of the environment in shaping the daily architecture of waking and sleep. We concluded that well-known phenotypic variability in daily sleep amount and architecture across species may represent an adaptation to changes in the environment. Our data suggest that the consolidated monophasic sleep patterns shaped by environmental pressures observed in slow lorises represent phylogenetic inertia in the evolution of sleep patterns in humans.