Effects of habitat fragmentation and disturbance on howler monkeys: a review

We examined the literature on the effects of habitat fragmentation and disturbance on howler monkeys (genus Alouatta) to (1) identify different threats that may affect howlers in fragmented landscapes; (2) review specific predictions developed in fragmentation theory and (3) identify the empirical evidence supporting these predictions. Although howlers are known for their ability to persist in both conserved and disturbed conditions, we found evidence that they are negatively affected by high levels of habitat loss, fragmentation and degradation. Patch size appears to be the main factor constraining populations in fragmented habitats, probably because patch size is positively related to food availability, and negatively related to anthropogenic pressures, physiological stress and parasite loads. Patch isolation is not a strong predictor of either patch occupancy or population size in howlers, a result that may be related to the ability of howlers to move among forest patches. Thus, we propose that it is probable that habitat loss has larger consistent negative effects on howler populations than habitat fragmentation per se. In general, food availability decreases with patch size, not only due to habitat loss, but also because the density of big trees, plant species richness and howlers' home range size are lower in smaller patches, where howlers' population densities are commonly higher. However, it is unclear which vegetation attributes have the biggest influence on howler populations. Similarly, our knowledge is still limited concerning the effects of postfragmentation threats (e.g. hunting and logging) on howlers living in forest patches, and how several endogenous threats (e.g. genetic diversity, physiological stress, and parasitism) affect the distribution, population structure and persistence of howlers. More long‐term studies with comparable methods are necessary to quantify some of the patterns discussed in this review, and determine through meta‐analyses whether there are significant inter‐specific differences in species' responses to habitat loss and fragmentation. Am. J. Primatol. 72:1–16, 2010. © 2009 Wiley‐Liss, Inc.     

Cougar Predation on Black-and-Gold Howlers on Mutum Island,Southern Brazil<Superscript>1</Superscript>

Researchers consider predation rates by terrestrial animals to be lower in the case of arboreal primates, particularly among large-bodied species. We recorded the consumption of black-and-gold howlers (Alouatta caraya) by cougars (Puma concolor) as evidence of predation on an island of the upper Paraná River. We collected and processed fecal samples of the felid in 2004 and 2005. We identified items in the laboratory by comparison with museum specimens. We considered each species in a fecal sample as a single occurrence. Based on analysis of the cuticle scale pattern, we identified the felid as cougar. Howlers occurred in 4 out of the 8 fecal samples (40% of the occurrences). In addition to howlers, we also recorded 5 occurrences of agouti (Dasyprocta azarae; 50%) and a small unidentified sigmodontine rodent (10%). The abundance of howlers and the low forest canopy in a successional vegetation might have facilitated the predation of the large primates by a primarily terrestrial predator. The versatility of cougars is corroborated by the consumption of prey species that were abundant in the region and that were available in different forest strata, such as howlers and agoutis.     

Morphology and somatometric growth of long-tailed macaques (Macaca fascicularis fascicularis) in Singapore

Crab-eating, or long-tailed, macaques [ Macaca fascicularis (Raffles, 1821)] have been studied extensively throughout their distribution in South and South-east Asia. Despite this extensive body of research, the island population of long-tailed macaques from Singapore remains virtually undescribed. In the present study, we compare the morphometric variability and patterns of growth observed in a population sample from Singapore with a composite sample from Thailand, north of the Isthmus of Kra. The results of our analyses indicate that there are statistically significant differences between the two populations in adult size and shape. For both males and females, the Singapore population is smaller than the Thai population. Relative to body length, the Singapore macaques exhibit significantly longer tails, and, relative to cranial length, they exhibit significantly more narrow faces than the Thai macaques. Although levels of sexual dimorphism for most morphometric traits are very similar, indicating similar levels of male–male competition for females, the Singapore males exhibit a significantly larger testicular volume relative to body weight, suggestive of an alternative male reproductive strategy. In addition to adult somatometric size and shape, comparisons of growth patterns relative to age and body size reveal significant differences between the two population samples. Combined, these results suggest either that statistically significant differences in adult morphology and patterns of growth can occur in presumably reproductively cohesive subspecies, or the Singapore macaques may be taxonomically distinct.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 675–694.     

Comparative morphometrics of the primate apical tuft

The relationship between the structure and function of the primate apical tuft is poorly understood. This study addresses several hypotheses about apical tuft morphology using a large modern primate comparative sample. Two indices of tuft size are employed: expansion and robusticity. First, comparisons of relative apical tuft size were drawn among extant nonhuman primate groups in terms of locomotion and phylogenetic category. Both of these factors appear to play a role in apical tuft size among nonhuman primates. Suspensory primates and all platyrrhines had the smallest apical tufts, while terrestrial quadrupeds and all strepsirrhines (regardless of locomotor category) had the largest tufts. Similarly, hypotheses regarding the apical tufts of hominins, especially the large tufts of Neandertals were addressed using a comparison of modern warm- and cold-adapted humans. The results showed that cold-adapted populations possessed smaller apical tufts than did warm-adapted groups. Therefore, the cold-adaptation hypothesis for Neandertal distal phalangeal morphology is not supported. Also, early modern and Early Upper Paleolithic humans had apical tufts that were significantly less expanded and less robust than those of Neandertals. The hypothesis that a large apical tuft serves as support for an expanded digital pulp is supported by radiographic analysis of modern humans in that a significant correlation was discovered between the width of the apical tuft and the width of the pulp. The implications of these findings for hypotheses about the association of apical tuft size and tool making in the hominin fossil record are discussed.     

Trisomy 17 in a baboon (Papio hamadryas) with polydactyly, patent foramen ovale and pyelectasis

Trisomy 13 in humans is the third most common autosomal abnormality at birth, after trisomy 21 and trisomy 18. It has a reported incidence of between 1:5,000 and 1:30,000 live births. It is associated with multiple abnormalities, many of which shorten lifespan. We describe here the first reported case of a baboon (Papio hamadryas) with trisomy of chromosome 17, which is homologous to human chromosome 13. The trisomic infant was born to a consanguineous pair of baboons and had morphological characteristics similar to those observed in human trisomy 13, including bilateral polydactyly in the upper limbs, a patent foramen ovale, and pyelectasis. Molecular DNA analysis using human chromosome 13 markers was consistent with the affected infant inheriting two copies of chromosome 17 derived from the same parental chromosome. This trisomy was, therefore, due to either an error in meiosis II or the result of postzygotic nondisjunction. The parental origin, however, could not be determined.     

Ecogeographic size variation in small-bodied subfossil primates from Ankilitelo, southwestern Madagascar

Variation in body size is well documented for both extant and extinct Malagasy primates, and appears to be correlated with geographic patterns of resource seasonality. Less attention has been paid to extant lemurs in subfossil collections, although it has been suggested that subfossil forms of extant species are characterized by greater size than their modern counterpart. This trend of phyletic size change has been related to climate change, habitat fragmentation, or human hunting. However, space- and time-averaging in the subfossil samples of previous studies may have obscured more general ecogeographic patterns underlying these size differences. Our objective is to examine size variation in subfossil still-extant primates within a regional comparative context to determine if subfossil and living forms conform to similar ecogeographic patterns. We report on the subfossil still-extant primate assemblage from Ankilitelo, southwestern Madagascar (approximately 500 yr BP) to test this hypothesis. The Ankilitelo primates were compared with museum specimens of known locality. Extant taxa were assigned to one of five distinct ecogeographic regions, including spiny thicket, dry deciduous forest, succulent woodland, lowland and subhumid rainforest. Comparisons of tooth size in extant lemurs reveal significant geographical patterns of variation within genera. In general, the primates from Ankilitelo are indeed larger than their modern counterpart. However, these differences fit an ecoregional model of size variation, whereby Ankilitelo species are comparable in size to living forms inhabiting ecoregions present near the cave today. This suggests that Malagasy primates have been subjected to similar patterns of resource seasonality for at least 500 years.     

Predicting euarchontan body mass: A comparison of tarsal and dental variables

Objective: Multiple meaningful ecological characterizations of a species revolve around body mass. Because body mass cannot be directly measured in extinct taxa, reliable body mass predictors are needed. Many published body mass prediction equations rely on dental dimensions, but certain skeletal dimensions may have a more direct and consistent relationship with body mass. We seek to evaluate the reliability of prediction equations for inferring euarchontan body mass based on measurements of the articular facet areas of the astragalus and calcaneus. Methods: Surface areas of five astragalar facets (n = 217 specimens) and two calcaneal facets (n = 163) were measured. Separate ordinary least squares and multiple regression equations are presented for different levels of taxonomic inclusivity, and the reliability of each equation is evaluated with the coefficient of determination, standard error of the estimate, mean prediction error, and the prediction sum of squares statistic. We compare prediction errors to published prediction equations that utilize dental and/or tarsal measures. Finally, we examine the effects of taxonomically specific regressions and apply our equations to a diverse set of non‐primates. Results: Our results reveal that predictions based on facet areas are more reliable than most linear dental or tarsal predictors. Multivariate approaches are often better than univariate methods, but require more information (making them less useful for fragmentary fossils). While some taxonomically specific regressions improve predictive ability, this is not true for all primate groups. Conclusions: Among individual facets, the ectal and fibular facets of the astragalus and the calcaneal cuboid facet are the best body mass predictors. Since these facets have primarily concave curvature and scale with positive allometry relative to body mass, it appears that candidate skeletal proxies for body mass can be identified based on their curvature and scaling coefficients. Am J Phys Anthropol 157:472–506, 2015. © 2015 Wiley Periodicals, Inc.     

Optimized microRNA purification from TRIzol-treated plasma

Background

MicroRNAs (miRNAs) represent new and potentially informative diagnostic targets for disease detection and prognosis. However, little work exists documenting the effect of TRIzol, a common viral inactivation and nucleic acid extraction reagent, on miRNA purification. Here, we developed an optimized protocol for miRNA extraction from plasma samples by evaluating five different RNA extraction kits, TRIzol phase separation, purification additives, and initial plasma sample volume. This method was then used for downstream profiling of plasma miRNAs found in archived samples from one nonhuman primate (NHP) experimentally challenged with Ebola virus by the aerosol route.

Results

Comparison of real-time RT-PCR results for spiked-in and endogenous miRNA sequences determined extraction efficiencies from five different RNA purification kits. These experiments showed that 50 μL plasma processed using the QIAGEN miRNeasy Mini Kit with 5 μg of glycogen as a co-precipitant yielded the highest recovery of endogenous miRNAs. Using this optimized protocol, miRNAs from archived plasma samples of one rhesus macaque challenged with aerosolized Ebola virus was profiled using a targeted real-time PCR array. A total of 519 of the 752 unique miRNAs assayed were present in the plasma samples at day 0 and day 7 (time of death) post-exposure. Statistical analyses revealed 25 sequences significantly up- or down-regulated between day 0 and day 7 post infection, validating the utility of the extraction method for plasma miRNA profiling.

Conclusions

This study contributes to the knowledgebase of circulating miRNA extraction methods and expands on the potential applications of cell-free miRNA profiling for diagnostics and pathogenesis studies. Specifically, we optimized an extraction protocol for miRNAs from TRIzol-inactivated plasma samples that can be used for highly pathogenic viruses.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1299-5) contains supplementary material, which is available to authorized users.     

Brevity is not always a virtue in primate communication

Semple et al. (Semple et al. in press, Biol. Lett. (doi:10.1098/rsbl.2009.1062)) argued that the ‘law of brevity’ (an inverse relationship between word length and frequency of use) applies not only to human language but also to vocal signalling in non-human primates, because coding efficiency is paramount in both situations. We analysed the frequency of use of signals of different duration in the vocal repertoires of two Neotropical primate species studied in the wild—the common marmoset (Callithrix jacchus) and the golden-backed uakari (Cacajao melanocephalus). The key prediction of the law of brevity was not supported in either species: although the most frequently emitted calls were relatively brief, they were not the shortest signals in the repertoire. The costs and benefits associated with signals of different duration must be appreciated to understand properly their frequency of use. Although relatively brief vocal signals may be favoured by natural selection in order to minimize energetic costs, the very briefest signals may be ambiguous, contain reduced information or be difficult to detect or locate, and may therefore be selected against. Analogies between human language and vocal communication in animals can be misleading as a basis for understanding frequency of use, because coding efficiency is not the only factor of importance in animal communication, and the costs and benefits associated with different signal durations will vary in a species-specific manner.