Phylogenetic diversity and the conservation biogeography of African primates

Aim Phylogenetics has an important role in conservation biogeography. However, there are few data on the phylogenetic diversity of African primates. The phylogenetic diversity (PD) of a species is a measure of its taxonomic distinctness and can be estimated by looking at the phylogenetic relationships among taxa. Species‐specific metrics on PD can then be used to determine conservation priorities at various biogeographical scales. We used PD metrics to rank 55 African primate species according to their conservation priorities at the country level and within six African biogeographical regions. We also addressed the following question: are there differences in conservation rankings between the IUCN Red List and our PD metrics? Location Africa. Methods We created a consensus phylogeny for all African primate clades based on genetic studies. Analyses of species distributions were determined using presence/absence scores at two levels: country and biogeographical region. A node‐based method that standardizes for widespread taxa and endemicity was used to calculate PD indices. Hierarchical cluster analysis was used to convert one of the standardized, phylogenetic indices into three clusters that could be ranked and compared with the main IUCN conservation rankings of endangered, vulnerable, and lower risk. Results At the country and region levels, the top‐priority species in terms of PD are Pan paniscus, Macaca sylvanus, Arctocebus calabarensis, Gorilla beringei, Arctocebus aureus, Allenopithecus nigroviridis, Gorilla gorilla, Procolobus verus, Cercopithecus solatus, Cercocebus galeritus, Colobus angolensis, Theropithecus gelada, Galagoides zanzibaricus, Galagoides granti, and Procolobus (Piliocolobus) badius. Geographic rankings were highest for the Democratic Republic of the Congo (country level) and Central Africa (region level). Although there were no overall differences between IUCN conservation ranks and the PD rankings, there were significant differences between the two systems for vulnerable and endangered primate taxa. Main conclusions There are few ecological and behavioural data on populations of some of the African primates that represent the highest levels of phylogenetic diversity. Studies of primate taxa with high PD rankings should focus on identifying sites suitable for intensive studies of population densities, feeding ecology, and reproductive behaviour. We suggest that PD metrics can serve as an important, complementary data set in the IUCN ranking system for primates.     

Conservation biology of Malagasy strepsirhines: a phylogenetic approach

The phylogenetic diversity of extant lemurs represents one of the most important but least studied aspects of the conservation biology of primates. The phylogenetic diversity of a species is inversely proportional to the relative number and closeness of its phylogenetic relatives. Phylogenetic diversity can then be used to determine conservation priorities for specific biogeographic regions. Although Malagasy strepsirhines represent the highest phylogenetic diversity among primates at the global level, there are few phylogenetic data on species-specific and regional conservation plans for lemurs in Madagascar. Therefore, in this paper the following questions are addressed for extant lemurs: 1) how does the measure of taxonomic uniqueness used by Mittermeier et al. (1992 Lemurs of Madagascar; Gland, Switzerland: IUCN) equate with an index of phylogenetic diversity, 2) what are the regional conservation priorities based on analyses of phylogenetic diversity in extant lemurs, and 3) what conservation recommendations can be made based on analyses of phylogenetic diversity in lemurs? Taxonomic endemicity standardized weight (TESW) indices of phylogenetic diversity were used to determine the evolutionary component of biodiversity and to prioritize regions for conserving lemur taxa. TESW refers to the standardization of phylogenetic diversity indices for widespread taxa and endemicity of species. The phylogenetic data came from recent genetic studies of Malagasy strepsirhines at the species level. Lemur species were assigned as being either present or absent in six biogeographic regions. TESW indices were combined with data on lemur complementarity and protected areas to assign conservation priorities at the regional level. Although there were no overall differences between taxonomic ranks and phylogenetic rankings, there were significant differences for the top-ranked taxa. The phylogenetic component of lemur diversity is greatest for Daubentonia madagascariensis, Allocebus trichotis, Lepilemur septentrionalis, Indri indri, and Mirza coquereli. Regional conservation priorities are highest for lemurs that range into northeast humid forests and western dry forests. Expansion of existing protected areas in these regions may provide the most rapid method for preserving lemurs. In the long term, new protected areas must be created because there are lemur species that: 1) are not found in existing protected areas, 2) exist only in one or two protected areas, and 3) are still being discovered outside the current network of protected areas. Data on the population dynamics and feeding ecology of phylogenetically important species are needed to ensure that protected areas adequately conserve lemur populations in Madagascar.     

Primate Conservation in Vietnam: Toward a Holistic Environmental Narrative

Vietnam is home to a considerable diversity of primates: Indeed, five of the world's top 25 most endangered primate species are found within Vietnam. To understand and ultimately address Vietnam's conservation crisis, the complex interplay of history, demography, economics, international relations, and culture must be analyzed within Vietnam's specific context. Conducting a holistic analysis with the example of hunting represents how seemingly disparate factors such as the U.S. war, increased tourism and globalization, population density, and cultural traditions converge to significantly impact wildlife.     

非人灵长类种群数量调查方法综述

监测估算野生动物的种群数量是保护的核心工作。由于气候变化和人类活动的影响,野生动物种群常处于不稳定的状态。非人灵长类是动物界的高等类群,具有复杂的社会行为、丰富的物种多样性,全球有701种 (含亚种),生活在多种类型的栖息地中,包括热带雨林、沼泽森林、红树林、次生林、落叶林、季雨林、山地森林,和包含孤存林、长廊森林、热带旱生林、山地草甸、地中海灌木林的稀树草原和干草原,以及荒漠、干旱的山地,甚至是雪地。绝大多数非人灵长类处于濒危的状态,长期有效的监测对于灵长类的保护十分重要。物种多样性和栖息地类型的多样性使得灵长类种群数量的调查方法多种多样。本文归纳总结了目前常用的非人灵长类种群数量调查方法的类型、基本原理、适用场景和局限性,并以研究实例加以分析;介绍了无人机、热成像、计算机学习系统等新技术应用在调查方法中的进展,希望为今后的非人灵长类野外数量调查、种群监测提供参考和启发。     

The primate palette: The evolution of primate coloration

Flip through The Pictorial Guide to the Living Primates¹ and you will notice a striking yet generally underappreciated aspect of primate biology: primates are extremely colorful. Primate skin and pelage coloration were highlighted examples in Darwin's² original discussions of sexual selection but, surprisingly, the topic has received little research attention since. Here we summarize the patterns of color variation observed across the primate order and examine the selective forces that might drive and maintain this aspect of primate phenotypic diversity. We discuss how primate color patterns might be adaptive for physiological function, crypsis, and communication. We also briefly summarize what is known about the genetic basis of primate pigmentation and argue that understanding the proximate mechanisms of primate coloration will be essential, not only for understanding the evolutionary forces shaping phenotypic variation, but also for clarifying primate taxonomies and conservation priorities.     

Agroecosystems and Primate Conservation in The Tropics: A Review

Agroecosystems cover more than one quarter of the global land area (ca. 50 million km²) as highly simplified (e.g. pasturelands) or more complex systems (e.g. polycultures and agroforestry systems) with the capacity to support higher biodiversity. Increasingly more information has been published about primates in agroecosystems but a general synthesis of the diversity of agroecosystems that primates use or which primate taxa are able to persist in these anthropogenic components of the landscapes is still lacking. Because of the continued extensive transformation of primate habitat into human‐modified landscapes, it is important to explore the extent to which agroecosystems are used by primates. In this article, we reviewed published information on the use of agroecosystems by primates in habitat countries and also discuss the potential costs and benefits to human and nonhuman primates of primate use of agroecosystems. The review showed that 57 primate taxa from four regions: Mesoamerica, South America, Sub‐Saharan Africa (including Madagascar), and South East Asia, used 38 types of agroecosystems as temporary or permanent habitats. Fifty‐one percent of the taxa recorded in agroecosystems were classified as least concern in the IUCN Red List, but the rest were classified as endangered (20%), vulnerable (18%), near threatened (9%), or critically endangered (2%). The large proportion of threatened primates in agroecosystems suggests that agroecosystems may play an important role in landscape approaches to primate conservation. We conclude by discussing the value of agroecosystems for primate conservation at a broad scale and highlight priorities for future research. Am. J. Primatol. 74:696‐711, 2012. © 2012 Wiley Periodicals, Inc.     

Interactions between Social Structure,Demography, and Transmission Determine Disease Persistence in Primates

Catastrophic declines in African great ape populations due to disease outbreaks have been reported in recent years, yet we rarely hear of similar disease impacts for the more solitary Asian great apes, or for smaller primates. We used an age-structured model of different primate social systems to illustrate that interactions between social structure and demography create ‘dynamic constraints’ on the pathogens that can establish and persist in primate host species with different social systems. We showed that this varies by disease transmission mode. Sexually transmitted infections (STIs) require high rates of transmissibility to persist within a primate population. In particular, for a unimale social system, STIs require extremely high rates of transmissibility for persistence, and remain at extremely low prevalence in small primates, but this is less constrained in longer-lived, larger-bodied primates. In contrast, aerosol transmitted infections (ATIs) spread and persist at high prevalence in medium and large primates with moderate transmissibility;, establishment and persistence in small-bodied primates require higher relative rates of transmissibility. Intragroup contact structure – the social network - creates different constraints for different transmission modes, and our model underscores the importance of intragroup contacts on infection prior to intergroup movement in a structured population. When alpha males dominate sexual encounters, the resulting disease transmission dynamics differ from when social interactions are dominated by mother-infant grooming events, for example. This has important repercussions for pathogen spread across populations. Our framework reveals essential social and demographic characteristics of primates that predispose them to different disease risks that will be important for disease management and conservation planning for protected primate populations.     

Interspecific Interactions between Primates,Birds, Bats,and Squirrels May Affect Community Composition on Borneo

For several decades, primatologists have been interested in understanding how sympatric primate species are able to coexist. Most of our understanding of primate community ecology derives from the assumption that these animals interact predominantly with other primates. In this study, we investigate to what extent multiple community assembly hypotheses consistent with this assumption are supported when tested with communities of primates in isolation versus with communities of primates, birds, bats, and squirrels together. We focus on vertebrate communities on the island of Borneo, where we examine the determinants of presence or absence of species, and how these communities are structured. We test for checkerboard distributions, guild proportionality, and Fox's assembly rule for favored states, and predict that statistical signals reflecting interactions between ecologically similar species will be stronger when nonprimate taxa are included in analyses. We found strong support for checkerboard distributions in several communities, particularly when taxonomic groups were combined, and after controlling for habitat effects. We found evidence of guild proportionality in some communities, but did not find significant support for Fox's assembly rule in any of the communities examined. These results demonstrate the presence of vertebrate community structure that is ecologically determined rather than randomly generated, which is a finding consistent with the interpretation that interactions within and between these taxonomic groups may have shaped species composition in these communities. This research highlights the importance of considering the broader vertebrate communities with which primates co‐occur, and so we urge primatologists to explicitly consider nonprimate taxa in the study of primate ecology. Am. J. Primatol. 75:170‐185, 2013. © 2012 Wiley Periodicals, Inc.     

Rarity in the tropics: biogeography and macroecology of the primates

Aim To describe rarity and elucidate its biology in a tropical mammalian order, the Primates. Location Africa, Central and South America, Asia, Madagascar. Methods A review of the literature, with some additional analyses using data from the literature. A variety of definitions of rarity are used in order to describe it and to investigate its biology by correlating the degree of rarity with a variety of biological traits indicative of resource use (e.g. size of annual home range), reproductive rate (e.g. birth interval)and specialization (e.g. number of habitat types used). Results Few primate taxa occur outside the tropics, and most taxa are rare (small geographical range size or latitudinal extent, low density or both). Latitudinal extent is narrower at lower latitudes in Africa and Asia, but the potential resultant packing of taxa appears not to explain the taxonomic diversity gradient. Whilst primate species do not show the common, positive density by range size relationship, primate genera show a significant shallow slope, and primate families/subfamilies a strongly positive slope. Rare taxa are specialized, but neither use more resources nor breed more slowly than common taxa. The correlation of rarity and specialization is via geographical range: taxa with small ranges, or small ranges for their density, are specialized, but not taxa at low density. Common taxa are generalized because they consist of more differently specialized subtaxa, not because each subtaxon is generalized. Main conclusions Most primate taxa are rare, in which case most are presumably likely to go extinct. Rare primates are specialized, but do not necessarily use more resources, nor breed more slowly. Specialization as an explanation for rarity appears to work via constriction of range size, not of density. Common primates might be common (large range size) not because subtaxa or individuals are generalized, but because they are composed of more subtaxa. A consequence could be that persistence of even common taxa will depend on conservation of several populations scattered across the taxon's geographical range.     

A global gap analysis of infectious agents in wild primates

A number of infectious diseases have emerged as threats to humans and wildlife. Despite the growing importance of georeferenced data for mitigating disease risk, information on parasite threat is patchily distributed at a global scale. In this paper, we explore the utility of gap analysis techniques to investigate the global geographical distribution of parasite sampling in non-human primates. Specifically, we identify geographical areas that are undersampled for parasites in relation to primate geographical distributions, primate taxonomic sampling, primate threat status, and parasite taxonomy. Our results reveal that East Asia (particularly China), South-East Asia, and the South American Amazon are the most deficient in sampling effort with respect to all criteria. We also identify sampling gaps based on several criteria in West and Central Africa. Future research aimed at filling these gaps is needed for both human health and primate conservation purposes.     

Taxonomic diversity of the terrestrial bird and mammal fauna in temperate and boreal biomes of the northern hemisphere

Abstract. Using comprehensive range information of northern Hemisphere birds and mammals, we assessed the taxonomic diversity of these two groups in four different regions: Europe, east Asia, and western and eastern North America. East Asia is the richest region in the number of bird and mammal species, genera, families and orders, except that mammal species richness is highest in western North America. Eastern North America is taxonomically the poorest region, but when only forest-associated taxa were considered in mammals taxonomic diversity is equally low in Europe and in eastern North America, and in birds, Europe is the least diverse region. Patterns in endemic taxa follow overall taxonomic diversity. The proportion of shared taxa between regions is higher among boreal species and genera than among all taxa. A comparison with tree species diversity underpins the role of east Asia as the most diverse of all northern biota. Largely congruent patterns at different taxonomic levels emphasizes the role of historical processes, such as differential extinction rate in response to paleoenvironmental fluctuations, in producing these patterns, but we stress the need for more research on the coevolution of species diversity and habitat diversity.     

Diversity,Body Mass,and Latitudinal Gradients in Primates

We examined latitudinal gradients in central value and diversity of body mass of primates to increase understanding of the Forster effect (decrease in taxonomic diversity with increasing latitude) and the Bergmann effect (increase of body mass with latitude). Data are from the literature. We used species’ median body mass of females and mid-latitude (N = 164). We account for phylogenetic effects with comparative analysis by independent contrasts and analysis at differing taxonomic levels. Globally, diversity of both taxonomy and body mass declined significantly with increasing latitude. The decrease in the range of body masses with increasing latitude was caused mainly by the absence of several small-bodied clades at higher latitudes, but also by the absence there of great apes. The disappearance of the small-bodied clades caused an increase in median body mass with latitude, i.e., primates show a significant taxon-wide Bergmann effect, including with phylogenetic correction. Within the Primates, the Bergmann effect was significant within taxa that extend from the equator the farthest into temperate regions: the Old World infraorder Catarrhini, family Cercopithecidae, and subfamily Cercopithecinae; the Asian Cercopithecidae; and in Southeast Asian Sunda, Macaca. The results accord with hypotheses for the Forster effect that latitudinal gradients in taxonomic diversity result from high rates of speciation in the tropics, and ecological, and therefore evolutionary, constraints on diversity at higher latitudes. For the Bergmann effect, the results support energetic hypotheses that the very largest-bodied and the small-bodied taxa cannot survive the long periods of limited resources at higher latitudes.     

Distribution,population density and conservation of the critically endangered brown spider monkey (<Emphasis Type="Italic">Ateles hybridus</Emphasis>) and other primates of the inter-Andean forests of Colombia

The inter-Andean tropical rainforests and dry forests of the Magdalena river basin (Tumbes-Choco-Magdalena biodiversity hotspot) in northern Colombia have undergone significant forest loss and degradation in recent decades. Six primate species inhabit this region, five of which are currently threatened with extinction and one of which—the brown spider monkey, Ateles hybridus—is considered critically endangered. Accurate and recent information on the distribution and conservation status of these threatened primate populations is scarce or nonexistent, even though such data are needed to implement successful conservation actions and management plans. Between 2006 and 2016, we evaluated the status and distribution of primates across inter-Andean lowland forests in northern Colombia. We visited 30 sites to evaluate the presence/absence of brown spider monkeys and other primate taxa in the region. We also carried out surveys at 10 of these sites to obtain estimates of primate population densities and demographic information from forests with different levels of anthropogenic disturbance. Novel data on primate presence/absence were obtained for 27 sites, and 136 records were collected in total. Only 33% of the sites visited were large forest fragments (>?500 Ha). This study confirms that at least six primate species are still present in the Rio Magdalena region, which represents the highest platyrrhine diversity west of the Andes. This study also confirms the persistence of a wild population of Colombian woolly monkeys (Lagothrix lagotricha lugens) in the Serranía de San Lucas. Assigning formal protected status to this region is an urgent priority for the conservation of primates in the Rio Magdalena region.     

Low Primate Diversity and Abundance in Northern Amazonia and its Implications for Conservation

Large areas of the Rio Negro basin in Amazonia are covered by continuous tracts of tropical forest, but have few primate species. This is anomalous considering the general relationship between area and number of species. One possibility is that much of the forest is unsuitable habitat for most primates and the area of suitable habitat is much less than the forested area. This has important consequences for the design of reserves and predictions of the consequences of climate change, which tend to be based on broad categories based on satellite images, and not on information of species distributions within those broad categories. The study was conducted through diurnal and nocturnal line‐transect surveys in the Biodiversity Research Program 25‐km² permanent grid in Viruá National Park, which has vegetation associations typical of much of northern Amazonia. The highest primate diversity and abundances occurred in tall terra firme forests (58%), whereas inundated forests and scrublands, which cover 42 percent of the survey grid and 90.8 percent of the Viruá National Park, have virtually no primates. This suggests that parks and reserves in northwestern Amazonia will have to be very large to maintain viable populations of most primates and their ecological interactions, and that very broad habitat categories are not sufficient to make predictions about actual and future suitability of areas for primate conservation.     

The subspecies concept in primatology: The case of mountain gorillas

The criteria for the application of subspecific units in living primate populations have received little attention relative to other vertebrate taxa, even though they have important implications for conservation strategies for many nonhuman primate populations. One of the most critically endangered primates is the mountain gorilla,Gorilla gorilla beringei, of which 600 animals exist in east-central Africa. FollowingSarmiento et al. (1996), taxonomists have proposed splitting these populations into two subspecies as part of a revised taxonomy of the genusGorilla. In this paper I review the application of the subspecies concept in primatology, using the gorillas of Bwindi Impenetrable National Park and the Virungas as case studies. An examination of genetic, morphological, biogeographic, ecological, and behavioral evidence indicates that reclassifying Bwindi gorillas as taxonomically distinct from those in the Virungas is not well supported and needs further study. Because taxonomy provides the basis of conservation management policies, a cautious and conservative approach to the subspecies question is warranted in the case of endangered primate populations.     

A Mitogenomic Phylogeny of Living Primates

Primates, the mammalian order including our own species, comprise 480 species in 78 genera. Thus, they represent the third largest of the 18 orders of eutherian mammals. Although recent phylogenetic studies on primates are increasingly built on molecular datasets, most of these studies have focused on taxonomic subgroups within the order. Complete mitochondrial (mt) genomes have proven to be extremely useful in deciphering within-order relationships even up to deep nodes. Using 454 sequencing, we sequenced 32 new complete mt genomes adding 20 previously not represented genera to the phylogenetic reconstruction of the primate tree. With 13 new sequences, the number of complete mt genomes within the parvorder Platyrrhini was widely extended, resulting in a largely resolved branching pattern among New World monkey families. We added 10 new Strepsirrhini mt genomes to the 15 previously available ones, thus almost doubling the number of mt genomes within this clade. Our data allow precise date estimates of all nodes and offer new insights into primate evolution. One major result is a relatively young date for the most recent common ancestor of all living primates which was estimated to 66-69 million years ago, suggesting that the divergence of extant primates started close to the K/T-boundary. Although some relationships remain unclear, the large number of mt genomes used allowed us to reconstruct a robust primate phylogeny which is largely in agreement with previous publications. Finally, we show that mt genomes are a useful tool for resolving primate phylogenetic relationships on various taxonomic levels.     

Knowledge of Colombian biodiversity: published and indexed

Documenting patterns of published studies on the biodiversity of megadiverse countries can offer valuable insights on global biodiversity knowledge. Here, I present results from a bibliometric analysis of 5,264 indexed publications on biodiversity in Colombia published during the period 1990–2011 and gathered by searching the Web of Knowledge database. I classified studies into six overlapping subjects: taxa lists, new taxa, new records, conservation, genetic diversity, and other. Publications were also classified by geographic location and the taxonomic group studied. I found variation in the number of studies per year, which presented a long-term trend of increasing volume. The 31 continental departments of Colombia and both the Atlantic and the Pacific oceans were represented in the studies, which included 98 taxonomic classes from 47 phyla. However, there were strong biases in taxonomic, geographic, and subject coverage. For instance, 75 % of studies focused on animals; and the Atlantic Ocean showed the highest number of studies, followed by Antioquia and Valle del Cauca departments. Genetic diversity and conservation were the least-studied subjects. I also found that Colombian researchers and Colombian institutions have played an important role in documenting the country’s outstanding biodiversity. However, Colombian biologists still prefer to publish in domestic or Latin American journals, which are mainly regional and have low international visibility. The patterns I present here can have important implications for optimizing and guiding research on Colombian biodiversity, and the paper concludes with some recommendations.     

Phylogenetics and the conservation of rare taxa in the Eucalyptus angustissima complex in Western Australia

Effective conservation that preservesevolutionary entities and processes requiresconservation action that is targeted atappropriate taxonomic units. Molecularphylogenetics can contribute to the resolutionof taxonomic uncertainties by defining therelationships between populations and species,and allowing the recognition of taxonomicentities that reflect evolutionary history.Some uncertainty surrounds the status of taxain the Eucalyptus angustissima complex,which includes threatened taxa with restricteddistributions. The phylogenetic relationshipsbetween populations and taxa in the E.angustissima complex were investigated usingnuclear and chloroplast RFLP analysis.Phylogenetic relationships confirmed thegenetic differentiation of two taxa, identifiedspecies level divergence between two taxacurrently recognised at subspecies level, andestablished the identity of a previouslyundetermined population. Phylogeneticrelationships between the taxa were notcongruent with presumed relationships based onmorphological characters alone.     

Taxonomic complexity,population genetics,and plant conservation in Scotland

Summary

Groups of plants that are undergoing active diversification often do not fall into neat and tidy taxonomies. In such groups it can sometimes be very difficult to establish what does, and what does not, constitute a species. This presents problems for species-based conservation programmes that are based around prioritised species-lists (e.g. the UK Biodiversity Action Plans; BAPs), particularly as the inclusion or exclusion of taxa on these lists largely determines the allocation of conservation resources. This is an important issue as almost half of the BAP priority higher plant species for which Scotland has prime responsibility are taxonomically controversial.

Recent research using population genetic approaches to tackle some taxonomically complex plant groups has enhanced our understanding of their biology. Such approaches provide objective and independent assessments of whether a given entity is distinct or not. This information can then be used to contribute towards the decision making process of which taxa to prioritise for conservation, and address specific questions regarding BAP listed species. In the long term, however, a broader issue needs tackling. Actively evolving groups often contain a series of localised lineages, as well as complex populations that exhibit atypical levels of morphological diversity. These types of diversity do not fit well into a ‘standard’ species-based conservation system. In most cases protection will best be supplied by designated site protection or wider countryside habitat schemes. Where additional protection is need, a conservation policy is required that accepts the diversity in these actively evolving groups for what it is, rather than trying to squeeze it into conservation legislation derived for taxa whose delimitation is routine.