Vincent Nijman

Impending extinction crisis of the world's primates: why primates matter

Impending extinction of the world’s primates due to human activities; immediate global attention is needed to reverse the trend. Nonhuman primates, our closest biological relatives, play important roles in the livelihoods, cultures, and religions of many societies and offer unique insights into human evolution, biology, behavior, and the threat of emerging diseases. They are an essential component of tropical biodiversity, contributing to forest regeneration and ecosystem health. Current information shows the existence of 504 species in 79 genera distributed in the Neotropics, mainland Africa, Madagascar, and Asia. Alarmingly, ~60% of primate species are now threatened with extinction and ~75% have declining populations. This situation is the result of escalating anthropogenic pressures on primates and their habitats—mainly global and local market demands, leading to extensive habitat loss through the expansion of industrial agriculture, large-scale cattle ranching, logging, oil and gas drilling, mining, dam building, and the construction of new road networks in primate range regions. Other important drivers are increased bushmeat hunting and the illegal trade of primates as pets and primate body parts, along with emerging threats, such as climate change and anthroponotic diseases. Often, these pressures act in synergy, exacerbating primate population declines. Given that primate range regions overlap extensively with a large, and rapidly growing, human population characterized by high levels of poverty, global attention is needed immediately to reverse the looming risk of primate extinctions and to attend to local human needs in sustainable ways. Raising global scientific and public awareness of the plight of the world’s primates and the costs of their loss to ecosystem health and human society is imperative.

CITES Proposal Highlights Rarity of Asian Nocturnal Primates (Lorisidae: Nycticebus)

In June 2007 the Asian slow lorises, genus Nycticebus, will be put forward by Cambodia at the 14th Conference of Parties to be transferred from Appendix II of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) to Appendix I. Appendix II allows trade, albeit regulated, whereas Appendix I will preclude all international commercial trade in the genus [CITES, 2007]. At present capture for trade is rampant and unregulated [Schulze and Groves, 2004]. The large volume of trade has led to the conclusion that Nycticebus species are not common enough to withstand the current level of off-take, being the number one protected species encountered during many in-country animal market surveys [Malone et al., 2002; Harris, 2003; Webber and Nekaris, 2004; Shepherd et al., 2005]. In order to qualify for listing in Appendix I of CITES, the CITES listing criteria require that the wild population is small, has a restricted area of distribution or has suffered a marked decline in the population size in the wild. Other than those from the trade, few data have been published from wild populations that can be presented to support the transfer from Appendix II to I. Until recently, slow lorises were considered a single highly polymorphic species, ranging from northern India to China and Vietnam, south to the Malay Peninsula, and into western Indonesia and the southern Philippines [Groves, 1971, 1998]. In Cambodia’s proposal [CITES, 2007], three species are listed, whereas recent and ongoing research shows that slow lorises in fact comprise a minimum of five cryptic species, differing in dentition, morphology, and genetic make-up [Roos, 2003; Brandon-Jones et al., 2004; Chen et al., 2006; Nekaris et al. , 2006]. At an IUCN Red List Primate Specialists Group Conservation Assessment and Management Plan (CAMP) in Cambodia in September 2006, these five species were individually assessed as Vulnerable or Endangered on the basis of continuing habitat loss alone. The threespecies approach can have a drastic impact on the conservation status of Nycticebus , underestimating threats in terms of habitat loss and the impacts of the trade. Before permitting exports of species listed in Appendix II of CITES, each national government within a species’ range is required to determine that trade is not detrimental to the species’ survival or to the ecosystem in which it occurs – in effect, to confirm that the species has been harvested at a sustainable level [Vonk and Published online: May 8, 2007

The trade in bear parts from Myanmar: an illustration of the ineffectiveness of enforcement of international wildlife trade regulations

We assessed the effectiveness of national and international wildlife trade regulations in Asia by surveying four wildlife markets in Myanmar for bears and bear parts. Bears are protected in Myanmar and neighbouring countries, and are included in CITES Appendix I, precluding international trade. Three of the four wildlife markets were situated at the border with neighbouring countries (China and Thailand) whereas the fourth, situated in Myanmar’s interior, also catered to international markets. During seven checks (1999–2006) we recorded 1,200 bear parts, representing a minimum of 215 individual bears. Most items were from Asiatic black bears Ursus thibetanus but also sun bear Helarctos malayanus parts were offered for sale. There were significant temporal and spatial differences in what items were offered for sale. Prices were low (USD 4–40 per item) and the total monetary value of the items for sale was USD 6,500–9,500 (not including gall bladders). Carcasses, skulls, canines, paws, claws, whole skins, pieces of skin, gall bladders and derivates, were openly displayed, with vendors being frank about prices, origin, and potential buyers. Only in the interior were prices quoted in the local currency; at the other three markets currencies of the neighbouring countries were used. Legal (international) trade in bears or bear parts from Myanmar is virtually non-existent, and the observed trade in bear parts strongly indicates a serious lack of enforcement effort. International trade in bear parts from Myanmar is significant, and open, and we conclude that the enforcement of wildlife trade regulations, at least when they concerns bear species, have by and large failed.

Decline of the endemic Hose's langur Presbytis hosei in Kayan Mentarang National Park, East Borneo

I present data on the decline of Hoses langur Presbytis hosei over a 7-year period in the Kayan Mentarang National Park in the remote northern part of East Kalimantan, Indonesia. In 1996 Hoses langurs were among the most common primates in the Nggeng Bio valley, occurring at densities of over two groups km −2 , and could be observed almost daily. A repeat census of the same area in 2003 indicated that these densities had dropped by 50–80%, and observation of the species in the valley had become a rare occurrence. During the 7-year period the forest remained in a relatively pristine condition but, despite being part of a National Park, active protection of the valley was lacking and hunting was common. From interviews with local hunters and Park staff it appeared that hunting for bezoar stones (visceral excretions found in langurs and used in traditional medicine) was the primary reason for the observed decline in Hoses langur. In 1998 a merchant calling at a nearby village had expressed an interest in the stones and guaranteed to purchase them, and this sparked excessive hunting of Hoses langur in the area, to such an extent that 3 years later this hunting was no longer economically viable. This study demonstrates that, with increasing access to markets, hunting large vertebrates for medicinal purposes, even for short periods only, can have a dramatic impact on population numbers. In such cases, habitat protection alone does not guarantee preservation, and more active protection of wildlife is required.

Population size, Red List status and conservation of the Natuna leaf monkey Presbytis natunae endemic to the island of Bunguran, Indonesia

We present the first population estimate for the Natuna leaf monkey Presbytis natunae, endemic to the island of Bunguran, Indonesia, based on a 2-month survey. Bunguran has a land area of only 1,605 km(2) and was until 1980 largely covered in primary forest. At present primary forest exists only in small patches within a matrix of logged forest, which covers nearly 70% of the island. Natuna leaf monkeys are confined to forest and have a preference for primary lowland forest patches. Groups average 3.5+/-SD 2.0 individuals and occur in a density of 2.3+/-SD 1.1 groups per km(2). Extrapolation of the density estimates to the entire island indicates that

DNA barcoding of Dutch birds

Abstract The mitochondrial cytochrome c oxidase subunit I (COI) can serve as a fast and accurate marker for the identification of animal species, and has been applied in a number of studies on birds. We here sequenced the COI gene for 387 individuals of 147 species of birds from the Netherlands, with 83 species being represented by > 2 sequences. The Netherlands occupies a small geographic area and 95% of all samples were collected within a 50 km radius from one another. The intraspecific divergences averaged 0.29% among this assemblage, but most values were lower; the interspecific divergences averaged 9.54%. In all, 95% of species were represented by a unique barcode, with 6 species of gulls and skua (Larus and Stercorarius) having at least one shared barcode. This is best explained by these species representing recent radiations with ongoing hybridization. In contrast, one species, the Lesser Whitethroat Sylvia curruca showed deep divergences, averaging 5.76% and up to 8.68% between individuals. These possibly represent two distinct taxa, S. curruca and S. blythi, both clearly separated in a haplotype network analysis. Our study adds to a growing body of DNA barcodes that have become available for birds, and shows that a DNA barcoding approach enables to identify known Dutch bird species with a very high resolution. In addition some species were flagged up for further detailed taxonomic investigation, illustrating that even in ornithologically well-known areas such as the Netherlands, more is to be learned about the birds that are present.

The Javan hawk-eagle: misconceptions about rareness and threat

The Javan hawk-eagle (Spizaetus bartelsi) is a threatened raptor endemic to the densely populated island of Java. Historically very little is known about its biology. Recent surveys showed that the population size has been underestimated in the past. The breeding population is estimated to be 137‐188 pairs with a total of 600‐900 birds and confirmed presence in 22 discrete forest blocks throughout Java. The eagles were present in isolated forest fragments as small as 3000 ha. Good dispersal abilities in juveniles, a niche width in habitat, which is broader than previously assumed, and rather opportunistic feeding behaviour are believed to mitigate the eAects of habitat fragmentation. The appointment of the eagle as a flagship species involves serious risks, as it appears to have put the species on the list of rare birds that are in great demand with malevolent aviculturists. # 2000 Elsevier Science Ltd. All rights reserved.

Primates in Fragments 10 Years Later: Once and Future Goals

In 2010, the Food and Agriculture Organization of the United Nations (FAO) estimated that 16 million hectares of forest per year were lost globally in the 1990s (FAO 2010), and approximately 12.5 million hectares/year were lost in countries with primate populations, an area just smaller than Greece or the US State of Mississippi (Chapman and Peres 2001; Chapman and Gogarten 2012). In contrast, in the last decade (2000–2010), the rate of deforestation has decreased globally by approximately 5.2 million hectares/year, and reforestation and natural expansion of forests in some countries significantly reduced the net loss of forest (FAO 2010). This may be in part due to the lack of resonance in satellite imagery between secondary and primary forest regions, particularly in the tropics. Unfortunately, the increase in forested lands has principally affected temperate regions of Europe and eastern Asia (e.g., China, Japan), but deforestation of most tropical forests has continued steadily (e.g., annual loss: 0.5 % in Africa, 1.2 % in Mesoamerica, 0.5 % in South America, 0.4 % in southeastern Asia; FAO 2011).

Declaration of the Javan hawk eagle Spizaetus bartelsi as Indonesia's National Rare Animal impedes conservation of the species

The endangered Javan hawk eagle Spizaetus bartelsi is threatened in part by the illegal pet trade. In 1993 the species was declared Indonesias National Rare/Precious Animal, by former President Soeharto. Trade in the species and keeping it as a pet are illegal. We consolidated data about the species in trade, as observed at bird markets, with private owners, in zoological gardens (to date the species has not been bred in captivity and those in zoos are all wild-caught that were formerly in trade) and wildlife rescue centres, involving at least 68 birds. The average price for the species at bird markets was USD 40 (n = 5). The number observed at bird markets appears to have increased over time. Furthermore, prior to its declaration as a National Rare/Precious Animal it was not considered in trade to be different from other large eagles. There are indications that individuals have been illegally exported to other parts of Asia. In the early 1990s no Javan hawk eagles were kept in zoos but it became in demand in the mid 1990s and now there are 11 in six zoos throughout Java. Law enforcement with respect to trade in eagles appears to be largely absent but nine Javan hawk eagles have been brought to a wildlife rescue centre on Java. Overall, the data suggest there was an increase in trade in Javan hawk eagles after it was declared the National Rare/Precious Animal. When a threatened species is put in the spotlight to highlight its conservation plight, this should be done with close cooperation between conservation NGOs and government organizations, with appropriate legislation and/or management plans to prevent overexploitation.

Seasonal variation in naturally occurring mobbing behaviour of drongos (Dicruridae) towards two avian predators

I tested the hypothesis that mobbing chiefly functions as a nest defence mechanism by studying the mobbing behaviour of two species of drongo (black drongo Dicrurus macrocercus and ashy drongo D. leucophaeus) towards two species of raptor in rain forest of western Java, Indonesia. It was predicted that firstly mobbing would occur more frequent and more intense during the drongos breeding season and secondly that it would be more frequently and more intensely directed towards the nest and egg predating black eagle Ictinaetus malayensis compared to the relatively harmless Javan hawk-eagle Spizaetus bartelsi. I found a seasonal difference in mobbing frequency and intensity in the predicted direction for the Javan hawk-eagle but not for the black eagle. Black eagles were not more frequently or more intensely mobbed than Javan hawkeagles. In the tropics, mobbing to repel a predator may be adaptive at both seasons due to the year-round residency of drongos. Furthermore, if black eagles use the frequency or intensity of mobbing as a clue to locate nests, a lack of seasonal difference in mobbing behaviour by drongos may be an evolutionary adaptive strategy.