Survey of practitioners handling slow lorises (Primates: Nycticebus): an assessment of the harmful effects of slow loris bites

Slow lorises (Nycticebus spp.) are one of six venomous mammals, and the only known venomous primate. In the wild envenomation occurs mainly during conspecific competition for mates and territory, but may also be used as an application against parasites or for predator defense. Envenomation in humans is documented, with the most extreme accounts detailing near-fatal anaphylactic shock. From September 2016 – August 2017, we received questionnaire responses from 80 wild animal practitioners working with Nycticebus spp. in zoos, rescue centres and in the wild. We identified 54 practitioners who had experience of being bitten or were otherwise affected by slow loris venom, and an additional 26 incomplete entries. No fatalities were reported. Fifteen respondents noted that medical intervention was required, 12 respondents indicated no reaction to being bitten (9 of these indicated they were wearing gloves). Symptoms for those affected included: anaphylactic shock, paraesthesia, haematuria, dyspnoea, extreme pain, infection and general malaise. Impact of slow loris bites ranged from instantaneous to long-persisting complications, and healing time ranged from 1 day to >8 months. Extremities, including hands and arms, were mostly affected from the bites. Six of nine species of slow loris were reported to bite, with N. pygmaeus being the most common in our sample. We make suggestions regarding the use of these highly threatened yet dangerous primates as unsuitable tourist photo props and zoo animal ambassadors. We discuss the medical complications experienced in relation to protein sensitisation, and bacterial pathogenesis. We recommend future work to ascertain the protein content of slow loris venom to aid in enabling mitigation of risks posed

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

Risky business: The function of play in a venomous mammal, the Javan slow loris (Nycticebus javanicus)

Immature mammals require opportunities to develop skills that will affect their competitive abilities and reproductive success as adults. One way these benefits may be achieved is through play behavior. While skills in developing use of tusks, antlers, and other weapons mammals have been linked to play, play in venomous animals has rarely been studied. Javan slow lorises (Nycticebus javanicus) use venom to aid in intraspecific competition, yet whether individuals use any behavioral mechanisms to develop the ability to use venom remains unclear. From April 2012 to December 2020, we recorded 663 play events and studied the factors influencing the frequency of play and the postures used during play in wild Javan slow lorises. Regardless of the presence of siblings, two thirds of play partners of young slow lorises were older and more experienced adults. Young lorises engaged in riskier behaviors during play, including using more strenuous postures and playing more in riskier conditions with increased rain and moonlight. We found that play patterns in immature lorises bear resemblance to venom postures used by adults. We suggest that play functions to train immature lorises to deal with future unexpected events, such as random attacks, as seen in other mammalian taxa with weapons. Given the importance of venom use for highly territorial slow lorises throughout their adult lives and the similarities between venom and play postures, we cannot rule out the possibility that play also prepares animals for future venomous fights. We provide here a baseline for the further exploration of the development of this unique behavior in one of the few venomous mammals

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

Slow lorises use venom as a weapon in intraspecific competition

Animals have evolved an array of spectacular weapons, including antlers, forceps, proboscises, stingers, tusks and horns [ 1 ]. Weapons can be present in males and females of species needing to defend critical limiting resources, including food (rhinoceros beetles, Trypoxylus) and territories (fang blennies, Meiacanthus) [ 1 , 2 , 3 ]. Chemicals, including sprays, ointments and injected venoms, are another defence system used by animals. As with morphological weapons, venom can serve multiple purposes, including to facilitate feeding, in predation, and in defence when attacked [ 4 ]. Although rare, several taxa use venom for agonistic intraspecific competition (e.g. ghost shrimp, Caprella spp.; sea anemones, Actinia equina; cone snails, Conidae; male platypus, Ornithorhynchus anatinus) [ 4 , 5 , 6 ]. Another group of venomous mammals are the nocturnal slow lorises ( Nycticebus) [ 7 ]. Slow loris bites often result in dramatic diagnostic wounds characterised by necrotic gashes to the head and extremities. Although these bites are the major cause of death of lorises in captivity, the function of this aggressive behaviour has never been studied in the wild [ 7 ]. Here, through an 8-year study of wounding patterns, territorial behaviour, and agonistic encounters of a wild population of Javan slow lorises ( Nycticebus javanicus), we provide strong evidence that venom is used differentially by both sexes to defend territories and mates

Conservation implications of primate trade in China over 18 years based on web news reports of confiscations

Primate species have been increasingly threatened by legal and illegal trade in China, mainly for biomedical research or as pets and traditional medicine, yet most reports on trade from China regard international trade. To assess a proxy for amount of national primate trades, we quantified the number of reports of native primate species featuring in unique web news reports from 2000 to 2017, including accuracy of their identification, location where they were confiscated or rescued, and their condition upon rescue. To measure temporal trends across these categories, the time span was divided into three sections: 2000–2005, 2006–2011 and 2012–2017. A total of 735 individuals of 14 species were reported in 372 news reports, mostly rhesus macaques (n = 165, 22.5%, Macaca mulatta) and two species of slow lorises (n = 487, 66.3%, Nycticebus spp.). During the same period, live individuals of rhesus macaques were recorded 206 times (70,949 individuals) in the Convention on International Trade in Endangered Species of Wild Fauna and Flora Trade Database, whereas slow lorises were only recorded four times (nine individuals), indicating that the species originated illegally from China or were illegally imported into China. Due to their rescued locations in residential areas (n = 211, 56.7%), most primates appeared to be housed privately as pets. A higher proportion of ‘market’ rescues during 2006–2011 (χ2 = 8.485, df = 2, p = 0.014), could be partly attributed to an intensive management on wildlife markets since the outbreak of severe acute respiratory syndrome (SARS) in 2003. More than half (68.3%, 502 individuals) of the primate individuals were unhealthy, injured or dead when rescued. Thus, identification and welfare training and capacity-building should be provided to husbandry and veterinary professionals, as well as education to the public through awareness initiatives. The increase in presence of some species, especially slow lorises, with a declining population in restricted areas, also suggests the urgent need for public awareness about the illegal nature of keeping these taxa as pets

From international to local: Promoting local volunteer tourism to guarantee the persistence of wildlife conservation projects in the post-COVID-19 era

Volunteer tourists, often foreigners, collect essential data in wildlife conservation projects worldwide. Due to the COVID-19 pandemic, international tourism activities reduced drastically, forcing many conservation projects to shut down. Using a nine-year (2013–2021) case study in Indonesia, we examine how local and foreign tourists construct the meaning of their volunteer experiences in the light of COVID-19. We aim to highlight the potential benefits of local volunteer tourism to face the travel limitations posed by COVID-19, and to show an example of how conservation projects can overcome the challenges of the current and potential future pandemics. We recruited 117 volunteers (49 Indonesians, 68 foreign; 73 females, 44 males; mean age: 24.2 ± SD 4.7) that collected 50.8% of the total amount of data collected by the project over the same period. Of the 117 volunteers, 81 of them (38 Indonesians, 43 foreigners) filled in a feedback form at the end of their stay. Via logistic regressions, we found that Indonesian volunteers declared more positive feedback on the logistics at the research station (p = 0.047). Via Bayesian structural equation models, we found that Indonesian volunteers reported significantly more frequently than foreign volunteers that they learned new skills (89% Credible Interval = 0.017–0.351) and that they gained personal wisdom, growth and maturity (89% Credible Interval = 0.891–1.003) from the volunteer experience. The volunteer program evolved from being 100% foreign volunteers in 2013 to 100% Indonesian volunteers by 2020 at the peak of the pandemic, which helped maintain the continuity of the research and conservation activities. We presented the positive implications of shifting towards local volunteer tourists in a long-term conservation project. We suggest that promoting local volunteer tourism through training new generations of nationals in conservation projects is key to guarantee the persistence of such initiatives in the post-COVID-19 Era

Conservation implications of primate trade in China over 18 years based on web news reports of confiscations

Primate species have been increasingly threatened by legal and illegal trade in China, mainly for biomedical research or as pets and traditional medicine, yet most reports on trade from China regard international trade. To assess a proxy for amount of national primate trades, we quantified the number of reports of native primate species featuring in unique web news reports from 2000 to 2017, including accuracy of their identification, location where they were confiscated or rescued, and their condition upon rescue. To measure temporal trends across these categories, the time span was divided into three sections: 2000–2005, 2006–2011 and 2012–2017. A total of 735 individuals of 14 species were reported in 372 news reports, mostly rhesus macaques (n = 165, 22.5%, Macaca mulatta) and two species of slow lorises (n = 487, 66.3%, Nycticebus spp.). During the same period, live individuals of rhesus macaques were recorded 206 times (70,949 individuals) in the Convention on International Trade in Endangered Species of Wild Fauna and Flora Trade Database, whereas slow lorises were only recorded four times (nine individuals), indicating that the species originated illegally from China or were illegally imported into China. Due to their rescued locations in residential areas (n = 211, 56.7%), most primates appeared to be housed privately as pets. A higher proportion of ‘market’ rescues during 2006–2011 (w2 = 8.485, df = 2, p = 0.014), could be partly attributed to an intensive management on wildlife markets since the outbreak of severe acute respiratory syndrome (SARS) in 2003. More than half (68.3%, 502 individuals) of the primate individuals were unhealthy, injured or dead when rescued. Thus, identification and welfare training and capacity-building should be provided to husbandry and veterinary professionals, as well as education to the public through awareness initiatives. The increase in presence of some species, especially slow lorises, with a declining population in restricted areas, also suggests the urgent need for public awareness about the illegal nature of keeping these taxa as pets

Large-scale trade in a songbird that is extinct in the wild

Indonesia is at the epicenter of the Asian Songbird Crisis, i.e., the recognition that the cage bird trade has a devastating impact on numerous imperiled bird species in Asia. The Javan pied starling Gracupica jalla, only in the last five years recognized as distinct from the pied starlings of mainland Southeast Asia, has been declared extinct the wild in 2021. Up until the 1980s, it used to be one of the most common open countryside birds on the islands of Java and Bali, Indonesia. From the early 2000s onwards, the species is commercially bred to meet the demand from the domestic cagebird trade. We conducted 280 market surveys in 25 bird markets in Java and Bali between April 2014 and March 2020, with 15 markets being surveyed at least six times. We recorded 24,358 Javan pied starlings, making it one of the most commonly observed birds in the markets. We established that, conservatively, around 40% of the birds in the market were sold within one week and used this to estimate that at a minimum ~80,000 Javan pied starlings are sold in the bird markets on Java and Bali. The latter represents a monetary value of USD5.2 million. We showed that prices were low in the 1980s, when all birds were sourced from the wild. It became more varied and differentiated in the 2000s when a combination of now expensive wild-caught and cheaper captive-bred birds were offered for sale, and prices stabilized in the 2010s when most, if not all birds were commercially captive-bred. Javan pied starlings are not protected under Indonesian law, and there are no linked-up conservation efforts in place to re-establish a wild population on the islands, although small-scale releases do take place

Global online trade in primates for pets

The trade in primates as pets is a global enterprise and as access to the Internet has increased, so too has the trade of live primates online. While quantifying primate trade in physical markets is relatively straightforward, limited insights have been made into trade via the Internet. Here we followed a three-pronged approach to estimate the prevalence and ease of purchasing primates online in countries with different socioeconomic characteristics. We first conducted a literature review, in which we found that Malaysia, Thailand, the USA, Ukraine, South Africa, and Russia stood out in terms of the number of primate individuals being offered for sale as pets in the online trade. Then, we assessed the perceived ease of purchasing pet primates online in 77 countries, for which we found a positive relationship with the Internet Penetration Rate, total human population and Human Development Index, but not to Gross Domestic Product per capita or corruption levels of the countries. Using these results, we then predicted the levels of online primate trade in countries for which we did not have first-hand data. From this we created a global map of potential prevalence of primate trade online. Finally, we analysed price data of the two primate taxa most consistently offered for sale, marmosets and capuchins. We found that prices increased with the ease of purchasing primates online and the Gross Domestic Product per capita. This overview provides insight into the nature and intricacies of the online primate pet trade and advocates for increased trade regulation and monitoring in both primate range and non-range countries where trade has been substantially reported. © 2023 The Author