The Harry Potter effect: The rise in trade of owls as pets in Java and Bali, Indonesia

Hundreds of species of wild-caught birds are offered for sale in the bird markets of Java and Bali, Indonesia, to meet the demand for the largely-domestic pet and songbird trade. In the past, owls were offered only in very small numbers in these bird markets but since the release of the Harry Potter series in Indonesia in the early 2000s their popularity as pets has increased. Whereas in the past owls were collective known as Burung Hantu (“Ghost birds”), in the bird markets they are now commonly referred to as Burung Harry Potter (“Harry Potter birds”). We made a retrospective quantitative assessment of the abundance of owls in the bird markets (1979–2010) and conducted 109 surveys in 20 bird markets in 2012–2016 to quantify owls in trade. In the 1980s, 1990s and early 2000s owls were rarely recorded in Indonesia's bird markets, typically one or two and up to five per survey, and frequently no owls were recorded at all. The trade was largely confined to small scops owls. In the late 2000s more species were offered for sale, including barn and bay owls, and larger owl species such as wood-owls, eagle-owls and fish-owls; typically 10 + owls were observed per survey. In recent years, the number of owl species increased even more, and on average we recorded 17 owls per survey, yielding a total of 1810 owls, and in >90% of the surveys owls were present. In the larger bird markets in Jakarta and Bandung typically 30 to 60 owls are on offer of up to 8 species at a time. The number of owls as a proportion of all birds in the markets increased from 0.43% post 2008, suggesting a delayed Harry Potter effect. Over this period, common species have become cheaper and less common ones have become more expensive. The owls are largely, if not exclusively, wild-caught and are sold into the domestic pet market. The release of Harry Potter films and novels in Indonesia coincided with the rise of the Internet and social media and, with some delay, the emergence of pet owl interest groups on Java and Bali, thus preventing us to demonstrate a causal Harry Potter effect on the owl trade. The overall popularity of owls as pets in Indonesia has risen to such an extent that it may imperil the conservation of some of the less abundant species. Inclusion of owls on Indonesia's protected species list, alongside all diurnal raptors, may be a first step to mitigate the negative effects of this emerging trend

Vertical clingers and gougers: rapid acquisition of adult limb proportions facilitates feeding behaviours in young Javan slow lorises (Nycticebus javanicus)

Animals of all ages need to access essential food resources, either on their own or with the assistance of conspecifics. Rapid physical and behavioural development is one strategy to help young animals reach adulthood. Specialized gum-feeding mammals exploit a food type that is relatively difficult to access and digest and must possess the appropriate adaptions to access large vertical substrates, i.e. tree trunks. Unlike other gum feeding mammals, the Javan slow loris (Nycticebus javanicus) lacks physical structures, such as keeled nails or claws, which animals commonly use to secure themselves to large vertical substrates. To understand how slow lorises of all ages exploit gum, we examined their vertical gouging posture, locomotor behaviour, habitat use during feeding, and their morphometric measures across three age classes (adult, sub-adult, juvenile). Using data collected in Cipaganti, Java, Indonesia between April 2012 and April 2016, we found that individuals of N. javanicus rely on their hand, foot, and limb morphology to maintain vertical gouging postures, in place of claws or keeled nails. Locomotor behaviour, position in tree, and tree DBH showed no significant difference across age classes while feeding. Juveniles were indistinguishable from adults and sub-adults in regards to limb proportion indices, lower leg length, hand span and foot span. Some morphometric measures scaled isometrically e.g. arm length, but those highlighted during prolonged vertical postures scaled allometrically e.g. leg, hand, and foot measures. These findings suggest that the rapid behavioural and physical development of key features may act as an ontogenetic adaptation to facilitate access to a stable food resource at a young age. The Javan slow loris exemplifies the complex relationship that exists between an animal’s diet and the specializations that facilitate access to these food resources

Do chemical cues in the venom of slow lorises repel avian predators?

Raptors are confirmed predators of Asian slow lorises (Nycticebus spp.), the only primates with a toxic bite. A possible function of this venom is to protect against predators. Slow lorises release volatile chemicals when threatened, thus potentially communicating their venomous status towards predators. Crested Serpent-eagles (Spilornis cheela) and Changeable Hawk-eagles (Nisaetus cirrhatus) are known to prey on venomous snakes and small mammals and are potential predators of slow lorises. We tested the anti-predator potential of slow loris venom by presenting pieces of chicken combined with swabs of Greater Slow Loris (Nycticebus coucang) venom to 10 Changeable Hawk-eagles and 5 Crested Serpent-eagles. The eagles showed few behavioural responses in reaction to slow loris venom, examining swabs with venom or control scents equally. Both eagle species did show higher rates of face-rubbing behaviour following consumption of foods paired with venom compared with control scents. Our data suggest that slow loris venom does not function to repel avian predators, but may have an anti-predator defence function. While the eagles are not repelled by the smell of slow lorises, contact with their venom causes discomfort, potentially limiting the palatability of slow lorises to eagles

Exploiting a readily available but hard to digest resource: A review of exudativorous mammals identified thus far and how they cope in captivity

Gum is a widely available carbohydrate, composed mainly of non-digestible structural carbohydrates. No mammalian enzymes can digest gum, therefore a mammal ingesting gum must rely on microbial fermentation in order to access the energy it possesses. Gums are known as relatively nutrient poor. Despite this, some mammals have evolved to exploit this food resource. We aim to review the literature for all mammal species which have been recorded to ingest gum, whether quantified or not and discuss this in context of their evolutionary adaptations. We also investigated the recommended captive diets for these species to look at if gum is recommended. We conducted a literature search on ISI Web of Knowledge to tabulate all mammal species observed ingesting gum and classify them as obligate, facultative or opportunistic feeders. We encountered 94 mammal species which eat gum in the wild (26 obligate feeders, 35 facultative feeders and 33 opportunistic feeders). Obligate feeders have entirely evolved to exploit this resource but were found to not be given gum in captivity, which may explain why they are failing to thrive, as opposed to facultative feeders which have fewer issues. Gum may be necessary for the health of obligate feeders in captivity. Future research should focus on the physiological effects that gum ingestion poses on different digestive systems

Trialling nutrient recommendations for slow lorises (Nycticebus spp.) based on wild feeding ecology

Slow loris (Nycticebus spp.) captive diets have been based on routine and anecdotes rather than scientific fact. The growing body of evidence contradicts the high fruit diet supported by such anecdotes. Non-human primate nutrient requirements are grouped into new (based on the common marmoset Callithrix jacchus) or old world (based on rhesus macaques Macaca mulatta) primates. Slow lorises are known to suffer from many health ailments in captivity such as dental disease, obesity, wasting and kidney issues all of which have been linked to diet. This study aimed to estimate nutrient intake from free-ranging slow lorises and to determine whether this intake can be used as nutrient recommendations. We collected data of nutrient intake, food passage rate and digestibility of captive slow lorises on three diet treatments 1: current captive type diet which is mostly fruits, 2: wild-type diet made only of food items from their natural diet, 3: new diet made to reflect wild slow loris nutrient intake. In order to validate our nutrient recommendations, diets 2 and 3 would have to be significantly different to Diet 1 in terms of nutrients, but not different from each other. Captive diets were significantly higher in soluble carbohydrates and lower in minerals and fibre fractions than both diets 2 and 3. Diets 2 and 3 led to a significantly increased food passage time and to more effective fibre and calcium digestion compared to Diet 1. We also observed obese individuals lost weight and underweight individuals gained weight. Our nutrient recommendations have been validated by our trials, and new or old world monkey nutrient recommendations are not consistent with our results. Diets should be high in protein and fibre and low in soluble carbohydrates and fats

Slow lorises (Nycticebus spp.) really are slow: A study into food passage rates

The characteristics of food ingested by a primate affect its assimilation of energy by modulating food passage rate. In general, digestive time increases in folivorous primates and decreases in frugivorous primates when they are fed higher fibre diets but this relationship is understudied in exudativorous primates. We compared the food passage rate of five slow loris species. We studied 34 wild-caught slow lorises (15 Nycticebus coucang, 15 N. javanicus, and four N. menegensis) in an Indonesian rescue centre and four captive-born slow lorises (two N. bengalensis and two N. pygmaeus) in a UK institution. We fed the Indonesian animals two different diets: a captive-type diet comprising fruits, vegetables and insects, and a wild-type diet formulated to be similar in nutrients to that consumed by slow lorises in the wild, consisting of gum, insects, vegetables and nectar. We fed the UK animals a diet of gum, vegetables, insects and hard-boiled eggs. We formulated this diet to mimic the wild diet, with notably higher fibre fractions and lower soluble sugars than the previous diet. We measured two variables: the transit time (TT) and the mean retention time (MRT). We mixed 1 tsp of glitter in bananas or gum as our markers and fed them to the slow lorises immediately prior to their main diet. We noted the date and time of feeding and of appearances of the marker in faeces. We weighed food given and left over for each animal to calculate ingested foods and nutrients. We found that TTs were not affected by diet treatment but MRTs were significantly longer for all species fed the wild type diet. Our results show that Nycticebus spp. have long MRTs for their body weight, and N. pygmaeus may have the slowest MRT of all primates in relation to body mass. The digestive flexibility of exudativorous primates should allow them to maximise fermentation opportunities when they ingest more (appropriate) fibre by increasing the amount of time the fibre substrate stays in the large intestine. Exudativorous primates appear to have plastic digestive strategies that may be an adaptation to cope with relatively nutrient-poor staple food sources such as gum. The provision of gum in a captive setting may therefore provide benefits for gut health in slow lorises

Checkerboard Patterns, Interspecific Competition, and Extinction: Lessons from Distribution Patterns of Tarsiers (Tarsius) and Slow Lorises (Nycticebus) in Insular Southeast Asia

Tarsiers (Tarsius) and slow lorises (Nycticebus) are the only extant nocturnal primates occurring in Southeast Asia. Harcourt (1999) hypothesized that in insular Southeast Asia, slow lorises and tarsiers showed a checkerboard distribution on 12 small (<12,000 km2) islands, i.e., only one or the other occurs, and attributed this to extreme levels of competition between these 2 largely faunivorous primates. Further, he predicted slow lorises were able to persist on smaller islands than tarsiers. We re-evaluated these findings using an expanded dataset including 49 islands where tarsiers or slow lorises occur. Tarsiers and slow lorises live on islands of similar size (median size of ca. 300–900 km2), and both taxa inhabit an equal proportion of small, medium, and large islands. On small islands within their area of sympatry tarsiers occur on 1 island, slow lorises on 8, both genera on 3, and we can assume they have become extinct from 11 small islands since the Last Glacial Maximum. Sizes of islands where tarsiers or slow lorises have become extinct do not differ from islands where they are still extant. We show that slow lorises occur on more islands in insular Southeast Asia than perhaps previously assumed, but these islands are not smaller on average than islands where tarsiers occur. A checkerboard distribution between these taxa is not evident. More studies are needed at the macroecological level to assess the importance of biogeographic history in explaining their present-day distribution patterns

Coexistence between Javan Slow Lorises (Nycticebus javanicus) and humans in a dynamic agroforestry landscape in West Java, Indonesia

In a world increasingly dominated by human demand for agricultural products, we need to understand wildlife’s ability to survive in agricultural environments. We studied the interaction between humans and Javan slow lorises (Nycticebus javanicus) in Cipaganti, Java, Indonesia. After its introduction in 2013, chayote (Sechium edule), a gourd grown on bamboo lattice frames, became an important cash crop. To evaluate people’s use of this crop and to measure the effect of this increase on slow loris behavior, home ranges, and sleep sites, we conducted interviews with local farmers and analysed the above variables in relation to chayote expansion between 2011 and 2015. Interviews with farmers in 2011, 2013, and 2015 confirm the importance of chayote and of bamboo and slow lorises in their agricultural practices. In 2015 chayote frames covered 12% of land in Cipaganti, occupying 4% of slow loris home ranges, which marginally yet insignificantly increased in size with the increase in chayote. Slow lorises are arboreal and the bamboo frames increased connectivity within their ranges. Of the sleep sites we monitored from 2013 to 2016, 24 had disappeared, and 201 continued to be used by the slow lorises and processed by local people. The fast growth rate of bamboo, and the recognition of the value of bamboo by farmers, allow persistence of slow loris sleep sites. Overall introduction of chayote did not result in conflict between farmers and slow lorises, and once constructed the chayote bamboo frames proved to be beneficial for slow lorises

Hiding from the Moonlight: Luminosity and Temperature Affect Activity of Asian Nocturnal Primates in a Highly Seasonal Forest

The effect of moonlight and temperature on activity of slow lorises was previously little known and this knowledge might be useful for understanding many aspects of their behavioural ecology, and developing strategies to monitor and protect populations. In this study we aimed to determine if the activity of the pygmy loris (Nycticebus pygmaeus) is affected by ambient temperature and/or moonlight in a mixed deciduous forest. We radio-collared five females and five males in the Seima Protection Forest, Cambodia, in February to May, 2008 and January to March, 2009 and recorded their behaviour at 5 minutes intervals, totalling 2736 observations. We classified each observation as either inactive (sleeping or alert) or active behaviour (travel, feeding, grooming, or others). Moon luminosity (bright/dark) and ambient temperature were recorded for each observation. The response variable, activity, was binary (active or inactive), and a logit link function was used. Ambient temperature alone did not significantly affect mean activity. Although mean activity was significantly affected by moonlight, the interaction between moonlight and temperature was also significant: on bright nights, studied animals were increasingly more active with higher temperature; and on dark nights they were consistently active regardless of temperature. The most plausible explanation is that on bright cold nights the combined risk of being seen and attacked by predators and heat loss outweigh the benefit of active behaviours

Remarkable Ancient Divergences Amongst Neglected Lorisiform Primates

Lorisiform primates (Primates: Strepsirrhini: Lorisiformes) represent almost 10% of the living primate species and are widely distributed in sub-Saharan Africa and South/South-East Asia; however, their taxonomy, evolutionary history, and biogeography are still poorly understood. In this study we report the largest molecular phylogeny in terms of the number of represented taxa. We sequenced the complete mitochondrial cytochrome b gene for 86 lorisiform specimens, including ∼80% of all the species currently recognized. Our results support the monophyly of the Galagidae, but a common ancestry of the Lorisinae and Perodicticinae (family Lorisidae) was not recovered. These three lineages have early origins, with the Galagidae and the Lorisinae diverging in the Oligocene at about 30 Mya and the Perodicticinae emerging in the early Miocene. Our mitochondrial phylogeny agrees with recent studies based on nuclear data, and supports Euoticus as the oldest galagid lineage and the polyphyletic status of Galagoides. Moreover, we have elucidated phylogenetic relationships for several species never included before in a molecular phylogeny. The results obtained in this study suggest that lorisiform diversity remains substantially underestimated and that previously unnoticed cryptic diversity might be present within many lineages, thus urgently requiring a comprehensive taxonomic revision of this primate group