The price of persistence: Small carnivore ecology within the anthropogenically-degraded Kinabatangan landscape

Habitat fragmentation and degradation by human activities, particularly agricultural development, threatens global biodiversity. This thesis presents a multifaceted evaluation of the ecology of Malay and common palm civets in the Lower Kinabatangan Floodplain (Sabah, Borneo), a patchwork forest landscape heavily fragmented by oil palm plantations. Morphometric measurements, reproductive observations, parasitic infections, blood samples for haematology and serum biochemistry analyses, and hair samples for heavy metal analysis were collected from wild civets captured between 2012 and 2018. The pioneering deployment of GPS-collars on four common palm and 17 Malay civets enabled the determination of home ranges, diurnal sleeping sites, home range overlaps, and movement behaviours. Haematological and biochemical blood profiles indicated potential anaemia, immunosuppression, and consumption of a low-protein diet in civets captured closer to oil palm plantations. Civets expressed significantly elevated liver enzyme levels relative to domestic animals. Individuals of both species used oil palm plantations for nocturnal foraging and diurnal rest sites; however, all collared individuals accessed forests. Home ranges of civets that accessed plantations were significantly larger than civets that did not, suggesting oil palm poses low habitat suitability. Civet hair concentrations of 13 heavy metals indicated detectable exposure to varying quantities of metals, with levels impacted by biological and landscape factors. Exposure to Ba, Cd, Cr, and Fe was associated with Malay civet proximity to tributaries, whilst elevated Al, Cd, and Pb concentrations were documented from GPS-collared civets using plantations. The extent of exposure scaled with the intensity of an individual’s usage of plantations. Finally, correlations between hair metal concentrations and blood parameters suggested exposure to Al, Cd, Cr, Ba, and Pb may impact civet physiology. This study represents a step change in the understanding of civet ecology, and provides novel insights into the price of carnivore persistence in degraded landscapes

First known satellite collaring of a viverrid species: preliminary performance and implications of GPS tracking Malay civets (Viverra tangalunga)

The application of advanced technologies to the study of little-known species is a necessary step in generating effective conservation strategies. Despite the biological importance of the small carnivore guild, a paucity of data exists in terms of the spatial ecology of these species, largely due to logistical constraints of large and bulky collar units. This study reports the first known satellite collaring of a viverrid, the Malay civet (Viverra tangalunga), in Sabah, Malaysian Borneo. Stationary tests of two generations of 65–70 g e-obs GmbH ‘Collar 1A’ units recorded high fix success rates and good accuracy and precision under semi-open canopy. From October 2013–August 2015, nine adult V. tangalunga were fit with e-obs collars recording hourly nocturnal GPS locations. Collars were successfully deployed for 27–187 days. Field GPS fix success varied from 22 to 88.3 %, with the study documenting a total GPS success of 58.1 % across all individuals. Despite this large in-field performance range, the quality and quantity of data collected by these units surpass that of previous VHF studies on Asian viverrids, collecting on average a 16-fold increase in locations per collaring day. The successful application of satellite technology to these little-known carnivores carries significant biological and conservation implications, and it is recommended that satellite collars are a viable technology to conduct detailed and well-designed ecological studies of Viverridae species

Physiological implications of life at the forest interface of oil palm agriculture: blood profiles of wild Malay civets (Viverra tangalunga)

Agricultural development is a major threat to global biodiversity, and effective conservation actions are crucial. Physiological repercussions of life alongside human-modified landscapes can undermine adaptable species’ health and population viability; however, baseline data are lacking for many wildlife species. We assessed the physiological status of a generalist carnivore, the Malay civet (Viverra tangalunga), persisting within an extensively human-modified system in Sabah, Malaysian Borneo. We characterized hematology and serum biochemistry panels from civets sampled across a mosaic landscape comprising tropical forest fragments and oil palm plantations. Intra-population variation in certain blood parameters were explained by expected biological drivers such as sex, age category and sampling season. Furthermore, we determined several erythrocyte measures, immune cell counts and dietary biochemistry markers significantly varied with proximity to oil palm plantation boundaries. These findings were supported by a case study, whereby blood profiles of GPS collared male civets were contrasted based on their exclusive use of forests or use of oil palm plantations. These data provide robust and valuable first insights into this species’ physiological status and suggest agricultural landscapes are impacting the persisting population

The price of persistence: Assessing the drivers and health implications of metal levels in indicator carnivores inhabiting an agriculturally fragmented landscape

Patterns and practices of agricultural expansion threaten the persistence of global biodiversity. Wildlife species surviving large-scale land use changes can be exposed to a suite of contaminants that may deleteriously impact their health. There is a paucity of data concerning the ecotoxicological impacts associated with the global palm oil (Elaeis guineensis) industry. We sampled wild Malay civets (Viverra tangalunga) across a patchwork landscape degraded by oil palm agriculture in Sabah, Malaysian Borneo. Using a non-lethal methodology, we quantified the levels of 13 essential and non-essential metals within the hair of this adaptable small carnivore. We robustly assessed the biological and environmental drivers of intrapopulation variation in measured levels. Metal concentrations were associated with civet age, weight, proximity to a tributary, and access to oxbow lakes. In a targeted case study, the hair metal profiles of 16 GPS-collared male civets with differing space use patterns were contrasted. Civets that entered oil palm plantations expressed elevated aluminium, cadmium, and lead, and lower mercury hair concentrations compared to civets that remained exclusively within the forest. Finally, we paired hair metal concentrations with 34 blood-based health markers to evaluate the possible sub-lethal physiological effects associated with varied hair metal levels. Our multi-facetted approach establishes these adaptable carnivores as indicator species within an extensively altered ecosystem, and provides critical and timely evidence for future studies

The genomes of two key bumblebee species with primitive eusocial organization

Background: The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats. Results: We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits. Conclusions: These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation

Small carnivores of the Lower Kinabatangan Wildlife Sanctuary, Sabah, Borneo, including a new locality for the otter civet Cynogale bennettii

The tropical rainforest biodiversity of Sabah, Borneo is threatened by large-scale agricultural development, logging, and increasing hunting pressures. From 2010—2015, an extensive camera-trapping study in the Lower Kinabatangan Wildlife Sanctuary (LKWS) monitored wildlife utilisation of a lowland riparian forest corridor. This effort, culminating in nearly 600,000 images, was the longest running cameratrapping study in the Sanctuary, and documented 11 small carnivore species over 24,506 trap nights. The Malay Civet Viverra tangalunga was the most frequently detected species, followed by the Malay Badger Mydaus javanensis and the Common Palm Civet Paradoxurus hermaphroditus. The survey also collected the first photographic record of an Otter Civet Cynogale bennettii in the LKWS, which represents a new locality for this little-known Southeast Asian species. Opportunistic sightings of five additional species, including the Endangered Flat-headed Cat Prionailurus planiceps, increased the total count of small carnivores persisting in the LKWS to 16. Given the highly degraded and fragmented status of the LKWS, this study highlights the importance of riparian lowland forest fragments in sustaining carnivore diversity, and also emphasizes the importance of continued, long-term monitoring efforts

Space-use patterns of Malay civets (Viverra tangalunga) persisting within a landscape fragmented by oil palm plantations

Context Agricultural land use is expanding and is a major driver of the biodiversity crisis. Land use planning initiatives seeking to optimize wildlife conservation are hindered by a lack of baseline data quantifying species’ tolerance to human-modified landscapes. Objectives We explored the influence of landscape characteristics on the fine-scale space-use patterns of a model generalist carnivore, the Malay civet (Viverra tangalunga), within degraded tropical forests and oil palm plantations. Methods We collected over 20,000 GPS locations from 21 male civets in Sabah, Malaysian Borneo to evaluate the species’ space-use patterns and habitat utilization processes. We used movement-based modeling to determine home ranges, and combined the results with high-resolution remotely sensed habitat characteristics. We developed resource utilization functions to determine individual and population-level functional responses to proximity to plantation edge, distance to water, terrain ruggedness, forest structure, and functional diversity. Results Civets foraged within oil palm plantations, yet all animals utilized forests. Home ranges scaled with proportion of plantation within both total and core ranges. Resource utilization functions reported individualism in the species’ responses to habitat characteristics. At the population-scale, civets consistently and more intensely used habitats closer to plantation edges and taller tree canopies. Conclusions Although plantations did not pose an inhospitable matrix, oil palm agriculture is a less suitable habitat than remnant forests for civets. Proximity measures and forest structure influenced the spatial behaviors of this adaptable generalist, highlighting the importance of protected areas. We recommend land-sparing and -sharing approaches to facilitate carnivore persistence across oil palm degraded landscapes

Chemical immobilization of free-ranging and captive Sunda clouded leopards (<i>Neofelis diardi</i>) with two anesthetic protocols: medetomidine-ketamine and tiletamine-zolazepam

There is currently no available information regarding the veterinary management of Sunda clouded leopards (Neofelis diardi), either in captivity or in the wild. In this study, 12 Sunda clouded leopards were anesthetized between January 2008 and February 2014 for medical exams, and/or GPS-collaring. Seven wild-caught individuals were kept in captivity and 5 free-ranging animals were captured by cage traps. Two anesthesia combinations were used: medetomidine-ketamine (M-K) or tiletamine-zolazepam (T-Z). Atipamezole (0.2 mg/kg im) was used as an antagonist for medetomidine. Medetomidine (range: 0.039-0.054 mg/kg) and ketamine (range: 3-4.39 mg/kg) were administered during 5 immobilizations, resulting in median induction times of 7 min. After a median anesthesia time of 56 min, atipamezole was injected, observing effects of antagonism at a median time of 12 min. T-Z (range: 6.8-10.8 mg/kg) was administered on 7 occasions. Median induction times observed with this combination were shorter than with M-K (4 min vs 7 min; P=0.04), and anesthesia and recovery times were significantly longer (244 and 35 min vs 56 and 16 min, respectively; P=0.02). Lower heart rates were measured in the M-K group, while lower rectal temperatures were found in the T-Z group. Both combinations resulted in safe and reliable immobilizations, although given the favorable anesthesia and recovery times of M-K, we recommend this approach over T-Z for the veterinary handling of Sunda clouded leopards