Resource-use and recursion by a mega-herbivore Elephas maximus borneensis

This thesis examines the ecology of elephants (Elephas maximus borneensis) that inhabit the Lower Kinabatangan region of Sabah, Malaysia. My research focused on improving our understanding of their habitat use and food-plant preference over varying spatial and temporal scales, and tested recursion hypotheses. Recursion, the reuse of sites or plants over time, has rarely been explored in wild animals. Studies of recursion promote understanding of species ecology as they explore temporal variation in resource-use. Recursion by herbivores may be a foraging strategy for optimising resource-use by returning to sites to coincide with plant recovery. A review of the recursion literature revealed that previous studies had not considered recursion that leads from foraging theory; this informed the research and the design of the chapters on recursion at two spatial scales – site and plant. The review also demonstrated the need to integrate the large amount of research on recursion-like processes with the new research topic of recursion. Such processes include site reuse associated with spatial memory, resource recovery and foraging site-fidelity. The scarcity of studies of these topics in large, wild herbivores was also evident. I chose to investigate recursion ecology in the Bornean elephant because this provided an opportunity to test hypotheses for repeated resource-use, and to improve our understanding of resource ecology for a mega-herbivore. I expected recursion to occur less frequently in elephants compared with smaller herbivores. Mega-herbivores have a reduced requirement for high quality food. They should also consume more resources per visit, resulting in more time needed for resources to recover and therefore less frequent recursions. However, elephants have a more highly developed spatio-temporal memory than other herbivores and therefore may have greater ability to return more often to profitable foraging sites and plants. To investigate elephant habitat use I first characterised the habitat types in the Lower Kinabatangan Wildlife Sanctuary (LKWS) based on their floristic composition and physical characteristics. Elephant habitat-use was measured using indirect observations of feed sign along ten 1 km long and 4 m wide strip-transects randomly placed throughout the LKWS. Elephants exhibited a strong preference for open grass areas along forest margins and avoided swamps and recently logged or cultivated habitat. Two of the most common habitats, lowland mixed dipterocarp and semi-inundated forest, were neither selected nor avoided. The habitat types identified and their use by elephants underpinned the subsequent chapters on recursion and elephant food-plant preferences. I investigated recursion to foraging sites using GPS collars to track the two main elephant herds in the LKWS in order to examine their behaviour and sample sites. Recursion was common, occurring at 48 of 87 foraging sites, within 48 hours and between 151-250 days. This indicated that elephant foraging strategies involve site sampling and timing of returns to coincide with some periodicity in site quality. I also found that recursion occurred if the site had previously been occupied for longer periods than sites receiving no recursions. The number of days that had passed between the first visit and recursion was also positively correlated with time spent at the recursion site. Sites that received most recursions were within the elephants’ preferred habitat; that is, open grass areas along forest margins. These findings indicate that recursion occurs for the repeated exploitation of higher quality foraging sites and is perhaps timed for the recovery of their food plants. The hypothesis that plant recovery rates influence recursion periodicity had not been tested previously in wild populations. The growth of new shoots on plants from 30 species that were previously selected for feeding by elephants were measured each month for 9 months, or until they were re-browsed by elephants, to learn if plant recovery rates influence recursion time. Recursion to grasses was found to coincide with full recovery but the elephants prematurely browsed other plant types. This suggests that elephant foraging strategies influence vegetation community structuring and may maintain or enhance grass patches. My results from Chapters 3-5 demonstrate recursion at two spatial scales, site and plant, and indicate that the elephants forage optimally in their preferred habitat. It was also necessary to understand the proportion of grass and browse in the elephant diet and what influences the selection of browse species. Food-plant use and availability analyses found that contrary to what was expected of a generalist herbivore, plants were not selected by elephants in proportion to their availability. The finding that grasses form a major and highly preferred part of Bornean elephant diet was unexpected because they had been regarded as a forest-feeding species. One hundred and eighty-two plants were eaten and 185 plants from 18 species were measured for species availability along 12 transects. I identified a preference for grass rather than browse species despite grasses being less abundant, confirming the importance of grass and grass patches – two spatial scales – to elephants in the LKWS. Previous work has implicated the size and vigour of plants as important in herbivore food-plant selection. I found that elephant browse preferences were not influenced by plant vigour and plant size. Bornean elephant foraging strategies are therefore primarily focussed on the optimum harvesting of grass in discrete patches within the forest and the riparian zone. To manage this population of elephants it is important to understand their relationship with their food resources. My study has contributed in this regard in ways that are of general importance to understanding elephants and other mega-herbivores, as well as in ways that are of specific importance to the conservation of Bornean elephants in the LKWS. Firstly, in order to meet the elephant population’s dietary needs, access to open grass areas must be maintained. Forest rehabilitation projects should incorporate these areas as part of their landscape management strategy. For example, corridors should be designed and placed to assist the movement of elephants amongst preferred grassy foraging sites. Secondly, this study provides scientific support for effective ways to identify profitable foraging areas for wild herbivores across a variety of landscapes. Studies of recursion and the characters of sites and plants that receive repeated visits provide more direct and rapid ways of identifying what is important to herbivore populations. Moreover, if the elephant, the largest land mammal and herbivore, is so elaborately and concurrently recursive at different spatial and temporal scales, then recursion is likely to be widespread amongst other herbivores. I therefore recommend further examination of recursion behaviour across a wider range of wild herbivores. Advances in our understanding of herbivore ecology and our ability to conserve and manage wildlife habitat will require a direct refocus on repeated resource-use and will depend on redesigning studies to consider the scales at which recursion occurs

Foraging site recursion by forest elephants Elephas maximus borneensis

Recursion by herbivores is the repeated use of the same site or plants. Recursion by wild animals is rarely investigated but may be ubiquitous. Optimal foraging theory predicts site recursion as a function of the quality of the site, extent of its last use, and time since its last use because these influence site resource status and recovery. We used GPS collars, behaviour and site sampling to investigate recursion to foraging sites for two elephant Elephas maximus borneensis herds in the Lower Kinabatangan Wildlife Sanctuary, Borneo, over a 12 month period. Recursion occurred to 48 out of 87 foraging sites and was most common within 48 hours or between 151–250 days, indicating two different types of recursion. Recursion was more likely to occur if the site had previously been occupied for longer. Moreover, the time spent at a site at recursion was the same as the time spent at the site on the first occasion. The number of days that had passed between the first visit and recursion was also positively correlated with how much time was spent at the site at recursion. Habitat type also influenced the intensity of site-use, with more time spent at recursion within riverine/open grass areas along forest margins compared to other habitat types. Recursion is a common behaviour used by the elephants and its pattern suggests it may be a foraging strategy for revisiting areas of greater value. The qualities of recursion sites might usefully be incorporated into landscape management strategies for elephant conservation in the are

Understanding the spatial distribution and hot spots of collared Bornean elephants in a multi-use landscape

Abstract: In the Kinabatangan floodplain, Sabah, Malaysian Borneo, oil palm and settlements have reduced and fragmented lowland tropical forests, home to around 200 endangered Bornean elephants (Elephas maximus borneensis). In this region, elephants range within forests, oil palm and community areas. The degree to which elephants are using these areas remains unclear. We used GPS telemetry data from 2010 to 2020 for 14 collared elephants to map their entire known ranges and highly used areas (hot spots) across four land use categories and estimate time spent within these. The use of land use types across elephants varied significantly. Typically, females had strong fidelity to forests, yet many of these forests are threatened with conversion. For the three males, and several females, they heavily used oil palm estates, and this may be due to decreased landscape permeability or foraging opportunities. At the pooled level, the entire range and hot spot extents, constituted 37% and 34% for protected areas, respectively, 8% and 11% for unprotected forests, 53% and 51% for oil palm estates, and 2% for community areas. Protecting all forested habitats and effectively managing areas outside of protected areas is necessary for the long-term survival of this population

Environmental predictability as a cause and consequence of animal movement

The impacts of environmental predictability on the ecology and evolution of animal movement have been the subject of vigorous speculation for several decades. Recently, the swell of new biologging technologies has further stimulated their investigation. This advancing research frontier, however, still lacks conceptual unification and has so far focused little on converse effects. Populations of moving animals have ubiquitous effects on processes such as nutrient cycling and seed dispersal and may therefore shape patterns of environmental predictability. Here, we synthesise the main strands of the literature on the feedbacks between environmental predictability and animal movement and discuss how they may react to anthropogenic disruption, leading to unexpected threats for wildlife and the environment

Behaviour and spatial ecology of the Bornean elephant (Elephas maximus borneensis) in Lower Kinabatangan, Sabah, Malaysia Borneo

The Bornean subspecies of Asian elephant (Elephas maximus borneensis) is mainly restricted to Sabah, Malaysia and the survival of these elephants in the wild is being jeopardized primarily through a combination of habitat loss, conflicts with people and low genetic diversity. Lower Kinabatangan Floodplain (LKF) which holds between 200 and 250 elephants is isolated from the other populations in Sabah and highly vulnerable to both anthropogenic and non-anthropogenic pressures such as climate change and further encroachments to their natural habitat. Solutions to these challenges require information on the factors affecting the movement and behaviour of the species. This thesis examines the behavioural and spatial ecology of the Bornean elephant in the Lower Kinabatangan region of Sabah, in Malaysian Borneo. Elephants were monitored visually, and to facilitate remote-monitoring of movement, six female elephants were fitted with satellite collars during the flooding and non-flooding seasons of 2011-2012 (n=3 individuals) and 2013-2014 (n=3 individuals) respectively. In Chapter 2, the seasonal variations in spatial utilization distribution were quantified using analytical methods such as dynamic Brownian Bridge Movement modelling (dBBMM) and Classification and Regression Tree (CART). This analysis showed that the size of utilization distribution (UD) varied significantly between individuals and seasonally. In both seasons, the elephants were observed to maintain their UD close to the river. In the flooding season elephants were less selective about their space use and were more predictable in their movements than in the non-flooding season and were more mobile in higher elevation and good quality habitats. In the non-flooding season, the utilization distribution of elephants was larger and mostly determined by anthropogenic factors such as roads. The core home range areas of elephants in both seasons mostly reflected the need to satisfy their dietary and water requirements. In Chapter 3, Brownian motion variance generated from the elephants’ movement data was used as a measure of behavioural state relating to motion, to describe the behaviour of the elephants (Chapter 3). Human activities and environmental features were used to explain the changes of motion variance and speed in a fragmented landscape. The data were analysed using generalized additive mixed model (GAMMs). This analysis revealed that elephant movement dynamics and speed show significant temporal (diurnal and seasonal) and spatial (between habitat) variation. Finally, in Chapter 4, I carried out the first longitudinal analysis of the activity budget of adult female elephants in the oil palm plantations, freshwater swamp and riparian habitats adjoining the Kinabatangan River, in order to understand how elephant behaviours vary in relation to habitat, time of day, season and group size. We used generalised additive mixed models (GAMMs) to examine how the behaviours of 40 individually-identified adult female elephants (primarily feeding, moving, resting, bathing, social interactions, and vigilance) varied in relation to time of the day, season and group size, in the major habitat types within this landscape. Elephants primarily fed in the morning and evening, and rested in the middle of the day. In oil palm plantations, elephants were observed to associate in smaller groups, and to feed less feed and to socialize less, and to be more restless, vigilant and mobile compared to riparian habitats. A similar comparison between semi swamp and riparian forest showed significantly higher feeding and vigilance behaviour in freshwater swamp forest but no significant difference in resting and moving. Our results show that riparian and seasonal freshwater swamp habitats play an important role as a social arena for the Bornean elephants in LKF, as well as providing food resources and connectivity for movement of elephants across this landscape that is increasingly fragmented by oil palm plantations and other human infrastructure such as roads and bridges. Chapter 5 summarises the main findings of this thesis and the implications for the conservation of the Bornean elephant at the local, national and global scale. These findings together comprise the most detailed account to date of the behaviour and spatial ecology of wild Bornean elephants, and will be used to inform conservation policy (e.g. maintaining connectivity between patches of natural habitat types) and mitigation of human-elephant conflict (e.g. through an improved understanding of daily and seasonal variation in behaviour, and behavioural differences between habitats)

Asian elephants as ecological filters in Sundaic forests

Megaherbivores exert strong top-down influence on the ecosystems they inhabit, yet little is known about the foraging impacts of Asian elephants (Elephas maximus) on the structure of Southeast Asia’s rainforests. Our goal was to document Asian elephants’ dietary composition, selectivity, and foraging impacts in a Sundaic rainforest and test whether these differed between habitats. We conducted controlled direct observations of five wild-born captive elephants feeding on six plant types (bamboo, grass, monocot herbs, palms, lianas, and trees) of different age 2 in two habitats (mature vs. early successional forest) in Krau, Peninsular Malaysia. Palms, trees, and lianas formed the bulk of the elephants’ diet. In the mature forest, elephants showed a strong preference for monocots (preference ratio, PR = 5.1), particularly large palms (PR = 5.4), while trees were negatively selected (PR = 0.14). Conversely, in early successional habitats, large tree saplings were positively selected (PR = 1.6). Elephants uprooted (30%) and broke the main stem (30%) of the dicot trees, mainly large saplings, that they handled. Tree saplings broken by elephants had an average diameter of 1.7 ± 1.1 cm (up to 7 cm), with breaks happening at 1.1 ± 0.5 m of height. We estimated that, in a year, an elephant could damage (i.e., either uproot or break) around 39,000 tree saplings if it fed entirely in mature forest, and almost double the number (73,000) if it fed solely in early successional habitats. Assuming a density of 0.05–0.18 elephants/km2, elephant foraging could damage 0.2–0.6% of the tree sapling population per year. Slow growth rates of understory plants in mature forests could result in negative feedbacks, whereby elephants suppress palms, other monocots, and highly preferred tree species. Alternatively, elephants may initiate positive feedbacks by impeding succession along forest edges and in semi-open environments, thereby increasing the size of gaps and the availability of their preferred foodplants. Overall, our results show that Asian elephants act as ecological filters by suppressing the plants they prefer in Southeast Asia’s rainforests

Determining the diet of wild Asian elephants (Elephas maximus) at human–elephant conflict areas in Peninsular Malaysia using DNA metabarcoding

Human–elephant conflict (HEC) contributes to the increasing death of Asian elephants due to road accidents, retaliatory killings and fatal infections from being trapped in snares. Understanding the diet of elephants throughout Peninsular Malaysia remains crucial to improve their habitat quality and reduce scenarios of HEC. DNA metabarcoding allows investigating the diet of animals without direct observation, especially in risky conflict areas. The aim of this study was to determine: i) the diet of wild Asian elephants from HEC areas in Peninsular Malaysia using DNA metabarcoding and ii) the influence of distinct environmental parameters at HEC locations on their feeding patterns. DNA was extracted from 39 faecal samples and pooled into 12 groups representing the different sample locations: Kuala Koh, Kenyir, Ulu Muda, Sira Batu, Kupang-Grik, Bumbun Tahan, Belum-Temengor, Grik, Kampung Pagi, Kampung Kuala Balah, Aring 10 and the National Elephant Conservation Centre, which served as a positive control for this study. DNA amplification and sequencing targeted the ribulose-bisphosphate carboxylase gene using the next-generation sequencing Illumina iSeq100 platform. Overall, we identified 35 orders, 88 families, 196 genera and 237 species of plants in the diet of the Asian elephants at HEC hotspots. Ficus (Moraceae), Curcuma (Zingiberaceae), Phoenix (Arecaceae), Maackia (Fabaceae), Garcinia (Clusiaceae) and Dichapetalum (Dichapetalaceae) were the highly abundant dietary plants. The plants successfully identified in this study could be used by the Department of Wildlife and National Parks (PERHILITAN) to create buffer zones by planting the recommended dietary plants around HEC locations and trails of elephants within Central Forest Spine (CFS) landscape

Habitat use and movement of proboscis monkeys (Nasalis larvatus) in a degraded and human-modified forest landscape

Proboscis monkeys (Nasalis larvatus) are endemic to Borneo and live in habitats threatened by land clearance for agriculture, aquaculture and timber. This thesis examines the roles of structural and landscape characteristics on both short- and long-term habitat use through the first application of GPS tags to proboscis monkeys. In a comparison of four home range estimators, biased random bridges provided the best home range estimates given the GPS-collar dataset and landscape characteristics (Chapter 3). Differences in long-term ranging patterns of 10 individuals across a range of forest-block sizes and disturbance levels were examined, as well as daily and seasonal variation in movement and sleeping site selection. Using Light Detection and Ranging (LiDAR) structural metrics of the forest, as well as landscape characteristics, forest with taller canopies, forests in close proximity to river edges were found to be of particular importance to proboscis monkeys, and plantation edges were avoided (Chapter 4). Changes in daily and monthly movements were associated with seasonal changes in rainfall and potential food availability. Movement patterns also changed near forest edges, with faster, more direct movements near agricultural boundaries. Less rainfall, higher temperatures and brighter moon phases correlated with selection of sleeping sites in the forest interior (Chapter 5). By understanding the ranging requirements of proboscis monkeys, drone and GPS collar data were combined to inform conservation policy (Chapter 6). This thesis provides the most in-depth examination of proboscis monkey ecology to date. They appeared more generalist in their home range use and structural habitat requirements than previously realised, suggesting a higher degree of versatility and resilience to habitat loss and degradation. This study provides increased understanding of potential consequences of human-mediated disturbances and can be used to assist in the protection of this charismatic species and the management of degraded landscapes