Conservation prioritisation through genomic reconstruction of demographic histories applied to two endangered suids in the Malay Archipelago

Aim

The biodiversity of the Malay Archipelago is the product of the region's rich biogeographical history with periods of island connectivity and isolation during the Pleistocene glacial cycles. Here, the case of two endemic suid species, the Javan (Sus verrucosus) and Bawean (S. blouchi) warty pigs, was used to illustrate how biogeographic processes and recent anthropogenic pressures can shape demographic histories with significant implications for species conservation.

Location

Malay Archipelago, with focus on Bawean and Java.

Methods

We employed genome-wide single nucleotide polymorphisms from the Porcine SNP60 v2 BeadChip to assess interspecific genetic differentiation, to estimate divergence times and to perform demographic model selection.

Results

In contrast to the hypothesis of recent divergence during the last glacial maximum, S. blouchi was found to have diverged from S. verrucosus at least 166 k years ago following a founder event. The contemporary S. blouchi population was characterised by a recent bottleneck that reduced the effective population size to less than 20. The genomic assessment supports the single species status of S. blouchi, as was previously proposed based on morphometrics. The demographic history of S. verrucosus showed evidence of secondary contact with the sympatric banded pig (S. scrofa vittatus) that colonised Java 70 k years ago.

Main Conclusions

While the Javan and Bawean warty pigs have persisted throughout the Pleistocene climatic oscillations, contemporary pressures from human activities threaten their survival and immediate action should be taken to grant legal protection to both S. verrucosus and S. blouchi. This study highlighted the use of demographic history modelling using genomic data to identify evolutionary significant units and inform conservation.     

Can Camera Traps Monitor Komodo Dragons a Large Ectothermic Predator?

Camera trapping has greatly enhanced population monitoring of often cryptic and low abundance apex carnivores. Effectiveness of passive infrared camera trapping, and ultimately population monitoring, relies on temperature mediated differences between the animal and its ambient environment to ensure good camera detection. In ectothermic predators such as large varanid lizards, this criterion is presumed less certain. Here we evaluated the effectiveness of camera trapping to potentially monitor the population status of the Komodo dragon (Varanus komodoensis), an apex predator, using site occupancy approaches. We compared site-specific estimates of site occupancy and detection derived using camera traps and cage traps at 181 trapping locations established across six sites on four islands within Komodo National Park, Eastern Indonesia. Detection and site occupancy at each site were estimated using eight competing models that considered site-specific variation in occupancy (ψ)and varied detection probabilities (p) according to detection method, site and survey number using a single season site occupancy modelling approach. The most parsimonious model [ψ (site), p (site*survey); ω = 0.74] suggested that site occupancy estimates differed among sites. Detection probability varied as an interaction between site and survey number. Our results indicate that overall camera traps produced similar estimates of detection and site occupancy to cage traps, irrespective of being paired, or unpaired, with cage traps. Whilst one site showed some evidence detection was affected by trapping method detection was too low to produce an accurate occupancy estimate. Overall, as camera trapping is logistically more feasible it may provide, with further validation, an alternative method for evaluating long-term site occupancy patterns in Komodo dragons, and potentially other large reptiles, aiding conservation of this species.     

Factors affecting seasonal habitat use,and predicted range of two tropical deer in Indonesian rainforest

There is an urgent recognized need for conservation of tropical forest deer. In order to identify some environmental factors affecting conservation, we analyzed the seasonal habitat use of two Indonesian deer species, Axis kuhlii in Bawean Island and Muntiacus muntjak in south-western Java Island, in response to several physical, climatic, biological, and anthropogenic variables. Camera trapping was performed in different habitat types during both wet and dry season to record these elusive species. The highest number of photographs was recorded in secondary forest and during the dry season for both Bawean deer and red muntjac. In models, anthropogenic and climatic variables were the main predictors of habitat use. Distances to cultivated area and to settlement were the most important for A. kuhlii in the dry season. Distances to cultivated area and annual rainfall were significant for M. muntjak in both seasons. Then we modelled their predictive range using Maximum entropy modelling (Maxent). We concluded that forest landscape is the fundamental scale for deer management, and that secondary forests are potentially important landscape elements for deer conservation. Important areas for conservation were identified accounting of habitat transformation in both study areas.     

Does variation between dry and wet seasons affect tropical forest mammals' occupancy and detectability by camera traps? Case study from the Udzungwa Mountains,Tanzania

The increasing use of camera trapping coupled to occupancy analysis to study terrestrial mammals has opened the way to inferential studies that besides estimating the probability of presence explicitly consider detectability. This in turn allows considering factors that can potentially confound the estimation of occupancy and detection probability, including seasonal variations in rainfall. To address this, we conducted a systematic camera trapping survey in the Udzungwa Mountains of Tanzania by deploying twenty camera traps for 30 days in dry and wet seasons and used dynamic occupancy modelling to determine the effect of season on estimated occupancy and detection probability for species with >10 capture events. The sampling yielded 7657 and 6015 images in dry and wet seasons, respectively, belonging to 21 mammal species. Models with no season dependency and with season‐dependent detectability were best supported, indicating that neither colonization nor extinction varied with seasons and hence occupancy did not vary. Only bush pig (Potamochoerus larvatus) showed a significant decrease in detectability from dry to wet seasons. Our study indicates that seasonal variation in rainfall may have limited effect on occupancy and detectability of resident mammals in Udzungwa rainforests; however, it remains a factor to consider when designing future studies.     

Local and Regional Determinants of Colonisation-Extinction Dynamics of a Riparian Mainland-Island Root Vole Metapopulation

The role of local habitat geometry (habitat area and isolation) in predicting species distribution has become an increasingly more important issue, because habitat loss and fragmentation cause species range contraction and extinction. However, it has also become clear that other factors, in particular regional factors (environmental stochasticity and regional population dynamics), should be taken into account when predicting colonisation and extinction. In a live trapping study of a mainland-island metapopulation of the root vole (Microtus oeconomus) we found extensive occupancy dynamics across 15 riparian islands, but yet an overall balance between colonisation and extinction over 4 years. The 54 live trapping surveys conducted over 13 seasons revealed imperfect detection and proxies of population density had to be included in robust design, multi-season occupancy models to achieve unbiased rate estimates. Island colonisation probability was parsimoniously predicted by the multi-annual density fluctuations of the regional mainland population and local island habitat quality, while extinction probability was predicted by island population density and the level of the recent flooding events (the latter being the main regionalized disturbance regime in the study system). Island size and isolation had no additional predictive power and thus such local geometric habitat characteristics may be overrated as predictors of vole habitat occupancy relative to measures of local habitat quality. Our results suggest also that dynamic features of the larger region and/or the metapopulation as a whole, owing to spatially correlated environmental stochasticity and/or biotic interactions, may rule the colonisation – extinction dynamics of boreal vole metapopulations. Due to high capacities for dispersal and habitat tracking voles originating from large source populations can rapidly colonise remote and small high quality habitat patches and re-establish populations that have gone extinct due to demographic (small population size) and environmental stochasticity (e.g. extreme climate events).     

Integrating aspects of ecology and predictive modelling: implications for the conservation of the leopard cat (Prionailurus bengalensis) in the Eastern Himalaya

An understanding of species ecology is vital for effective conservation, particularly if the species forms an important constituent of the lesser mammal guild and regulates small mammal and bird populations. As the ecological role of the leopard cat (Prionailurus bengalensis) in the intricate eastern Himalayan habitats is not known, we assessed the site occupancy, detection probability and activity pattern of leopard cats in Khangchendzonga Biosphere Reserve, India, based on sign surveys and camera trapping. The estimated site occupancy was 0.352?±?0.061 and detection probability was 0.143?±?0.0484. Occupancy modelling indicated low elevation, high rodent abundance and tree cover as best predictors for the occupancy of leopard cat. Diet based on analysed scats revealed murids as the most dominant prey (89.2 %). Information based on photographic captures indicated that the leopard cat exhibited a nocturnal activity pattern (peak activity between 0200–0300 hours), which coincided with its principal prey (revealed through diet analysis), but mainly contradicted with other sympatric competitors, hence indicating a temporal partitioning of resources among them. Ecological niche factor analysis indicated that the leopard cat exhibits high global marginality (1.32) and low global tolerance (0.275). The habitat suitability map for leopard cats showed majority of the habitat as unsuitable (1,959.44 km²) and predicted only 164.54 km² areas of lower temperate forests as moderate to highly suitable. As highly suitable habitats of the leopard cat are in close proximity to villages, conflict issues are a major threat and therefore need to be addressed in conservation program for this felid.     

Population density of striped hyenas in relation to habitat in a semi-arid landscape,western India

We used camera trapping in conjunction with a spatial explicit capture–recapture model to estimate striped hyena (Hyaena hyaena) density and occupancy models to investigate factors affecting striped hyena detection probabilities in Ranthambhore Tiger Reserve (RTR), Rajasthan, India. A sampling effort of 4,450 trap days/nights over 75 days yield 68 photo captures of 21 unique striped hyenas (based on individual markings and visual identification); the estimated striped hyena density was 5.49?±?1.27 individuals/100 km². Results of our occupancy model suggested that a rugged terrain is an important factor that influences striped hyena detection probability. Correlation with striped hyena detection with human settlement provides evidence of social tolerance of striped hyena towards humans, and more occurrence of resources allowed coexistence of hyena in a human-dominated landscape. This elasticity (inhabited areas close to humans) demonstrated by striped hyenas is an exception among carnivore communities living in this semi-arid habitat.     

Factors influencing the distribution of leopard in a semiarid landscape of Western India

Previously, factors governing distribution of leopard (Panthera pardus fusca) in forest habitats of the Indian subcontinent were unknown. The present study assessed the influence of different ecogeographic variables determining the distribution of leopards in and around Sariska Tiger Reserve through MaxEnt habitat suitability model based on camera trapping method. Camera trapping was used to collect presence/absence information in the study area from December 2008 to June 2010. Information of 11 macrohabitat characteristics and variables (habitat types, prey species, Normalized Difference Vegetation Index (NDVI), elevation, livestock, village, water source, etc.) were collected along with leopard presence data. The probability of presence of leopards increased with decreasing distance to water and increasing encounter rate of peafowl (Pavo cristatus), chital (Axis axis), sambar (Rusa unicolor), and wild pig (Sus scrofa). It was found that the probability of presence of leopards increased with increasing area of Zizyphus mixed forest patches and NDVI. Results of this study showed that the probability of presence of leopards was higher in habitat types with intermediate cover, high wild prey base, and water sources. They also indicated that leopards are not always ‘generalists’ showing some degree of specialization, at least in their choice of habitat, and this information is useful for conserving leopard in human-dominated landscapes.     

Local-level determinants of wildcat occupancy in Northeast Scotland

We studied the influence of food abundance, land cover and disturbance on European wildcat (Felis silvestris silvestris Schreber, 1777) presence in Scotland. Wildcat records were collected using camera trapping, and prey data were assessed through linear transects and small mammal trapping. Surveys were carried out in three study areas in northeast Scotland. Wildcat occupancy was best predicted by a combination of food and land cover variables. This species detection was associated with higher rodent abundance and areas of higher habitat diversity encompassing patches of mixed and coniferous woodlands. Wildcat presence was negatively linked with the prevalence of dwarf shrub areas. We suggest that wildcat conservation actions at local scale should take into account the availability of feeding resources and landscape heterogeneity.     

Traditional livestock activities modify the spatial behavior of small wildcats in the high Andes

Human activities lead to declines in species’ abundance and diversity, as well as loss of habitat quality from overexploitation. The effects of livestock grazing increase on small felids are poorly understood, primarily due to the low detectability of these species. The grazing of domestic camelids, such as the llama (Lama glama) and the alpaca (Vicugna pacos), is the main traditional source of income for the inhabitants of the Andes, where the Andean cat (Leopardus jacobita) and Pampas cat (L. colocolo) are also present. In this study, we employ camera trap data to evaluate the association of llama and alpaca grazing with occupancy by the Andean and Pampas cat in Sajama National Park. In each of 36 sampling stations, we installed a camera trap, a grid of traps for rodents and two habitat transects along a gradient of intensity of livestock grazing. Occupancy models showed that negative effect of camelid abundance was stronger for the Andean cat than the Pampas cat. For both species, occupancy was also associated positively to the abundance of prey, proximity to water bodies, and vegetation. Given that livestock activity is a way of life for human populations in the Andes, we suggest that mechanisms should be implemented to compensate for the negative effects of livestock on Andean and Pampas cat populations.     

Habitat selection by two species of small mammals in the Atlantic Forest,Brazil: Comparing results from live trapping and spool-and-line tracking

Habitat selection by small mammals is usually evaluated using data from live trapping, which provides little information about the movements of individuals. Few studies used movement data or compared the results of different sampling methods to study habitat selection by these animals. We evaluated habitat selection by the rodent Nectomys squamipes and the marsupial Micoureus paraguayanus in the Atlantic Forest of Brazil using the spool-and-line technique. We also determined if percentage of captures reflected the amount of movements in each habitat. Habitat selection was determined comparing use and availability of five habitat types at two spatial scales (movement paths and movement areas) using compositional analysis, which allowed ranking of habitats according to their relative use by animals. The use of available habitat types was non-random for both species at both spatial scales. The two species had contrasting habitat affinities directly related to their particular habits, with N. squamipes using predominantly the stream habitat, and M. paraguayanus using mainly the restinga forest habitat. Patterns of habitat selection were similar at both spatial scales probably due to the small size of movement areas, which may not represent habitat use at a broader scale. For both species, live trapping and movement data provided the same ranking in habitat use, demonstrating that simple capture indices may be used to study habitat selection by these species across different habitat types.     

Estimating Species Richness and Modelling Habitat Preferences of Tropical Forest Mammals from Camera Trap Data

Medium-to-large mammals within tropical forests represent a rich and functionally diversified component of this biome; however, they continue to be threatened by hunting and habitat loss. Assessing these communities implies studying species’ richness and composition, and determining a state variable of species abundance in order to infer changes in species distribution and habitat associations. The Tropical Ecology, Assessment and Monitoring (TEAM) network fills a chronic gap in standardized data collection by implementing a systematic monitoring framework of biodiversity, including mammal communities, across several sites. In this study, we used TEAM camera trap data collected in the Udzungwa Mountains of Tanzania, an area of exceptional importance for mammal diversity, to propose an example of a baseline assessment of species’ occupancy. We used 60 camera trap locations and cumulated 1,818 camera days in 2009. Sampling yielded 10,647 images of 26 species of mammals. We estimated that a minimum of 32 species are in fact present, matching available knowledge from other sources. Estimated species richness at camera sites did not vary with a suite of habitat covariates derived from remote sensing, however the detection probability varied with functional guilds, with herbivores being more detectable than other guilds. Species-specific occupancy modelling revealed novel ecological knowledge for the 11 most detected species, highlighting patterns such as ‘montane forest dwellers’, e.g. the endemic Sanje mangabey (Cercocebus sanjei), and ‘lowland forest dwellers’, e.g. suni antelope (Neotragus moschatus). Our results show that the analysis of camera trap data with account for imperfect detection can provide a solid ecological assessment of mammal communities that can be systematically replicated across sites.     

Habitat associations of four ungulates in mountain forests of southwest China, based on camera trapping and dung counts data

The present study aimed to assess abundance indices and habitat associations of four sympatric ungulate species (alpine musk deer Moschus chrysogaster, tufted deer Elaphodus cephalophus, Chinese serow Capricornis milneedwardsii, and Chinese goral Naemorhedus griseus) in Baima Xueshan Nature Reserve of southwest China, using camera trapping and dung counts data. Camera traps were set along six dung transects in different habitats and explored habitat use of the sympatric ungulates using trapping rates. The results obtained revealed that Chinese serow showed a negative association with open canopy cover and low canopy cover. Alpine musk deer were associated with oak shrubs, oak forests and open canopy cover, while tufted deer avoided oak shrubs. Goral showed no significant associations with habitat variables. Alpine musk deer and tufted deer had considerable habitat overlap with Chinese serow. By finding a high correlation between indices, the study indicates that camera trapping may represent a valid index of relative abundance, matching results from other studies.     

Leopard (Panthera pardus) occupancy in the Chure range of Nepal

Conservation of large carnivores such as leopards requires large and interconnected habitats. Despite the wide geographic range of the leopard globally, only 17% of their habitat is within protected areas. Leopards are widely distributed in Nepal, but their population status and occupancy are poorly understood. We carried out the sign‐based leopard occupancy survey across the entire Chure range (~19,000 km²) to understand the habitat occupancy along with the covariates affecting their occupancy. Leopard signs were obtained from in 70 out of 223 grids surveyed, with a naïve leopard occupancy of 0.31. The model‐averaged leopard occupancy was estimated to be 0.5732 (SE 0.0082) with a replication‐level detection probability of 0.2554 (SE 0.1142). The top model shows the additive effect of wild boar, ruggedness, presence of livestock, and human population density positively affecting the leopard occupancy. The detection probability of leopard was higher outside the protected areas, less in the high NDVI (normalized difference vegetation index) areas, and higher in the areas with livestock presence. The presence of wild boar was strong predictor of leopard occupancy followed by the presence of livestock, ruggedness, and human population density. Leopard occupancy was higher in west Chure (0.70 ± SE 0.047) having five protected areas compared with east Chure (0.46 ± SE 0.043) with no protected areas. Protected areas and prey species had positive influence on leopard occupancy in west Chure range. Similarly in the east Chure, the leopard occupancy increased with prey, NDVI, and terrain ruggedness. Enhanced law enforcement and mass awareness activities are necessary to reduce poaching/killing of wild ungulates and leopards in the Chure range to increase leopard occupancy. In addition, maintaining the sufficient natural prey base can contribute to minimize the livestock depredation and hence decrease the human–leopard conflict in the Chure range.     

Arboreal camera trapping sheds light on seed dispersal of the world’s only epiphytic gymnosperm: Zamia pseudoparasitica

Epiphytic lifestyles have evolved independently in ecologically, morphologically, and taxonomically diverse plant species. Although this adaptation is widespread among angiosperms, it is only known to have arisen in a single gymnosperm species, Zamia pseudoparasitica (Cycadophyta). Zamia pseudoparasitica is endemic to the mountains of Western Panama, and little is known about the ecology of this unusual cycad. Here, we provide the first report of a potential seed disperser of Z. pseudoparasitica. Between late October 2019 and March 2020, we conducted arboreal camera trapping at three sites along the Talamanca Cordillera in Western Panama, yielding an accumulated survey effort of 271 camera days. Weekly direct observations were also performed using handheld binoculars at one site. Arboreal camera trapping revealed at least seven mammal species that visit this epiphytic cycad. At all three sites, the Northern olingo (Bassaricyon gabbii) was seen visiting individuals of Z. pseudoparasitica repeatedly, both while cones were closed and after they had opened. We estimated the time‐varying intensity of the visits throughout our sampling and used mixed models to compare the length of visits when cones were closed versus when they were open. Both duration and time‐varying intensity of visits increased after cones had opened and we documented Northern olingo removing and carrying away seeds. We also observed predation by the yellow‐eared toucanet (Selenidera spectabilis) which picked and destroyed mature Z. pseudoparasitica seeds. These results suggest that the Northern olingo could be an important seed dispersal agent for this rare epiphytic gymnosperm.     

Transient persistence of bobcat (Lynx rufus) occurrence throughout a human-dominated landscape

Human developments have detrimental effects on wildlife populations globally with carnivores being particularly sensitive. The bobcat (Lynx rufus) is often considered an adaptable mesocarnivore that occurs throughout varied landcover types within its wide distribution and may be less susceptible to the negative effects of development. Our objectives were to investigate the landscape occupancy dynamics of bobcats in a highly developed and densely populated region of the northeastern United States to evaluate the sensitivity of bobcat occurrence to natural and anthropogenic landscape features. We established a large-scale camera trapping survey throughout Rhode Island, USA, sampling from 2018 to 2020. Using dynamic occupancy models, we found initial site occupancy was positively influenced by the amount of forested wetland habitat, while increasing road density and shrub cover negatively influenced the probability of site colonization. Surprisingly, we found no hypothesized variables to influence site-level extirpation probability, or any seasonal effects on dynamic parameters. Lastly, we found that forest cover and road density negatively influenced the probability of detection. The probability of occupancy was high, >0.8, throughout much of the study area (49%), but we also found relatively high site transients, with the probability a site would change occurrence status from season to season at ≈0.27 in the majority of the study area (70%). Our results show that although bobcats can persist in human-dominated landscapes, they require contiguous natural areas to do so. Future expansion of road infrastructure may reduce habitat connectivity and increase road mortalities, thus jeopardizing the population.     

Evaluating the effects of landscape configuration on site occupancy and movement dynamics of odonates in Iowa

Odonates contribute highly to global biodiversity and are considered good indicators of environmental quality, but they are under-studied and quantitative information on their habitat associations is lacking. Our objective was to examine the effects of landscape configuration on site occupancy and movement dynamics of four odonate species in Iowa: Tramea onusta, Epitheca princeps, Pantala flavescens, and Calopteryx maculata. We conducted standardized visual encounter surveys for odonates at 233 public properties in Iowa from 2007 to 2011 and computed landscape variables within a 200, 600 m, and 1 km radius of each surveyed site. Using a robust design occupancy model in Program MARK, we estimated detection probability and site occupancy, site extinction, and site colonization probabilities for each species. We found few significant effects of landscape variables on site occupancy, extinction, or colonization, although landscape variables at 600 m were included in the best model for all species. Detection probability (SE) ranged from 0.30 (0.04) for Pantala flavescens to 0.49 (0.04) for Calopteryx maculata. Our study provides information to aid habitat restoration and management efforts on sites having suitable characteristics in the surrounding landscape and ultimately help conserve odonates.     

Using occupancy models to investigate space partitioning between two sympatric large predators, the jaguar and puma in central Brazil

Coexistence of sympatric species is mediated by resource partitioning. Pumas occur sympatrically with jaguars throughout most of the jaguar's range but few studies have investigated space partitioning between both species. Here, camera trapping and occupancy models accounting for imperfect detection were employed in a Bayesian framework to investigate space partitioning between the jaguar and puma in Emas National Park (ENP), central Brazil. Jaguars were estimated to occupy 54.1% and pumas 39.3% of the sample sites. Jaguar occupancy was negatively correlated with distance to water and positively correlated with the amount of dense habitat surrounding the camera trap. Puma occupancy only showed a weak negative correlation with distance to water and with jaguar presence. Both species were less often present at the same site than expected under independent distributions. Jaguars had a significantly higher detection probability at cameras on roads than at off-road locations. For pumas, detection was similar on and off-road. Results indicate that both differences in habitat use and active avoidance shape space partitioning between jaguars and pumas in ENP. Considering its size, the jaguar is likely the competitively dominant of the two species. Owing to its habitat preferences, suitable jaguar habitat outside the park is probably sparse. Consequently, the jaguar population is likely largely confined to the park, while the puma population is known to extend into ENP's surroundings.     

Temperature Impacts the Development and Survival of Common Cutworm (Spodoptera litura): Simulation and Visualization of Potential Population Growth in India under Warmer Temperatures through Life Cycle Modelling and Spatial Mapping

The common cutworm, Spodoptera litura, has become a major pest of soybean (Glycine max) throughout its Indian range. With a changing climate, there is the potential for this insect to become an increasingly severe pest in certain regions due to increased habitat suitability. To examine this possibility, we developed temperature-based phenology model for S. litura, by constructing thermal reaction norms for cohorts of single life stages, at both constant and fluctuating temperatures within the ecologically relevant range (15–38°C) for its development. Life table parameters were estimated stochastically using cohort updating and rate summation approach. The model was implemented in the geographic information system to examine the potential future pest status of S. litura using temperature change projections from SRES A₁B climate change scenario for the year 2050. The changes were visualized by means of three spatial indices demonstrating the risks for establishment, number of generations per year and pest abundance according to the temperature conditions. The results revealed that the development rate as a function of temperature increased linearly for all the immature stages of S. litura until approximately 34–36°C, after which it became non-linear. The extreme temperature of 38°C was found lethal to larval and pupal stages of S. litura wherein no development to the next stage occurred. Females could lay no eggs at the extreme low (15°C) and high (> 35°C) test temperatures, demonstrating the importance of optimum temperature in determining the suitability of climate for the mating and reproduction in S. litura. The risk mapping predicts that due to temperature increase under future climate change, much of the soybean areas in Indian states like Madhya Pradesh, Maharashtra and Rajasthan, will become suitable for S. litura establishment and increased pest activity, indicating the expansion of the suitable and favourable areas over time. This has serious implication in terms of soybean production since these areas produce approximately 95% of the total soybeans in India. As the present model results are based on temperature only, and the effects of other abiotic and biotic factors determining the pest population dynamics were excluded, it presents only the potential population growth parameters for S. litura. However, if combined with the field observations, the model results could certainly contribute to gaining insight into the field dynamics of S. litura.