Using the multivariate Hawkes process to study interactions between multiple species from camera trap data.

Interspecific interactions can influence species' activity and movement patterns. In particular, species may avoid or attract each other through reactive responses in space and/or time. However, data and methods to study such reactive interactions have remained scarce and were generally limited to two interacting species. At this time, the deployment of camera traps opens new opportunities but adapted statistical techniques are still required to analyze interaction patterns with such data. We present the multivariate Hawkes process (MHP) and show how it can be used to analyze interactions between several species using camera trap data. Hawkes processes use flexible pairwise interaction functions, allowing us to consider asymmetries and variations over time when depicting reactive temporal interactions. After describing the theoretical foundations of the MHP, we outline how its framework can be used to study interspecific interactions with camera trap data. We design a simulation study to evaluate the performance of the MHP and of another existing method to infer interactions from camera trap-like data. We also use the MHP to infer reactive interactions from real camera trap data for five species from South African savannas (impala Aepyceros melampus, greater kudu Tragelaphus strepsiceros, lion Panthera leo, blue wildebeest Connochaetes taurinus and Burchell's zebra Equus quagga burchelli). The simulation study shows that the MHP can be used as a tool to benchmark other methods of interspecific interaction inference and that this model can reliably infer interactions when enough data are considered. The analysis of real data highlights evidence of predator avoidance by prey and herbivore-herbivore attraction. Lastly, we present the advantages and limits of the MHP and discuss how it can be improved to infer attraction/avoidance patterns more reliably. As camera traps are increasingly used, the multivariate Hawkes process provides a promising framework to decipher the complexity of interactions structuring ecological communities.

Impact of artificial waterholes on temporal partitioning in a carnivore guild: a comparison of activity patterns at artificial waterholes to roads and trails.

Temporal partitioning in large carnivores have previously been found to be one of the main factors enabling co-existence. While activity patterns have been investigated separately at artificial waterholes and e.g., game trails, simultaneous comparative analyses of activity patterns at artificial waterholes and game trails have not been attempted. In this study, camera trap data from Maremani Nature Reserve was used to investigate whether temporal partitioning existed in a carnivore guild of four species (spotted hyena, leopard, brown hyena and African wild dog). Specifically, we investigated temporal partitioning at artificial waterholes and on roads and trails an average of 1,412 m away from an artificial waterhole. Activity patterns for the same species at artificial waterholes and roads/game trails were also compared. We found no significant differences in temporal activity between species at artificial waterholes. Temporal partitioning on game trails and roads was only found between spotted hyena (nocturnal) and African wild dog (crepuscular). Between nocturnal species (spotted hyena and leopard) no temporal partitioning was exhibited. Only African wild dog exhibited significantly different activity patterns at waterholes and roads/game trails. This indicates artificial waterholes may be a location for conflict in a carnivore guild. Our study highlights the impact of anthropogenic landscape changes and management decisions on the temporal axis of carnivores. More data on activity patterns at natural water sources such as ephemeral pans are needed to properly assess the effect of artificial waterholes on temporal partitioning in a carnivore guild.

Context-dependency in carnivore co-occurrence across a multi-use conservation landscape.

Carnivore intraguild dynamics depend on a complex interplay of environmental affinities and interspecific interactions. Context-dependency is commonly expected with varying suites of interacting species and environmental conditions but seldom empirically described. In South Africa, decentralized approaches to conservation and the resulting multi-tenure conservation landscapes have markedly altered the environmental stage that shapes the structure of local carnivore assemblages. We explored assemblage-wide patterns of carnivore spatial (residual occupancy probability) and temporal (diel activity overlap) co-occurrence across three adjacent wildlife-oriented management contexts-a provincial protected area, a private ecotourism reserve, and commercial game ranches. We found that carnivores were generally distributed independently across space, but existing spatial dependencies were context-specific. Spatial overlap was most common in the protected area, where species occur at higher relative abundances, and in game ranches, where predator persecution presumably narrows the scope for spatial asymmetries. In the private reserve, spatial co-occurrence patterns were more heterogeneous but did not follow a dominance hierarchy associated with higher apex predator densities. Pair-specific variability suggests that subordinate carnivores may alternate between pre-emptive behavioral strategies and fine-scale co-occurrence with dominant competitors. Consistency in species-pairs diel activity asynchrony suggested that temporal overlap patterns in our study areas mostly depend on species' endogenous clock rather than the local context. Collectively, our research highlights the complexity and context-dependency of guild-level implications of current management and conservation paradigms; specifically, the unheeded potential for interventions to influence the local network of carnivore interactions with unknown population-level and cascading effects.

Broad aggressive interactions among African carnivores suggest intraguild killing is driven by more than competition.

Theory on intraguild killing (IGK) is central to mammalian carnivore community ecology and top-down ecosystem regulation. Yet, the cryptic nature of IGK hinders empirical evaluations. Using a novel data source - online photographs of interspecific aggression between African carnivores - we revisited existing predictions about the extent and drivers of IGK. Compared with seminal reviews, our constructed IGK network yielded 10 more species and nearly twice as many interactions. The extent of interactions increased 37% when considering intraguild aggression (direct attack) as a precursor of killing events. We show that IGK occurs over a wider range of body-mass ratios than predicted by standing competition-based views, with highly asymmetrical interactions being pervasive. Evidence that large species, particularly hypercarnivore felids, target sympatric carnivores with a wide range of body sizes suggests that current IGK theory is incomplete, underestimating alternative competition pathways and the role of predatory and incidental killing. Our findings reinforce the potential for IGK-mediated cascades in species-rich assemblages and community-wide suppressive effects of large carnivores.

Patterns and Drivers of Rodent Abundance across a South African Multi-Use Landscape.

South Africa's decentralized approach to conservation entails that wildlife outside formally protected areas inhabit complex multi-use landscapes, where private wildlife business (ecotourism and/or hunting) co-exist in a human-dominated landscape matrix. Under decentralized conservation, wildlife is perceived to benefit from increased amount of available habitat, however it is crucial to understand how distinct management priorities and associated landscape modifications impact noncharismatic taxa, such as small mammals. We conducted extensive ink-tracking-tunnel surveys to estimate heterogeneity in rodent distribution and investigate the effect of different environmental factors on abundance patterns of two size-based rodent groups (small- and medium-sized species), across three adjacent management contexts in NE KwaZulu-Natal, South Africa: a private ecotourism game reserve, mixed farms and traditional communal areas (consisting of small clusters of houses interspersed with grazing areas and seminatural vegetation). Our hypotheses were formulated regarding the (1) area typology, (2) vegetation structure, (3) ungulate pressure and (4) human disturbance. Using a boosted-regression-tree approach, we found considerable differences between rodent groups' abundance and distribution, and the underlying environmental factors. The mean relative abundance of medium-sized species did not differ across the three management contexts, but small species mean relative abundance was higher in the game reserves, confirming an influence of the area typology on their abundance. Variation in rodent relative abundance was negatively correlated with human disturbance and ungulate presence. Rodent abundance seems to be influenced by environmental gradients that are directly linked to varying management priorities across land uses, meaning that these communities might not benefit uniformly by the increased amount of habitat promoted by the commercial wildlife industry.

Surveillance of the rabies-related lyssavirus, Mokola in non-volant small mammals in South Africa.

The reservoir host of Mokola virus (MOKV), a rabies-related lyssavirus species endemic to Africa, remains unknown. Only sporadic cases of MOKV have been reported since its first discovery in the late 1960s, which subsequently gave rise to various reservoir host hypotheses. One particular hypothesis focusing on non-volant small mammals (e.g. shrews, sengis and rodents) is buttressed by previous MOKV isolations from shrews (Crocidura sp.) and a single rodent (Lophuromys sikapusi). Although these cases were only once-off detections, it provided evidence of the first known lyssavirus species has an association with non-volant small mammals. To investigate further, retrospective surveillance was conducted in 575 small mammals collected from South Africa. Nucleic acid surveillance using a pan-lyssavirus quantitative real-time reverse transcription polymerase chain reaction (qRT-PCR) assay of 329 brain samples did not detect any lyssavirus ribonucleic acid (RNA). Serological surveillance using a micro-neutralisation test of 246 serum samples identified 36 serum samples that were positive for the presence of MOKV neutralising antibodies (VNAs). These serum samples were all collected from Gerbilliscus leucogaster (Bushveld gerbils) rodents from Meletse in Limpopo province (South Africa). Mokola virus infections in Limpopo province have never been reported before, and the high MOKV seropositivity of 87.80% in these gerbils may indicate a potential rodent reservoir.

Viral Prevalence in Wild Serval Population is Driven by Season and Sex.

One of the key factors influencing the population dynamics of threatened species such as felids is disease, but long-term studies of the factors influencing seroprevalence of wild felids are extremely rare, hindering conservation efforts. We set out to determine seroprevalence of six viral diseases (feline panleukopenia virus, feline leukemia virus, feline coronavirus, feline calicivirus, feline herpes virus, and feline immunodeficiency virus) among a population of serval (Leptailurus serval) with an extremely high density in South Africa. We captured 55 individuals over four years and screened blood samples for antibodies to each virus. We found that seroprevalence were high (ranging from 30.0% positive for a single virus to 1.8% positive for up to five viruses) and that seroprevalence was influenced by season and sex, but not body condition. We suggest further monitoring of this population and recommend that long-term studies are conducted for serval and other felids to determine whether these trends are representative on a broader scale.

Mesocarnivore community structuring in the presence of Africa's apex predator.

Apex predator reintroductions have proliferated across southern Africa, yet their ecological effects and proposed umbrella benefits of associated management lack empirical evaluations. Despite a rich theory on top-down ecosystem regulation via mesopredator suppression, a knowledge gap exists relating to the influence of lions (Panthera leo) over Africa's diverse mesocarnivore (less than 20 kg) communities. We investigate how geographical variation in mesocarnivore community richness and occupancy across South African reserves is associated with the presence of lions. An interesting duality emerged: lion reserves held more mesocarnivore-rich communities, yet mesocarnivore occupancy rates and evenness-weighted diversity were lower in the presence of lions. Human population density in the reserve surroundings had a similarly ubiquitous negative effect on mesocarnivore occupancy. The positive association between species richness and lion presence corroborated the umbrella species concept but translated into small differences in community size. Distributional contractions of mesocarnivore species within lion reserves, and potentially corresponding numerical reductions, suggest within-community mesopredator suppression by lions, probably as a result of lethal encounters and responses to a landscape of fear. Our findings offer empirical support for the theoretical understanding of processes underpinning carnivore community assembly and are of conservation relevance under current large-predator orientated management and conservation paradigms.

Molecular screening indicates high prevalence and mixed infections of Hepatozoon parasites in wild felines from South Africa.

Genetic diversity within partial 18S rRNA sequences from Hepatozoon protozoan parasites from wild felines in South Africa was assessed and compared with data from domestic cats to assess patterns of host specificity. Lions, leopards, servals, a caracal and an African wildcat were all positive for parasites of the Hepatozoon felis-complex. However, haplotypes were not species-specific, and potential mixed infections were widespread. Additional genetic markers are needed to untangle the extremely complex situation of these parasites in both domestic cats and wild felines in South Africa.

Comparative assessment on rodent impacts and cultural perceptions of ecologically based rodent management in 3 Afro-Malagasy farming regions.

Rodents generate negative consequences for smallholder farmers in Africa that directly impact household and livestock damage, food security, and public health. Ecologically Based Rodent Management (EBRM) seeks sustainable solutions for the mitigation of rodent damage through assessments of rodent population dynamics, agro-ecosystems, and socio-cultural contexts. We adopt a comparative approach across 3 rural Afro-Malagasy smallholder farming regions in South Africa, Tanzania, and Madagascar to assess the household impacts of rodent pests and current perceptions and preferences associated with several rodent control measures. We conducted focus group questionnaires and interviews in different study site locations. Rodents assert multiple impacts on Afro-Malagasy farmers demonstrating recurrent and emerging agricultural and household costs, and public health impacts. We identify a significant knowledge gap in educating communities about the application of different EBRM approaches in favor of acute poisons that are perceived to be more effective. Cultural issues and taboos also have a significant impact on the social acceptance of rodent hunting as well as biological control using indigenous predators. We advocate for an enhanced investigation of the socio-cultural beliefs associated with different rodent practices to understand the factors underlying social acceptance. A collaborative approach that integrates the perspectives of target communities to inform the design of EBRM initiatives according to the specific agro-ecosystem and socio-cultural context is necessary to ensure programmatic success.

Adapting Methodology Used on Captive Subjects for Estimating Gut Passage Time in Wild Monkeys.

Gut passage time of food has consequences for primate digestive strategies, which subsequently affect seed dispersal. Seed dispersal models are critical in understanding plant population and community dynamics through estimation of seed dispersal distances, combining movement data with gut passage times. Thus, developing methods to collect in situ data on gut passage time are of great importance. Here we present a first attempt to develop an in situ study of gut passage time in an arboreal forest guenon, the samango monkey (Cercopithecus albogularis schwarzi) in the Soutpansberg Mountains, South Africa. Cercopithecus spp. consume large proportions of fruit and are important seed dispersers. However, previous studies on gut passage times have been conducted only on captive Cercopithecusspp. subjects, where movement is restricted, and diets are generally dissimilar to those observed in the wild. Using artificial digestive markers, we targeted provisioning of a male and a female samango monkey 4 times over 3 and 4 days, respectively. We followed the focal subjects from dawn until dusk following each feeding event, collecting faecal samples and recording the date and time of deposition and the number of markers found in each faecal sample. We recovered 6.61 ± 4 and 13 ± 9% of markers from the male and the female, respectively, and were able to estimate a gut passage window of 16.63-25.12 h from 3 of the 8 trials. We discuss methodological issues to help future researchers to develop in situ studies on gut passage times.

Using road patrol data to identify factors associated with carnivore roadkill counts.

As the global road network expands, roads pose an emerging threat to wildlife populations. One way in which roads can affect wildlife is wildlife-vehicle collisions, which can be a significant cause of mortality through roadkill. In order to successfully mitigate these problems, it is vital to understand the factors that can explain the distribution of roadkill. Collecting the data required to enable this can be expensive and time consuming, but there is significant potential in partnering with organisations that conduct existing road patrols to obtain the necessary data. We assessed the feasibility of using roadkill data collected daily between 2014 and 2017 by road patrol staff from a private road agency on a 410 km length of the N3 road in South Africa. We modelled the relationship between a set of environmental and anthropogenic variables on the number of roadkill carcasses, using serval (Leptailurus serval) as a model species. We recorded 5.24 serval roadkill carcasses/100 km/year. The number of carcasses was related to season, the amount of wetland, and NDVI, but was not related to any of the anthropogenic variables we included. This suggests that roadkill patterns may differ greatly depending on the ecology of species of interest, but targeting mitigation measures where roads pass through wetlands may help to reduce serval roadkill. Partnering with road agencies for data collection offers powerful opportunities to identify factors related to roadkill distribution and reduce the threats posed by roads to wildlife.

High carnivore population density highlights the conservation value of industrialised sites.

As the environment becomes increasingly altered by human development, the importance of understanding the ways in which wildlife interact with modified landscapes is becoming clear. Areas such as industrial sites are sometimes presumed to have little conservation value, but many of these sites have areas of less disturbed habitats around their core infrastructure, which could provide ideal conditions to support some species, such as mesocarnivores. We conducted the first assessments of the density of serval (Leptailurus serval) at the Secunda Synfuels Operations plant, South Africa, using camera trap surveys analysed within a spatially explicit capture recapture framework. We show that servals occurred at densities of 76.20-101.21 animals per 100 km², which are higher than previously recorded densities for this species, presumably due to high abundance of prey and the absence of persecution and/or competitor species. Our findings highlight the significant conservation potential of industrialised sites, and we suggest that such sites could help contribute towards meeting conservation goals.

Diversity of haemoprotozoan parasites infecting the wildlife of South Africa.

Tissue samples from wildlife from South Africa were opportunistically collected and screened for haemoprotozoan parasites using nonspecific PCR primers. Samples of 127 individuals were tested, comprising over 50 different species. Haemogregarines were the most commonly identified parasites, but sarcocystids and piroplasmids were also detected. Phylogenetic analyses estimated from the 18S rDNA marker highlighted the occurrence of several novel parasite forms and the detection of parasites in novel hosts. Phylogenetic relationships, which have been recently reviewed, appear to be much more complex than previously considered. Our study highlights the high diversity of parasites circulating in wildlife in this biodiverse region, and the need for further studies to resolve taxonomic issues.

Camera trap and questionnaire dataset on ecosystem services provided by small carnivores in agro-ecosystems in South Africa.

This dataset includes data derived from camera trap surveys and questionnaire surveys relating to small carnivores in agro-ecosystems in the Vhembe Biosphere Reserve, South Africa. The data were collected as part of the study "Predation by small mammalian carnivores in rural agro-ecosystems: An undervalued ecosystem service?" (Williams et al., 2017a) [1]. Camera trap locations were stratified by land use: settlement, crops, and grazing areas. The camera trap data provide an insight into the ecology of the nine species of small carnivores that were recorded: striped polecat (Ictonyx striatus), honey badger (Mellivora capensis), large-spotted genet (Genetta maculata), African civet (Civettictis civetta), slender mongoose (Galerella sanguinea), Meller's mongoose (Rhynchogale melleri), Selous' mongoose (Paracynictis selousi), white tailed mongoose (Ichneumia albicauda), and dwarf mongoose (Helogale parvula). We also recorded domesticated animals such as domestic cats (Felis catus), domestic dogs (Canis lupus familiaris), and cattle (Bos taurus) on the camera traps. The questionnaire data are comprised of responses of stakeholders to questions regarding the impacts of these species on rural farming communities. In the accompanying data repository hosted on Figshare (doi 10.6084/m9.figshare.4750807, (Williams et al., 2017b) [2]) we provide raw data, along with processed data and R code used to analyse these data to determine the impact of land use and domestic animals on the species richness and occupancy of small carnivores in rural agro-ecosystems (Williams et al., 2017a) [1].

Animal taxa contrast in their scale-dependent responses to land use change in rural Africa.

Human-dominated landscapes comprise the bulk of the world's terrestrial surface and Africa is predicted to experience the largest relative increase over the next century. A multi-scale approach is required to identify processes that maintain diversity in these landscapes. Here we identify scales at which animal diversity responds by partitioning regional diversity in a rural African agro-ecosystem between one temporal and four spatial scales. Human land use practices are the main driver of diversity in all seven animal assemblages considered, with medium sized mammals and birds most affected. Even the least affected taxa, bats and non-volant small mammals (rodents), responded with increased abundance in settlements and agricultural sites respectively. Regional turnover was important to invertebrate taxa and their response to human land use was intermediate between that of the vertebrate extremes. Local scale (< 300 m) heterogeneity was the next most important level for all taxa, highlighting the importance of fine scale processes for the maintenance of biodiversity. Identifying the triggers of these changes within the context of functional landscapes would provide the context for the long-term sustainability of these rapidly changing landscapes.

The Occurrence of Some Nonblood Protozoan Parasites in Wild and Domestic Mammals in South Africa.

Relatively little is known about protozoan parasites in African animals. Here we investigated the occurrence of protozoan parasites in mammals from South Africa. Oocysts of protozoan parasites were detected in 13 of 56 (23%) fecal samples using conventional microscopic examination methods. Cryptosporidium spp. and Cystoisospora spp. were detected in eight (14%) and five (9%) samples, respectively. Mixed parasitic infection of Cryptosporidium spp. and Cystoisospora spp. was recorded in banded mongoose ( Mungos mungo). Cryptosporidium spp. was detected for the first time in cheetah ( Acinonyx jubatus), spotted hyena ( Crocuta crocuta), and African polecat ( Ictonyx striatus). Antibodies to Toxoplasma gondii and Neospora caninum were not detected by enzyme-linked immunosorbent assay in any of 32 sera tested. We detected T. gondii by PCR in tissues of five of 243 (2%) animals: domestic dog ( Canis lupus familiaris), gerbil ( Gerbilliscus spp.), greater kudu ( Tragelaphus strepsiceros), honey badger ( Mellivora capensis), and white-tailed mongoose ( Ichneumia albicauda). Our isolation of T. gondii from white-tailed mongoose and honey badger was a unique finding. All tissue samples were negative for N. caninum. The study increases our knowledge on the occurrence of protozoan parasites in populations of wild and domestic animals in South Africa.

Correction: A systematic review of rodent pest research in Afro-Malagasy small-holder farming systems: Are we asking the right questions?

[This corrects the article DOI: 10.1371/journal.pone.0174554.].

A systematic review of rodent pest research in Afro-Malagasy small-holder farming systems: Are we asking the right questions?

Rodent pests are especially problematic in terms of agriculture and public health since they can inflict considerable economic damage associated with their abundance, diversity, generalist feeding habits and high reproductive rates. To quantify rodent pest impacts and identify trends in rodent pest research impacting on small-holder agriculture in the Afro-Malagasy region we did a systematic review of research outputs from 1910 to 2015, by developing an a priori defined set of criteria to allow for replication of the review process. We followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines. We reviewed 162 publications, and while rodent pest research was spatially distributed across Africa (32 countries, including Madagascar), there was a disparity in number of studies per country with research biased towards four countries (Tanzania [25%], Nigeria [9%], Ethiopia [9%], Kenya [8%]) accounting for 51% of all rodent pest research in the Afro-Malagasy region. There was a disparity in the research themes addressed by Tanzanian publications compared to publications from the rest of the Afro-Malagasy region where research in Tanzania had a much more applied focus (50%) compared to a more basic research approach (92%) in the rest of the Afro-Malagasy region. We found that pest rodents have a significant negative effect on the Afro-Malagasy small-holder farming communities. Crop losses varied between cropping stages, storage and crops and the highest losses occurred during early cropping stages (46% median loss during seedling stage) and the mature stage (15% median loss). There was a scarcity of studies investigating the effectiveness of various management actions on rodent pest damage and population abundance. Our analysis highlights that there are inadequate empirical studies focused on developing sustainable control methods for rodent pests and rodent pests in the Africa-Malagasy context is generally ignored as a research topic.

Functional Responses of Retaliatory Killing versus Recreational Sport Hunting of Leopards in South Africa.

Predation strategies in response to altering prey abundances can dramatically influence the demographic effects of predation. Despite this, predation strategies of humans are rarely incorporated into quantitative assessments of the demographic impacts of humans killing carnivores. This scarcity largely seems to be caused by a lack of data. In this study, we contrasted predation strategies exhibited by people involved in retaliatory killing and recreational sport hunting of leopards (Panthera pardus) in the Waterberg District Municipality, South Africa. We predicted a specialist predation strategy exemplified by a type II functional response for retaliatory killing, and a generalist strategy exemplified by a type III functional response for recreational sport hunting. We could not distinguish between a type I, a type II, or a type III functional response for retaliatory killing, but the most parsimonious model for recreational sport hunting corresponded to a type I functional response. Kill rates were consistently higher for retaliatory killing than for recreational sport hunting. Our results indicate that retaliatory killing of leopards may have severe demographic consequences for leopard populations, whereas the demographic consequences of recreational sport hunting likely are less dramatic.