Recolonizing gray wolves increase parasite infection risk in their prey

The recent recolonization of Central Europe by the European gray wolf (Canis lupus) provides an opportunity to study the dynamics of parasite transmission for cases when a definitive host returns after a phase of local extinction. We investigated whether a newly established wolf population increased the prevalence of those parasites in ungulate intermediate hosts representing wolf prey, whether some parasite species are particularly well adapted to wolves, and the potential basis for such adaptations. We recorded Sarcocystis species richness in wolves and Sarcocystis prevalence in ungulates harvested in study sites with and without permanent wolf presence in Germany using microscopy and DNA metabarcoding. Sarcocystis prevalence in red deer (Cervus elaphus) was significantly higher in wolf areas (79.7%) than in control areas (26.3%) but not in roe deer (Capreolus capreolus) (97.2% vs. 90.4%) or wild boar (Sus scrofa) (82.8% vs. 64.9%). Of 11 Sarcocystis species, Sarcocystis taeniata and Sarcocystis grueneri occurred more often in wolves than expected from the Sarcocystis infection patterns of ungulate prey. Both Sarcocystis species showed a higher increase in prevalence in ungulates in wolf areas than other Sarcocystis species, suggesting that they are particularly well adapted to wolves, and are examples of “wolf specialists”. Sarcocystis species richness in wolves was significantly higher in pups than in adults. “Wolf specialists” persisted during wolf maturation. The results of this study demonstrate that (1) predator–prey interactions influence parasite prevalence, if both predator and prey are part of the parasite life cycle, (2) mesopredators do not necessarily replace the apex predator in parasite transmission dynamics for particular parasites of which the apex predator is the definitive host, even if meso‐ and apex predators were from the same taxonomic family (here: Canidae, e.g., red foxes Vulpes vulpes), and (3) age‐dependent immune maturation contributes to the control of protozoan infection in wolves

Identifying refuges for Borneo's elusive Hose's civet

Human-induced environmental changes, particularly climate change, pose a threat to many tropical montane species, making the identification of optimal future habitat a conservation priority. Here we used maximum entropy (Maxent) and boosted regression trees to predict suitable habitat of the threatened Bornean highland endemic Hose's civet (Diplogale hosei), that is currently available, and for future time periods (2050s and 2080s), considering future land cover and climate change predictions. Next, we identified areas that were consistently suitable under current and future model predictions as forest refuges. Our analysis predicted that Hose's civet is restricted mainly to the highlands of Borneo to an area less than 20,000 km2 (about 2% of the entire island of Borneo). Changes in land cover have little impact on predicted suitable area for the species. However, we predicted habitat loss due to climate change to approximate 86% by 2080, except under a “green economy scenario” which showed stable or increasing suitable habitat. Refuges were small, about 11% of 2010 habitat, and mostly restricted to lower montane forest. About 28–35% of refuges lie within the current protected area network though much is designated as commercial forests within the proposed Heart of Borneo (HoB). For the conservation of Hose's civet and likely other Bornean highland endemics, we recommend increased wildlife and forest law enforcement in identified protected refuges and sustainable timber harvesting practices in surrounding commercial forests, both within the HoB and the extensions we identified. Results of our green model showed that efforts to reduce greenhouse gas emissions will likely contribute immensely to the long-term conservation of highland species such as Hose's civet

Surrogate hosts: Hunting dogs and recolonizing grey wolves share their endoparasites

Understanding how closely related wildlife species and their domesticated counterparts exchange or share parasites, or replace each other in parasite life cycles, is of great interest to veterinary and human public health, and wildlife ecology. Grey wolves (Canis lupus) host and spread endoparasites that can either directly infect canid conspecifics or their prey serving as intermediate hosts of indirectly transmitted species. The wolf recolonization of Central Europe represents an opportunity to study parasite transmission dynamics between wildlife and domestic species for cases when a definitive host returns after local extinction – a situation equivalent to a ‘removal experiment’. Here we investigate whether the re–appearance of wolves has increased parasite pressure on hunting dogs – a group of companion animals of particular interest as they have a similar diet to wolves and flush wolf habitats when hunting. We compared prevalence (P) and species richness (SR) of helminths and the protozoan Sarcocystis to determine whether they were higher in hunting dogs from wolf areas (ndogs = 49) than a control area (ndogs = 29) without wolves. Of particular interest were S. grueneri and S. taeniata, known as ‘wolf specialists’. Five helminth and 11 Sarcocystis species were identified, of which all helminths and eight Sarcocystis species were shared between dogs and wolves. Overall prevalence and species richness of helminths (P:38.5% vs. 24.1%; SRmean:0.4 vs. 0.3 species) and Sarcocystis (P:63.3% vs. 65.5%, SRmean:2.1 vs. 1.8 species) did not differ between study sites. However, hunting dogs were significantly more likely to be infected with S. grueneri in wolf areas (P:45.2% vs. 10.5%; p = 0.035). The findings suggest that wolves indirectly increase S. grueneri infection risk for hunting dogs since cervids are intermediate hosts and occasionally fed to dogs. Furthermore, a periodic anthelminthic treatment of hunting dogs may be an effective measure to control helminth infections regardless of wolf presence

The interplay between social rank, physiological constraints and investment in courtship in male spotted hyenas

In many animal societies, dominant males have a higher reproductive success than subordinate males. The proximate mechanisms by which social rank influences reproductive success are poorly understood. One prominent hypothesis posits that rank-related male attributes of attractiveness and fighting ability are the main mediators of reproductive skew. Yet, empirical evidence in support of this hypothesis is limited. An alternative hypothesis emphasises the inherent social dimension of dominance relationships and posits that the relationship between male social rank and reproductive success is mediated by the physiological costs of male?male competition. This has not been tested in systems in which the two hypotheses can be disentangled. We investigated the interplay between male social rank, physiological costs and male investment in social and sexual activities. We used measurements of faecal glucocorticoid metabolite concentrations (fGMC) as biomarkers of physiological costs and long-term behavioural data of 319 males in free-ranging spotted hyenas Crocuta crocuta, a species in which male access to females and reproductive success do not depend on physical attributes. When males courted females and interacted with male competitors, low-ranking males had higher fGMC than high-ranking males. In contrast, fGMC did not vary with social rank when males were alone or when they courted females and competitors were absent. Low-ranking males minimised their exposure to physiologically costly intrasexual competition; they spent more time alone and less time engaging in social and sexual activities than did high-ranking males. They also invested less than high-ranking males in courting the most contested and highest-quality females. Our findings demonstrate that the physiological costs of intrasexual competition in male spotted hyenas vary with social rank and shape behavioural trade-offs between the allocation of time and physiological resources to social integration, reproduction and self-maintenance. Our study suggests that physiological and social constraints play a pivotal role in the emergence of rank-related male reproductive success. The study provides insights into how the social organisation and breeding system shape physiological constraints and patterns of reproductive skew within and between species. A free Plain Language Summary can be found within the Supporting Information of this article

Data from: Recolonizing grey wolves increase parasite infection risk in their prey

The recent recolonization of Central Europe by the European grey wolf (Canis lupus) provides an opportunity to study the dynamics of parasite transmission for cases when a definitive host returns after a phase of local extinction. We investigated whether a newly established wolf population increased the prevalence of those parasites in ungulate intermediate hosts representing wolf prey, whether some parasite species are particularly well adapted to wolves, and the potential basis for such adaptations. We recorded Sarcocystis species richness in wolves and Sarcocystis prevalence in ungulates harvested in study sites with and without permanent wolf presence in Germany using microscopy and DNA metabarcoding. Sarcocystis prevalence in red deer (Cervus elaphus) was significantly higher in wolf areas (79.7%) than in control areas (26.3%) but not in roe deer (Capreolus capreolus) (97.2% vs. 90.4%) or wild boar (Sus scrofa) (82.8% vs. 64.9%). Of 11 Sarcocystis species, S. taeniata and S. grueneri occurred more often in wolves than expected from the Sarcocystis infection patterns of ungulate prey. Both Sarcocystis species showed a higher increase in prevalence in ungulates in wolf areas than other Sarcocystis species, suggesting that they are particularly well adapted to wolves, and are examples of ‘wolf specialists’. Sarcocystis species richness in wolves was significantly higher in pups than in adults. ‘Wolf specialists’ persisted during wolf maturation. The results of this study demonstrate that (1) predator–prey interactions influence parasite prevalence, if both predator and prey are part of the parasite life cycle, (2) mesopredators do not necessarily replace the apex predator in parasite transmission dynamics for particular parasites of which the apex predator is the definitive host, even if meso– and apex predators were from the same taxonomic family (here: Canidae, e.g. red foxes Vulpes vulpes), and (3) age–dependent immune maturation contributes to the control of protozoan infection in wolves

Sarcocystis results table prey

As described in the Material & Methods section (2.4. Bioinformatics) of the corresponding paper, this csv results table contains the assignment of 18S operational taxonomic units (OTUs) to Sarcocystis species, when applying an identity threshold of 98% using BLAST® (blastn, Altschul et al., 1990). Only hits with a biunique best bit score for one parasite species were collected. Additionally, the table provides the sample ID, ungulate species, OTU number, amplicon name, blast identity as well as information about whether samples had been collected in an area recolonized by wolves or not

Population expansion and individual age affect endoparasite richness and diversity in a recolonising large carnivore population

The recent recolonisation of the Central European lowland (CEL) by the grey wolf (Canis lupus) provides an excellent opportunity to study the effect of founder events on endoparasite diversity. Which role do prey and predator populations play in the re-establishment of endoparasite life cycles? Which intrinsic and extrinsic factors control individual endoparasite diversity in an expanding host population? In 53 individually known CEL wolves sampled in Germany, we revealed a community of four cestode, eight nematode, one trematode and 12 potential Sarcocystis species through molecular genetic techniques. Infections with zoonotic Echinococcus multilocularis, Trichinella britovi and T. spiralis occurred as single cases. Per capita endoparasite species richness and diversity significantly increased with population size and changed with age, whereas sex, microsatellite heterozygosity, and geographic origin had no effect. Tapeworm abundance (Taenia spp.) was significantly higher in immigrants than natives. Metacestode prevalence was slightly higher in ungulates from wolf territories than from control areas elsewhere. Even though alternative canid definitive hosts might also play a role within the investigated parasite life cycles, our findings indicate that (1) immigrated wolves increase parasite diversity in German packs, and (2) prevalence of wolf-associated parasites had declined during wolf absence and has now risen during recolonisation

MHC-dependent mate choice is linked to a trace-amine-associated receptor gene in a mammal

Major histocompatibility complex (MHC) genes play a pivotal role in vertebrate self/nonself recognition, parasite resistance and life history decisions. In evolutionary terms, the MHC’s exceptional diversity is likely maintained by sexual and pathogen-driven selection. Even though MHC-dependent mating preferences have been confirmed for many species, the sensory and genetic mechanisms underlying mate recognition remain cryptic. Since olfaction is crucial for social communication in vertebrates, variation in chemosensory receptor genes could explain MHC-dependent mating patterns. Here, we investigated whether female mate choice is based on MHC alleles and linked to variation in chemosensory trace amine-associated receptors (TAARs) in the greater sac-winged bat (Saccopteryx bilineata). We sequenced several MHC and TAAR genes and related their variation to mating and paternity data. We found strong evidence for MHC class I-dependent female choice for genetically diverse and dissimilar males. We also detected a significant interaction between mate choice and the female TAAR3 genotype, with TAAR3-heterozygous females being more likely to choose MHC-diverse males. These results suggest that TAARs and olfactory cues may be key mediators in mammalian MHC-dependent mate choice. Our study may help identify the ligands involved in the chemical communication between potential mates

Population expansion and individual age affect endoparasite richness and diversity in a recolonising large carnivore population

The recent recolonisation of the Central European lowland (CEL) by the grey wolf (Canis lupus) provides an excellent opportunity to study the effect of founder events on endoparasite diversity. Which role do prey and predator populations play in the re-establishment of endoparasite life cycles? Which intrinsic and extrinsic factors control individual endoparasite diversity in an expanding host population? In 53 individually known CEL wolves sampled in Germany, we revealed a community of four cestode, eight nematode, one trematode and 12 potential Sarcocystis species through molecular genetic techniques. Infections with zoonotic Echinococcus multilocularis, Trichinella britovi and T. spiralis occurred as single cases. Per capita endoparasite species richness and diversity significantly increased with population size and changed with age, whereas sex, microsatellite heterozygosity, and geographic origin had no effect. Tapeworm abundance (Taenia spp.) was significantly higher in immigrants than natives. Metacestode prevalence was slightly higher in ungulates from wolf territories than from control areas elsewhere. Even though alternative canid definitive hosts might also play a role within the investigated parasite life cycles, our findings indicate that (1) immigrated wolves increase parasite diversity in German packs, and (2) prevalence of wolf-associated parasites had declined during wolf absence and has now risen during recolonisation

The importance of correcting for sampling bias in MaxEnt species distribution models

Aim:Advancement in ecological methods predicting species distributions is a crucial precondition for deriving sound management actions. Maximum entropy (MaxEnt) models are a popular tool to predict species distributions, as they are considered able to cope well with sparse, irregularly sampled data and minor location errors. Although a fundamental assumption of MaxEnt is that the entire area of interest has been systematically sampled, in practice, MaxEnt models are usually built from occurrence records that are spatially biased towards better‐surveyed areas. Two common, yet not compared, strategies to cope with uneven sampling effort are spatial filtering of occurrence data and background manipulation using environmental data with the same spatial bias as occurrence data. We tested these strategies using simulated data and a recently collated dataset on Malay civet Viverra tangalunga in Borneo.Location:Borneo, Southeast Asia.Methods:We collated 504 occurrence records of Malay civets from Borneo of which 291 records were from 2001 to 2011 and used them in the MaxEnt analysis (baseline scenario) together with 25 environmental input variables. We simulated datasets for two virtual species (similar to a range‐restricted highland and a lowland species) using the same number of records for model building. As occurrence records were biased towards north‐eastern Borneo, we investigated the efficacy of spatial filtering versus background manipulation to reduce overprediction or underprediction in specific areas.Results:Spatial filtering minimized omission errors (false negatives) and commission errors (false positives). We recommend that when sample size is insufficient to allow spatial filtering, manipulation of the background dataset is preferable to not correcting for sampling bias, although predictions were comparatively weak and commission errors increased.Main Conclusions:We conclude that a substantial improvement in the quality of model predictions can be achieved if uneven sampling effort is taken into account, thereby improving the efficacy of species conservation planning.publishe