The impact of the COVID-19 lockdowns on wildlife-vehicle collisions in the UK.

Wildlife-vehicle collisions (WVCs) cause millions of vertebrate mortalities globally, threatening population viability and influencing wildlife behaviour and survival. Traffic volume and speed can influence wildlife mortality on roads, but roadkill risk is species specific and depends on ecological traits. The COVID-19 pandemic, and associated UK-wide lockdowns, offered a unique opportunity to investigate how reducing traffic volume alters WVC. These periods of reduced human mobility have been coined the 'anthropause'. We used the anthropause to identify which ecological traits may render species vulnerable to WVC. We did this by comparing the relative change in WVC of species with differing traits before and during the anthropause. We used Generalised Additive Model predictions to assess which of the 19 species most frequently observed as WVC in the UK exhibited changes in road mortality during two lockdown periods, March-May 2020 and December 2020-March 2021, relative to the same time periods in previous years (2014-2019). Compositional data analysis was used to identify ecological traits associated with changes in the relative number of observations during lockdown periods compared to previous years. WVC were, across all species, 80% lower during the anthropause than predicted. Compositional data analysis revealed proportionally fewer reports of nocturnal mammals, urban visitors, mammals with greater brain mass and birds with a longer flight initiation distance. Species that have several of these traits, and correspondingly significantly lower than predicted WVC during lockdowns, included badgers Meles meles, foxes Vulpes vulpes, and pheasants, Phasianus colchicus; we posit they stand to benefit most from reduced traffic, and, of the species studied here, have highest mortality under 'normal' traffic levels. This study identifies traits and species that may have experienced a temporary reprieve during the anthropause, and highlights the impacts of traffic-induced mortality on species numbers and ultimately on trait frequency in a road-dominated landscape. By taking advantage of reductions in traffic offered by the anthropause, we can understand how vehicles influence wildlife survival and behaviour and may be exerting a selective force for certain species and traits.

Transmission risk predicts avoidance of infected conspecifics in Trinidadian guppies.

Associating with conspecifics afflicted with infectious diseases increases the risk of becoming infected, but engaging in avoidance behaviour incurs the cost of lost social benefits. Across systems, infected individuals vary in the transmission risk they pose, so natural selection should favour risk-sensitive avoidance behaviour that optimally balances the costs and benefits of sociality. Here, we use the guppy Poecilia reticulata-Gyrodactylus turnbulli host-parasite system to test the prediction that individuals avoid infected conspecifics in proportion to the transmission risk they pose. In dichotomous choice tests, uninfected fish avoided both the chemical and visual cues, presented separately, of infected conspecifics only in the later stages of infection. A transmission experiment indicated that this avoidance behaviour accurately tracked transmission risk (quantified as both the speed at which transmission occurs and the number of parasites transmitting) through the course of infection. Together, these findings reveal that uninfected hosts can use redundant cues across sensory systems to inform dynamic risk-sensitive avoidance behaviour. This correlation between the transmission risk posed by infected individuals and the avoidance response they elicit has implications for the evolutionary ecology of infectious disease, and its explicit inclusion may improve the ability of epidemic models to predict disease spread.

Population dynamics of wild rodents induce stochastic fadeouts of a zoonotic pathogen.

Stochastic processes play an important role in the infectious disease dynamics of wildlife, especially in species subject to large population oscillations. Here, we study the case of a free ranging population of yellow-necked mice (Apodemus flavicollis) in northern Italy, where circulation of Dobrava-Belgrade hantavirus (DOBV) has been detected intermittently since 2001, until an outbreak emerged in 2010. We analysed the transmission dynamics of the recent outbreak using a computational model that accounts for seasonal changes of the host population and territorial behaviour. Model parameters were informed by capture-mark-recapture data collected over 14 years and longitudinal seroprevalence data from 2010 to 2013. The intermittent observation of DOBV before 2010 can be interpreted as repeated stochastic fadeouts after multiple introductions of infectious rodents migrating from neighbouring areas. We estimated that only 20% of introductions in a naïve host population results in sustained transmission after 2 years, despite an effective reproduction number well above the epidemic threshold (mean 4·5, 95% credible intervals, CI: 0·65-15·8). Following the 2010 outbreak, DOBV has become endemic in the study area, but we predict a constant probability of about 4·7% per year that infection dies out, following large population drops in winter. In the absence of stochastic fadeout, viral prevalence is predicted to continue its growth to an oscillating equilibrium around a value of 24% (95% CI: 3-57). We presented an example of invasion dynamics of a zoonotic virus where stochastic fadeout have played a major role and may induce future extinction of the endemic infection.

East-West Divide: temperature and land cover drive spatial variation of Toxoplasma gondii infection in Eurasian otters (Lutra lutra) from England and Wales.

Toxoplasma gondii, a zoonotic parasite of global importance, infects all endothermic vertebrates, with extensive health implications. The prevalence of this parasite is seldom monitored in wildlife. Here, a semi-aquatic species, the Eurasian otter (Lutra lutra) was used as a model to assess the potential effect of climate, land cover and biotic factors on T. gondii seroprevalence in British wildlife. The Sabin-Feldman cytoplasm-modifying dye test identified T. gondii antibodies in 25·5% of blood samples from otters found dead, mainly as road kill, in England and Wales, between 2004 and 2010. Otters in the east of England were more likely to be infected with T. gondii than those in western regions. Land cover and temperature are key determinants of T. gondii infection risk, with more infection in arable areas and lower infection where temperatures are higher. The probability of T. gondii infection increased with host age, reflecting cumulative exposure with time, but there was no association between T. gondii seroprevalence and cause of host death.

AI-based discovery of habitats from museum collections.

Museum collection records are a source of historic data for species occurrence, but little attention is paid to the associated descriptions of habitat at the sample locations. We propose that artificial intelligence methods have potential to use these descriptions for reconstructing past habitat, to address ecological and evolutionary questions.

Adaptive evolution during an ongoing range expansion: the invasive bank vole (Myodes glareolus) in Ireland.

Range expansions are extremely common, but have only recently begun to attract attention in terms of their genetic consequences. As populations expand, demes at the wave front experience strong genetic drift, which is expected to reduce genetic diversity and potentially cause 'allele surfing', where alleles may become fixed over a wide geographical area even if their effects are deleterious. Previous simulation models show that range expansions can generate very strong selective gradients on dispersal, reproduction, competition and immunity. To investigate the effects of range expansion on genetic diversity and adaptation, we studied the population genomics of the bank vole (Myodes glareolus) in Ireland. The bank vole was likely introduced in the late 1920s and is expanding its range at a rate of ~2.5 km/year. Using genotyping-by-sequencing, we genotyped 281 bank voles at 5979 SNP loci. Fourteen sample sites were arranged in three transects running from the introduction site to the wave front of the expansion. We found significant declines in genetic diversity along all three transects. However, there was no evidence that sites at the wave front had accumulated more deleterious mutations. We looked for outlier loci with strong correlations between allele frequency and distance from the introduction site, where the direction of correlation was the same in all three transects. Amongst these outliers, we found significant enrichment for genic SNPs, suggesting the action of selection. Candidates for selection included several genes with immunological functions and several genes that could influence behaviour.

Do invasive species perform better in their new ranges?

A fundamental assumption in invasion biology is that most invasive species exhibit enhanced performance in their introduced range relative to their home ranges. This idea has given rise to numerous hypotheses explaining "invasion success" by virtue of altered ecological and evolutionary pressures. There are surprisingly few data, however, testing the underlying assumption that the performance of introduced populations, including organism size, reproductive output, and abundance, is enhanced in their introduced compared to their native range. Here, we combined data from published studies to test this hypothesis for 26 plant and 27 animal species that are considered to be invasive. On average, individuals of these 53 species were indeed larger, more fecund, and more abundant in their introduced ranges. The overall mean, however, belied significant variability among species, as roughly half of the investigated species (N=27) performed similarly when compared to conspecific populations in their native range. Thus, although some invasive species are performing better in their new ranges, the pattern is not universal, and just as many are performing largely the same across ranges.

The presence of territorial damselfish predicts choosy client species richness at cleaning stations.

Mutualisms are driven by partners deciding to interact with one another to gain specific services or rewards. As predicted by biological market theory, partners should be selected based on the likelihood, quality, reward level, and or services each partner can offer. Third-party species that are not directly involved in the interaction, however, may indirectly affect the occurrence and or quality of the services provided, thereby affecting which partners are selected or avoided. We investigated how different clients of the sharknose goby (Elacatinus evelynae) cleaner fish were distributed across cleaning stations, and asked what characteristics, relating to biological market theory, affected this distribution. Through quantifying the visitation and cleaning patterns of client fish that can choose which cleaning station(s) to visit, we found that the relative species richness of visiting clients at stations was negatively associated with the presence of disruptive territorial damselfish at the station. Our study highlights, therefore, the need to consider the indirect effects of third-party species and their interactions (e.g., agonistic interactions) when attempting to understand mutualistic interactions between species. Moreover, we highlight how cooperative interactions may be indirectly governed by external partners.

Demographic effects of road mortality on mammalian populations: a systematic review.

In light of rapidly expanding road networks worldwide, there is increasing global awareness of the growing amount of mammalian roadkill. However, the ways in which road mortality affects the population dynamics of different species remains largely unclear. We aimed to categorise the demographic parameters in mammalian populations around the world that are directly or indirectly affected by road mortality, as well as identify the most effective study designs for quantifying population-level consequences of road mortality. We conducted a comprehensive systematic review to synthesise literature published between 2000 and 2021 and out of 11,238 unique studies returned, 83 studies were retained comprising 69 mammalian species and 150 populations. A bias towards research-intensive countries and larger mammals was apparent. Although searches were conducted in five languages, all studies meeting the inclusion criteria were in English. Relatively few studies (13.3%) provided relevant demographic context to roadkill figures, hampering understanding of the impacts on population persistence. We categorised five direct demographic parameters affected by road mortality: sex- and age-biased mortality, the percentage of a population killed on roads per year (values up to 50% were reported), the contribution of roadkill to total mortality rates (up to 80%), and roadkill during inter-patch or long-distance movements. Female-biased mortality may be more prevalent than previously recognised and is likely to be critical to population dynamics. Roadkill was the greatest source of mortality for 28% of studied populations and both additive and compensatory mechanisms to roadkill were found to occur, bringing varied challenges to conservation around roads. In addition, intra-specific population differences in demographic effects of road mortality were common. This highlights that the relative importance of road mortality is likely to be context specific as the road configuration and habitat quality surrounding a population can vary. Road ecology studies that collect data on key life parameters, such as age/stage/sex-specific survival and dispersal success, and that use a combination of methods are critical in understanding long-term impacts. Quantifying the demographic impacts of road mortality is an important yet complex consideration for proactive road management.

Passive citizen science: The role of social media in wildlife observations.

Citizen science plays an important role in observing the natural environment. While conventional citizen science consists of organized campaigns to observe a particular phenomenon or species there are also many ad hoc observations of the environment in social media. These data constitute a valuable resource for 'passive citizen science'-the use of social media that are unconnected to any particular citizen science program, but represent an untapped dataset of ecological value. We explore the value of passive citizen science, by evaluating species distributions using the photo sharing site Flickr. The data are evaluated relative to those submitted to the National Biodiversity Network (NBN) Atlas, the largest collection of species distribution data in the UK. Our study focuses on the 1500 best represented species on NBN, and common invasive species within UK, and compares the spatial and temporal distribution with NBN data. We also introduce an innovative image verification technique that uses the Google Cloud Vision API in combination with species taxonomic data to determine the likelihood that a mention of a species on Flickr represents a given species. The spatial and temporal analyses for our case studies suggest that the Flickr dataset best reflects the NBN dataset when considering a purely spatial distribution with no time constraints. The best represented species on Flickr in comparison to NBN are diurnal garden birds as around 70% of the Flickr posts for them are valid observations relative to the NBN. Passive citizen science could offer a rich source of observation data for certain taxonomic groups, and/or as a repository for dedicated projects. Our novel method of validating Flickr records is suited to verifying more extensive collections, including less well-known species, and when used in combination with citizen science projects could offer a platform for accurate identification of species and their location.

Temporal patterns of wildlife roadkill in the UK.

Wildlife-vehicle collisions are one of the main causes of mortality for wild mammals and birds in the UK. Here, using a dataset of 54,000+ records collated by a citizen science roadkill recording scheme between 2014-2019, we analyse and present temporal patterns of wildlife roadkill of the 19 most commonly reported taxa in the UK (84% of all reported roadkill). Most taxa (13 out of 19) showed significant and consistent seasonal variations in road mortality and fitted one of two seasonal patterns; bimodal or unimodal: only three species (red fox Vulpes vulpes, European polecat Mustela putorius and Reeves' muntjac deer Muntiacus reevesi) showed no significant seasonality. Species that increase movement in spring and autumn potentially have bimodal patterns in roadkill due to the increase in mate-searching and juvenile dispersal during these respective time periods (e.g. European badger Meles meles). Unimodal patterns likely represent increased mortality due to a single short pulse in activity associated with breeding (e.g. birds) or foraging (e.g. grey squirrels Sciurus carolinensis in autumn). Importantly, these patterns also indicate periods of increased risk for drivers, potentially posing a greater threat to human welfare. In addition to behaviour-driven annual patterns, abiotic factors (temperature and rainfall) explained some variance in roadkill. Notably, high rainfall was associated with decreased observations of two bird taxa (gulls and Eurasian magpies Pica pica) and European rabbit Oryctolagus cuniculus. By quantifying seasonal patterns in roadkill, we highlight a significant anthropogenic impact on wild species, which is important in relation to conservation, animal welfare, and human safety.

Diet-driven mercury contamination is associated with polar bear gut microbiota.

The gut microbiota may modulate the disposition and toxicity of environmental contaminants within a host but, conversely, contaminants may also impact gut bacteria. Such contaminant-gut microbial connections, which could lead to alteration of host health, remain poorly known and are rarely studied in free-ranging wildlife. The polar bear (Ursus maritimus) is a long-lived, wide-ranging apex predator that feeds on a variety of high trophic position seal and cetacean species and, as such, is exposed to among the highest levels of biomagnifying contaminants of all Arctic species. Here, we investigate associations between mercury (THg; a key Arctic contaminant), diet, and the diversity and composition of the gut microbiota of polar bears inhabiting the southern Beaufort Sea, while accounting for host sex, age class and body condition. Bacterial diversity was negatively associated with seal consumption and mercury, a pattern seen for both Shannon and Inverse Simpson alpha diversity indices (adjusted R2 = 0.35, F1,18 = 8.00, P = 0.013 and adjusted R2 = 0.26, F1,18 = 6.04, P = 0.027, respectively). No association was found with sex, age class or body condition of polar bears. Bacteria known to either be involved in THg methylation or considered to be highly contaminant resistant, including Lactobacillales, Bacillales and Aeromonadales, were significantly more abundant in individuals that had higher THg concentrations. Conversely, individuals with higher THg concentrations showed a significantly lower abundance of Bacteroidales, a bacterial order that typically plays an important role in supporting host immune function by stimulating intraepithelial lymphocytes within the epithelial barrier. These associations between diet-acquired mercury and microbiota illustrate a potentially overlooked outcome of mercury accumulation in polar bears.

Different evolutionary trajectories of European avian-like and classical swine H1N1 influenza A viruses.

In 1979, a lineage of avian-like H1N1 influenza A viruses emerged in European swine populations independently from the classical swine H1N1 virus lineage that had circulated in pigs since the Spanish influenza pandemic of 1918. To determine whether these two distinct lineages of swine-adapted A/H1N1 viruses evolved from avian-like A/H1N1 ancestors in similar ways, as might be expected given their common host species and origin, we compared patterns of nucleotide and amino acid change in whole genome sequences of both groups. An analysis of nucleotide compositional bias across all eight genomic segments for the two swine lineages showed a clear lineage-specific bias, although a segment-specific effect was also apparent. As such, there appears to be only a relatively weak host-specific selection pressure. Strikingly, despite each lineage evolving in the same species of host for decades, amino acid analysis revealed little evidence of either parallel or convergent changes. These findings suggest that although adaptation due to evolutionary lineages can be distinguished, there are functional and structural constraints on all gene segments and that the evolutionary trajectory of each lineage of swine A/H1N1 virus has a strong historical contingency. Thus, in the context of emergence of an influenza A virus strain via a host switch event, it is difficult to predict what specific polygenic changes are needed for mammalian adaptation.

Applying predator-prey theory to modelling immune-mediated, within-host interspecific parasite interactions.

Predator-prey models are often applied to the interactions between host immunity and parasite growth. A key component of these models is the immune system's functional response, the relationship between immune activity and parasite load. Typically, models assume a simple, linear functional response. However, based on the mechanistic interactions between parasites and immunity we argue that alternative forms are more likely, resulting in very different predictions, ranging from parasite exclusion to chronic infection. By extending this framework to consider multiple infections we show that combinations of parasites eliciting different functional responses greatly affect community stability. Indeed, some parasites may stabilize other species that would be unstable if infecting alone. Therefore hosts' immune systems may have adapted to tolerate certain parasites, rather than clear them and risk erratic parasite dynamics. We urge for more detailed empirical information relating immune activity to parasite load to enable better predictions of the dynamic consequences of immune-mediated interspecific interactions within parasite communities.

Consistency in mutualism relies on local, rather than wider community biodiversity.

Mutualistic interactions play a major role in shaping the Earth's biodiversity, yet the consistent drivers governing these beneficial interactions are unknown. Using a long-term (8 year, including > 256 h behavioural observations) dataset of the interaction patterns of a service-resource mutualism (the cleaner-client interaction), we identified consistent and dynamic predictors of mutualistic outcomes. We showed that cleaning was consistently more frequent when the presence of third-party species and client partner abundance locally increased (creating choice options), whilst partner identity regulated client behaviours. Eight of our 12 predictors of cleaner and client behaviour played a dynamic role in predicting both the quality (duration) and quantity (frequency) of interactions, and we suggest that the environmental context acting on these predictors at a specific time point will indirectly regulate their role in cleaner-client interaction patterns: context-dependency can hence regulate mutualisms both directly and indirectly. Together our study highlights that consistency in cleaner-client mutualisms relies strongly on the local, rather than wider community-with biodiversity loss threatening all environments this presents a worrying future for the pervasiveness of mutualisms.

To clean or not to clean: Cleaning mutualism breakdown in a tidal environment.

The dynamics and prevalence of mutualistic interactions, which are responsible for the maintenance and structuring of all ecological communities, are vulnerable to changes in abiotic and biotic environmental conditions. Mutualistic outcomes can quickly shift from cooperation to conflict, but it unclear how resilient and stable mutualistic outcomes are to more variable conditions. Tidally controlled coral atoll lagoons that experience extreme diurnal environmental shifts thus provide a model from which to test plasticity in mutualistic behavior of dedicated (formerly obligate) cleaner fish, which acquire all their food resources through client interactions. Here, we investigated cleaning patterns of a model cleaner fish species, the bluestreak wrasse (Labroides dimidiatus), in an isolated tidal lagoon on the Great Barrier Reef. Under tidally restricted conditions, uniquely both adults and juveniles were part-time facultative cleaners, pecking on Isopora palifera coral. The mutualism was not completely abandoned, with adults also wandering across the reef in search of clients, rather than waiting at fixed site cleaning stations, a behavior not yet observed at any other reef. Contrary to well-established patterns for this cleaner, juveniles appeared to exploit the system, by biting ("cheating") their clients more frequently than adults. We show for the first time, that within this variable tidal environment, where mutualistic cleaning might not represent a stable food source, the prevalence and dynamics of this mutualism may be breaking down (through increased cheating and partial abandonment). Environmental variability could thus reduce the pervasiveness of mutualisms within our ecosystems, ultimately reducing the stability of the system.

Impacts and Potential Mitigation of Road Mortality for Hedgehogs in Europe.

Transport infrastructure is a pervasive element in modern landscapes and continues to expand to meet the demands of a growing human population and its associated resource consumption. Road-induced mortality is often thought to be a major contributor to the marked declines of European hedgehog populations. This review synthesizes available evidence on the population-level impacts of road mortality and the threat to population viability for the five hedgehog species in Europe. Local and national studies suggest that road mortality can cause significant depletions in population sizes, predominantly removing adult males. Traffic collisions are a probable cause of fragmentation effects, subsequently undermining ecological processes such as dispersal, as well as the genetic variance and fitness of isolated populations. Further studies are necessary to improve population estimates and explicitly examine the consequences of sex- and age-specific mortality rates. Hedgehogs have been reported to use crossing structures, such as road tunnels, yet evaluations of mitigation measures for population survival probability are largely absent. This highlights the need for robust studies that consider population dynamics and genetics in response to mitigation. In light of ongoing declines of hedgehog populations, it is paramount that applied research is prioritised and integrated into a holistic spatial planning process.

Predicting hedgehog mortality risks on British roads using habitat suitability modelling.

Road vehicle collisions are likely to be an important contributory factor in the decline of the European hedgehog (Erinaceus europaeus) in Britain. Here, a collaborative roadkill dataset collected from multiple projects across Britain was used to assess when, where and why hedgehog roadkill are more likely to occur. Seasonal trends were assessed using a Generalized Additive Model. There were few casualties in winter-the hibernation season for hedgehogs-with a gradual increase from February that reached a peak in July before declining thereafter. A sequential multi-level Habitat Suitability Modelling (HSM) framework was then used to identify areas showing a high probability of hedgehog roadkill occurrence throughout the entire British road network (∼400,000 km) based on multi-scale environmental determinants. The HSM predicted that grassland and urban habitat coverage were important in predicting the probability of roadkill at a national scale. Probabilities peaked at approximately 50% urban cover at a one km scale and increased linearly with grassland cover (improved and rough grassland). Areas predicted to experience high probabilities of hedgehog roadkill occurrence were therefore in urban and suburban environments, that is, where a mix of urban and grassland habitats occur. These areas covered 9% of the total British road network. In combination with information on the frequency with which particular locations have hedgehog road casualties, the framework can help to identify priority areas for mitigation measures.

Parasites of an Arctic scavenger; the wolverine (Gulo gulo).

Parasites are fundamental components within all ecosystems, shaping interaction webs, host population dynamics and behaviour. Despite this, baseline data is lacking to understand the parasite ecology of many Arctic species, including the wolverine (Gulo gulo), a top Arctic predator and scavenger. Here, we combined traditional count methods (i.e. adult helminth recovery, where taxonomy was confirmed by molecular identification) with 18S rRNA high-throughput sequencing to document the wolverine parasite community. Further, we investigated whether the abundance of parasites detected using traditional methods were associated with host metadata, latitude, and longitude (ranging from the northern limit of the boreal forest to the low Arctic and Arctic tundra in Nunavut, Canada). Adult parasites in intestinal contents were identified as Baylisascaris devosi in 72% (n = 39) of wolverines and Taenia spp. in 22% (n = 12), of which specimens from 2 wolverines were identified as T. twitchelli based on COX1 sequence. 18S rRNA high-throughput sequencing on DNA extracted from faeces detected additional parasites, including a pseudophyllid cestode (Diplogonoporus spp. or Diphyllobothrium spp.), two metastrongyloid lungworms (Angiostrongylus spp. or Aelurostrongylus spp., and Crenosoma spp.), an ascarid nematode (Ascaris spp. or Toxocara spp.), a Trichinella spp. nematode, and the protozoan Sarcocystis spp., though each at a prevalence less than 13% (n = 7). The abundance of B. devosi significantly decreased with latitude (slope = -0.68; R2 = 0.17; P = 0.004), suggesting a northerly limit in distribution. We describe B. devosi and T. twitchelli in Canadian wolverines for the first time since 1978, and extend the recorded geographic distribution of these parasites ca 2000 km to the East and into the tundra ecosystem. Our findings illustrate the value of molecular methods in support of traditional methods, encouraging additional work to improve the advancement of molecular screening for parasites.

Does elevated testosterone result in increased exposure and transmission of parasites?

Male-biased infection is a common phenomenon in vertebrate-parasite systems and male-biased transmission has been experimentally demonstrated. One mechanism that is hypothesized to create male-biased transmission is the immuno-suppressive effect of testosterone because it increases susceptibility to infection. Testosterone also influences host behaviour and, consequently, may increase exposure to parasites. To test how testosterone could increase exposure and transmission, we undertook a longitudinal mark-recapture study where we experimentally elevated testosterone levels in wild male rodents. Individuals in control populations reduced the average number of contacts over the treatment period, while populations with experimentally elevated testosterone levels maintained the number of contacts between hosts. As a result, the transmission potential was higher in testosterone treated populations compared to controls. Our results indicated that males with high-testosterone levels alter the population-level contacts, producing different social networks and increasing transmission potential compared to those where testosterone is at background levels.