Population crash in an invasive species following the recovery of a native predator: the case of the American grey squirrel and the European pine marten in Ireland

In Ireland, the UK and Italy, the invasive North American grey squirrel, Sciurus carolinensis, threatens the survival of the Eurasian red squirrel, Sciurus vulgaris, as the effects of competition and disease almost inevitably lead to total replacement of red squirrel populations. However the results of a recent national squirrel survey suggested that the normally invasive grey squirrel had gone into decline in the Irish midlands, which was anecdotally attributed to an increase in European pine marten, Martes martes, range and numbers. This study aimed to quantify changes in squirrel distribution in Ireland and to investigate the role, if any, of the pine marten in red and grey squirrel population dynamics. A distribution survey of the midlands was carried out which confirmed the grey squirrel population has crashed in approximately 9,000 km² of its former range and the red squirrel is common after an absence of up to 30 years. At landscape level, pine marten and red squirrel abundance were positively correlated, whereas a strong negative correlation between pine marten and grey squirrel presence at woodland level was found to exist. Squirrel demographics were determined by means of live trapping programs which confirmed that the red squirrel in the midlands is now in competitive release and the grey squirrel is present at unusually low density. This study provides the first evidence of a regional grey squirrel population crash and suggests that European pine marten abundance may be a critical factor in the American grey squirrel’s success or failure as an invasive species.     

Non-invasive multi-species monitoring: real-time PCR detection of small mammal and squirrel prey DNA in pine marten (Martes martes) scats

DNA identification of mammal species occurring in the diet of a predator is potentially a useful approach to remotely monitor the distribution of multiple species. This is important in Ireland, where it has been shown that the combined presence of the introduced bank vole and greater white-toothed shrew impact the distribution of the indigenous small mammals, the wood mouse and pygmy shrew. Direct monitoring of these species and their interactions requires trapping, a labour-intensive and costly approach. In this study, we applied an indirect method by genetically testing the presence of small mammals in pine marten scats collected during the National Pine Marten Survey (2005–2007) to map their distribution. We also included additional scats to investigate if less common prey items, the red squirrel and grey squirrel, could also be detected. This study demonstrates that all target species were genetically detected from pine marten scats. This strategy could be implemented as a monitoring programme for indigenous and introduced mammal species.     

Non-invasively determined multi-site variation in pine marten <Emphasis Type="Italic">Martes martes</Emphasis> density,a recovering carnivore in Europe

Pine martens (Martes martes) are subject to national and international conservation legislation throughout most of their European range. Yet population density and abundance estimates, which are a key component of effective conservation management, are lacking in many countries. In this study, a large-scale non-invasive survey was undertaken in 14 forested study sites throughout Ireland to assess variation in pine marten density and abundance. Pine marten hair samples were collected in each study site and analysed using genetic techniques to determine individual identity data. Density and abundance estimates were obtained using spatially explicit capture-recapture models and CAPWIRE. Across all study sites, a total of 93 individual pine marten were identified and captured 217 times. Estimated pine marten density varied from 0 to 2.60 individuals per km² of forested habitat, with all but a single site having estimated densities of ≤1 pine marten per km² of forest habitat. Mean population abundance estimates across all study sites ranged from 0 to 27 individuals. Spatially explicit capture-recapture models on combined data across all 14 study sites provided a mean density estimate of 0.64 (95% CI 0.49–0.81). Combining this with data on the current distribution and estimated area of forest habitat occupied by the species in Ireland, the total pine marten population abundance of pine marten in Ireland was estimated at 3043 (95% CI 2330–3852) individuals. This research has conducted the largest scale investigation of pine marten density and abundance in any part of its global distribution and provided an improved basis for future population assessment and monitoring of this species.     

Does size dimorphism reduce competition between sexes? The diet of male and female pine martens at local and wider geographical scales

Sex-specific niche segregation is often used to explain sexual size dimorphism (SSD). However, whether food niche partitioning between sexes occurs as a case of sexual size dimorphism or by other mechanisms, such as behavioural dimorphism or habitat segregation, remains poorly understood. To evaluate the nature and extent of food-niche differentiation between sexes in a solitary predator I examined variation in the diet of male and female pine martensMartes martes Linnaeus, 1758 in years of high and low rodent abundance. Small mammals were the most important prey for pine martens in years of both low and high rodent abundance (occurring in more than 49% of scats). Birds, invertebrates and plant material were relatively common food items in summer diet, whereas ungulate carcasses were often consumed in autumn—winter. In general, males consumed more ungulate carcasses, plant material, amphibians and reptiles than did females, whereas females preyed more on squirrels and birds than males. There was significant seasonally dependent, between-sex variation in the occurrence of shrews, small rodents, other mammals, birds and invertebrates in marten diet. Whereas the occurrence of bank vole, birds, carcasses and plant material changed between sexes, seasons and years with various rodent abundances, both sexes consumed larger prey and had increased food niche breadth in years of low compared with high rodent abundance. Neither prey size nor food niche breadth were significantly different between males and females. The food-niche overlap between sexes was consistently lower in spring and in years of low rodent abundance. A wider geographical comparison of different marten populations showed that the diet of males and females varied significantly between locations. Females consistently preyed on squirrels and birds, whereas males fed more often on ungulate carcasses and plant material. Local and geographical comparison of male and female diets suggest that food-niche partitioning between male and female pine martens changes across different habitat and food conditions, and is not related to sexual size dimorphism, but rather to behavioural differences between sexes.     

Effect of felling on red fox (Vulpes vulpes) and pine marten (Martes martes) diets in transitional mixed forest in Belarus

In transitional mixed forests in northern and central Belarus the influence of intensified felling on the diets of red foxes Vulpes vulpes L. and pine martens Martes martes L. was investigated in two model forested terrains with sandy and clay top-grounds. A total of 1904 scats of red foxes and 1624 scats of pine martens were analysed over two periods differed by logging rate. When logging rate was conservative, red fox and pine marten diets were found to be similar, but under heavy logging feeding of the predator species shifted. In both model woodlands we found the same pronounced dietary trend of higher consumption of rodents, first of all, Microtus voles. The dietary changes were well related to the registered increase in Microtus vole numbers and total number of rodents in felling areas. The increased preying on rodents caused lower consumption of other food items, particularly medium-sized mammals (year-round) or/and birds or/and fruits (in the warm season) or/and mammalian carrion (in the cold season). In the conditions of intensified felling the food niches of the red fox and pine marten diverged mostly because of the great difference in the species structure of rodents consumed. Red foxes turned to preying on Microtus voles more frequently, but less on bank voles Myodes glareolus; while pine martens increased their taking of Microtus voles, continued foraging for bank voles and began taking slightly more of Apodemus mice. Before heavy logging dietary similarity between the red fox and pine marten was high and did not vary considerably through seasons and study areas, whereas after felling was intensified their diet overlap became lower.     

A species distribution model for pine marten (<Emphasis Type="Italic">Martes martes</Emphasis>) in the least forested region of Europe

Species distribution modelling is a useful technique that provides data on factors that can influence a species range, identify high suitability areas and model future scenarios. The pine marten (Martes martes) has undergone major historical declines in abundance and distribution in Northern Ireland, similar to that which has occurred throughout its range. Currently, the species is in a phase of range expansion in Northern Ireland, in what is the least forested landscape in Europe. To assess the suitability of this environment for pine marten re-establishment, presence only distribution data combined with landcover data at a 10-km scale were used in a species distribution modelling study using Maxent. The results indicated that approximately 32% (4500 km²) of the land area of Northern Ireland had a high probability of pine marten occurrence. Pine marten distribution was positively associated with the extent of conifer forest landcover types, which also had the highest single attribute contribution to the model. Landcover types that were negatively associated with pine marten distribution included the extent of open, dwarf and urban areas.     

Pine marten (Martes martes) distribution and abundance in Ireland: A cross-jurisdictional analysis using non-invasive genetic survey techniques

On the Island of Ireland, pine martens (Martes martes) exist at the western edge of their global geographic range in the least forested region of Europe. The species has undergone substantial declines in abundance and distribution during the 20th century. Here, we report on the first cross-jurisdictional (Republic of Ireland and Northern Ireland) survey that aimed to investigate current pine marten distribution, assess any recent historical change and provide preliminary estimates of population abundance.A standardised non-invasive survey technique that used scat-based transect surveys and DNA analysis to confirm scat identity was deployed in 258 10 km national grid squares during 2005–2007. In the Republic of Ireland, an occupancy rate of 59.6% was found. Comparisons with historical data indicated that a range expansion of pine marten had occurred over the last 30 years. Indicative core population range extended to over 50% of the land area with population abundance estimates of 2740 individuals.In Northern Ireland, an occupancy rate of 56.7% was determined with the population largely concentrated in western areas. There was little or no evidence of any recent expansion from core population areas (18% of land area) despite recent increases in forest cover and full legal protection. Population abundance estimates of 320 emphasise the critical requirement for action to conserve this species.The pine marten is one of the rarest wildlife species in Ireland and, based on our studies, an evidenced based conservation strategy that promotes a sustainable future for the species needs to be developed.     

Shifts in fisher (Pekania pennanti) diet in response to climate-induced tree mortality in California assessed with DNA metabarcoding

A recent climate-induced tree mortality event in California, USA has led to dramatic landscape-level changes in the southern Sierra Nevada. Wide-spread conifer mortality was documented in habitat occupied by fisher (Pekania pennanti), a mature-forest associated species of conservation concern in this region. We analyzed fisher scats collected on the Sierra National Forest from the pre-tree-mortality period (PreTM, 2011 – 2013) and post-tree-mortality period (PostTM, 2017 – 2018). We used DNA metabarcoding to successfully identify taxa and summarized diet composition for 109 PreTM and 102 PostTM fisher scats. We observed 48 different diet items (33 assigned to species and 15 to genus). Mammals, birds, and plants of the Ribes genus (gooseberries and currents) comprised the highest proportions of diet items, although scats also contained DNA from reptiles, insects, arachnids, snails, and fungi. The frequency of occurrence of mammalian prey items was lower in PostTM (49.0%) versus PreTM scats (81.7%) with a reduction in the occurrence of two tree squirrels (Douglas squirrel and Humboldt’s flying squirrel). A higher proportion of scats collected PostTM (46.1%) contained DNA from Ribes spp. versus scats collected PreTM (19.3%). Our data reveal potential cascading effects of climate-induced tree mortality on fisher diet in the southern Sierra Nevada. Flexibility in fisher diet, however, may allow resilience to ecological change though future studies should consider the behavioral, energetic, demographic or fitness consequences from a shift away from medium-sized mammalian prey to plants.     

Variation in the diet of red foxes on Scottish moorland in relation to prey abundance

The diet of red fox Vulpes vulpes was investigated through analysis of 340 scats collected during 1992-1996 from moorland in south-west Scotland. Rodents, game-birds, lagomorphs, carrion and insectivores were the most frequently occurring food types. Fox diet and prey abundance were compared between heather dominant and grass dominant habitat types within the study area. Rodents were the most frequently occurring food type in each habitat and occurred in 63% of seats overall. Rodents occurred more often in scats from grass dominant sites while gamebirds and lagomorphs were more frequent in scats from heather dominant sites. The occurrence of rodents in winter fox scats increased with rodent abundance. In contrast, the occurrence of gamebirds in winter fox scats was unrelated to gamebird abundance but negatively related to rodent abundance. It appeared that foxes switched to gamebirds in years, or habitats, where rodents were uncommon.     

Spring and summer food habits and habitat use of the Europena pine marten (Martes martes) on the island of Micorca, Spain

The food habits and habitat use of pine marten ( Martes martes L.) on the Balearic Island of Mincorca were studied from March-August 1990. In a 28.2 km² area, a series of hiking trails/forest roads were used to collect pine marten faeces bi-monthly and study te species' differential use of habitats. A total of 28 different food items were identified in 723 faeces. Small mammals were the most important food overall, constituting 34% of the volume During March-April, small mammals were the principal food consumed (63% of volume), followed by birds (19%). In May-June, birds were the main food (40%), then small mammals. Plant material and insects were the most important foods in July-August, both made up 68% of the pine marten diet. The abundance of certain foods and the degree of difficulty in obtaining them appear to be important factors that govern pine marten food selection in Minorca. Habitat use was studied along 12 routes totalling 32.6 km. Pine marten showed preference in March-April for Coastal Shrubland habitat, while during May-June they were found most in the Upland Pine type. During July-August, the Upland Pine and Open Pine habitats were most frequented by pine marten. According to bimonthly food habits data, habitat use seems largely determined by the abundance and availability of their prey items in the available habitat types. Martens may concentrate hunting efforts in areas different from when they are not hunting. The Minorcan pine marten differs from continental populations in its wide use of shrublands, in addition to forests.     

Non-invasive genetic sampling of sympatric marten species (Martes martes and Martes foina): assessing species and individual identification success rates on faecal DNA genotyping

The use of non-invasive genetic sampling (NGS) has become increasingly popular in wildlife research but needs well-planned sampling strategies and reliable laboratory protocols. In this study, we planned to assess the reliability and success of species and individual identifications of sympatric martens (European pine marten Martes martes and stone marten Martes foina) by genotyping non-invasively collected faecal samples. First, we developed a novel and accurate multiplex panel of 15 microsatellite loci, selected by cross species amplification of 41 loci. The application of this panel facilitated species distinction, discarding the presence of putative hybrids. Then, we assessed the impact of sample collector skills on the lab protocol performances. The faecal DNA quality was evaluated by (a) the success of polymerase chain reaction–restriction fragment length polymorphism identification of the two Martes species and (b) the genotyping success and error rates of individual pine marten identifications. The survey was conducted over all the sympatric range of the two species in the Iberian Peninsula by three groups of sample collectors with different experience: expert wildlife biologist, trained volunteers and technical staff from natural parks. Results show that the different expertise between sample collectors significantly influences the success rate of pine marten individual genotyping, but not the species identification success rate. Based on our results, we recommend conducting sampling by experienced field biologist to maximise the quality of NGS and ensure accurate genotyping success. Application of our methods to field collected scats can be used in a cost-effective way to investigate distribution, patterns of genetic diversity and structure as well as to estimate population abundance for sympatric martens.     

Interspecific coprophagia by wild red foxes: DNA metabarcoding reveals a potentially widespread form of commensalism among animals

Vertebrate animals are known to consume other species'' faeces, yet the role of such coprophagy in species dynamics remains unknown, not least due to the methodological challenges of documenting it. In a large‐scale metabarcoding study of red fox and pine marten scats, we document a high occurrence of domestic dog DNA in red fox scats and investigate if it can be attributed to interspecific coprophagia. We tested whether experimental artifacts or other sources of DNA could account for dog DNA, regressed dog occurrence in the diet of fox against that of the fox’s main prey, short‐tailed field voles, and consider whether predation or scavenging could explain the presence of dog DNA. Additionally, we determined the calorific value of dog faeces through calorimetric explosion. The high occurrence of dog DNA in the diet of fox, the timing of its increase, and the negative relationship between dog and the fox''s main prey, point to dog faeces as the source of DNA in fox scats. Dog faeces being highly calorific, we found that foxes, but not pine martens, regularly exploit them, seemingly as an alternative resource to fluctuating prey. Scattered accounts from the literature may suggest that interspecific coprophagia is a potentially frequent and widespread form of interaction among vertebrates. However, further work should address its prevalence in other systems and the implications for ecological communities. Tools such as metabarcoding offer a way forward.     

The feeding ecology of mink (Mustela vison) in coastal habitat

The diet of a coast-living population of mink was investigated from the scats collected over a three-year period, and compared with information on the availability of principal prey species. Lagomorphs were the single most important prey, and predation upon them matched the abundance of rabbits as determined by monthly counts. Aquatic foraging was particularly important, with rockpool-inhabiting fish accounting for 29–1% occurrence of food items. Fish predation was more pronounced during winter months when lagomorph prey was less available. Crustacean prey, particularly the shore crab, Carcinus maenas , occurred frequently in the diet. Seabirds figured regularly in the diet; these were either taken as carrion from the strand-line or through predation on breeding colonies during the summer months.     

Summer food of sympatric red fox and pine marten in the German Alps

Based on fecal analyses, we compared summer diet composition and trophic niche breadth for the sympatric red fox Vulpes vulpes (n=55 scats) and pine marten Martes martes (n=64) in the foothills of the German Alps. Mammals accounted for 41 and 51% of the consumed biomass by pine martens and red foxes, respectively, and no single mammal species exceeded 8% of the diet. The larger red fox consumed a wider range of prey sizes than the smaller pine marten, and both consumed large amounts of plants and also insects. Whereas the Levins index suggested that both predators have specialist feeding niches, the Shannon-Wiener index showed that both predators were relatively generalist. Despite its preliminary nature, our study suggests that a strict distinction between generalist and specialist trophic niches is not justified for medium-sized carnivores in the Alps, particularly as results greatly depend on the indices used.     

Apex predators and the facilitation of resource partitioning among mesopredators

Apex predators may influence carnivore communities through the suppression of competitively dominant mesopredators, however they also provide carrion subsidies that could influence foraging and competition among sympatric mesopredators when small prey is scarce. We assessed coyote Canis latrans and red fox Vulpes vulpes winter diet overlap and composition from scats collected in two study areas with 3‐fold difference in grey wolf Canis lupus density due to a wolf control program. We hypothesized that differences in diet composition would be driven by the use of carrion, and tested whether 1) apex predators facilitate resource overlap, or 2) apex predators facilitate resource partitioning. We estimated the available biomass of snowshoe hares and voles based on pellet density and vole capture rates in each study area. We used molecular analysis to confirm species identification of predator scats, and used microscopic evaluation of prey remains to analyze diet composition of 471 coyote and fox scats. Ungulate carrion, voles and snowshoe hares comprised 73% of coyote and fox diet, and differences in use of carrion and microtines accounted for nearly 60% of the dissimilarity in diet among these canids. Carrion was the top‐ranked item in the coyote diet in both study areas, whereas carrion use by red foxes declined 3‐fold in the study area with higher wolf and small prey abundance. Diet overlap tended to be lower and diet diversity tended to be higher where wolves were more abundant, though these trends were not statistically significant. Taken together, our findings indicate that carrion provisions could facilitate resource partitioning in mesocarnivore communities by alleviating exploitation competition for small mammals.     

Prey choice by marten during a decline in prey abundance

Summary We examined variation in diet choice by marten (Martes americana) among seasons and between sexes and ages from 1980–1985. During this period prey populations crashed simultaneously, except for ruffed grouse (Bonasa umbellus) which was common at the beginning and end of the study, and masked shrews (Sorex cinereus) which were abundant in 1983. Marten were catholic in selection of prey and made use of most available mammalian prey, ruffed grouse, passerine birds, berries, and insects. Diet niche was widest during the latter three years when prey was scare, particularly in late winter. Diet niche breadth was negatively correlated with abundance of all common prey species. Proportion of small prey species in the diet was correlated with absolute abundance of those species, but proportion of some large prey was related to their relative abundance. Diet choice varied among years and among seasons. Berries and insects were common in summer diets while large prey, particularly varying hare (Lepus americanus), were more frequent in winter diet than in summer diet. We found little evidence that any small mammal species was a preferred prey. Sexual size dimorphism between the sexes did not affect prey choice, nor did age. Reduced foraging effort in winter resulted in a wider diet niche only when prey was scarce. The only prediction of optimal foraging models fully supported by our data was a wider diet niche with reduced prey abundance. However, among the three most profitable prey species choice was dependent on the absolute abundance of the most profitable type (varying hare). We suggest that marten primarily forage for large prey but employ a strategy which results in encounters with small prey as well. These small prey are eaten as they provide energy at minimal cost, between captures of large prey.     

Food habits of genetically identified pine marten (<Emphasis Type="Italic">Martes martes</Emphasis>) expanding in agricultural lowlands (NW Italy)

We assessed the diet of pine marten (Martes martes) expanding in the heavily human-altered agricultural plain of the River Po, northern Italy. Between February 2008 and November 2009, surveys were carried out twice a week during seasonal sampling sessions of three to four consecutive weeks. To distinguish the faecal samples from those of sympatric carnivores, a polymerase chain reaction-restriction fragment length polymorphism method was applied. The availability of small mammals was assessed by the analysis of 59 barn owl (Tyto alba) pellets. A total of 109 pine marten faeces were analysed. Its diet consisted of fruit, rodents, lagomorphs and birds. Seasonal variation occurred for fruit, which prevailed in summer, and rodents, which were more preyed upon in autumn. In winter, the diet of the pine marten was almost totally based on vertebrates, and lagomorphs were the main source of protein in summer. Use of small mammals differed significantly from their availability, voles, particularly bank vole Myodes glareolus, being preferred to mice (Apodemus sp.) and rats (Rattus sp.). Medium-size mammals formed about 18% of pine marten diet, a value generally reported for high-latitude habitats. In agricultural areas, the pine marten proved to be an opportunistic predator, able to face the reduced availability of small mammals by preying upon medium-size prey and fruit.     

The diet of the subantarctic fur seal Arctocephalus tropicalis at Marion Island

Scats of subantarctic fur seals Arctocephalus tropicalis at Marion Island were collected from 1996 to 2,000, to examine temporal variability in the diet, factors affecting the variability and how the diet differed from that of the Antarctic fur seal A. gazella in the same period. For A. tropicalis, 19 prey species, of which 18 were fish and one a cephalopod, were identified in 213 scats. Fish were the main prey, occurring in 98.1 % of scats, whereas the cephalopod was present in only 1.4 % of scats. Amongst fish species, Myctophidae were most abundant, with Gymnoscopelus piabilis, G. fraseri and Electrona carlsbergi being the commonest prey items. Other fish families present in the diet in small numbers were Channichthyidae, Paralepididae, Nototheniidae, Microstomatidae and Notosudidae. Fish eaten ranged in size from Protomyctophum bolini and Krefftichthys anderssoni of standard length (SL) 25 mm to a single Dissostichus eleginoides of SL 249 mm. Differences in the diet existed between summer and winter. However, prey type accounted for most variability in the diet. In previous studies based on scats, a dominance of fish in the diet of A. tropicalis was also found at Possession Island (Iles Crozet), Amsterdam Island and Macquarie Island, but the dominant prey species differed between the various localities, also suggesting that prey availability is a major determinant of diet. At Marion Island, from 1996 to 2000 the diet of A. gazella comprised similar prey to that of A. tropicalis, but the proportional contribution of prey types differed in instances.     

Feeding responses of the red fox (<Emphasis Type="Italic">Vulpes vulpes</Emphasis>) to different wild rabbit (<Emphasis Type="Italic">Oryctolagus cuniculus</Emphasis>) densities: a regional approach

We investigate the feeding responses of the red fox (Vulpes vulpes) at a regional scale to different densities of European wild rabbit (Oryctolagus cuniculus) in central–southern Spain. Rabbit abundance indices were obtained in 86 localities during summer 2002. The diet of the fox was studied by analysis of 114 scats collected in 47 of these localities. The feeding response of the fox was examined by a representation of the dry weight percent of rabbit in the diet as a function of the abundance of rabbits; this used data only from those localities where at least 3 scats were collected (70 fox scats from 18 localities). We evaluated the relationship between rabbit abundance and the diversity of the diet of the fox. The feeding patterns of red foxes approximated to Holling’s type III functional response, typical of opportunistic predators. There was a negative relationship between the diversity of the fox’s diet and the abundance of rabbits. Therefore, the fox apparently behaves as a facultative predator, feeding on rabbits when they are abundant and shifting to other prey (and hence a more diverse diet) when rabbits are scarce. These findings are the first step towards understanding the potential role of red foxes in regulating rabbit populations in central–southern Spain.     

Socio-spatial ecology of pine marten (Martes martes) in conifer forests,Ireland

Understanding the social organisation and spacing patterns of wildlife populations is an important aspect of conservation management and applied science. The present study investigated the spatial ecology of pine marten (Martes martes) inhabiting conifer forests in Ireland, the largest habitat resource available for the species. It represented the first study of pine marten spacing patterns in Irish conifer forests. Pine marten (n?=?7; five males and two females) were live-trapped and radio-tracked for between 4 and 10 months from March 2008 to March 2009. Mean annual home-range estimates (95 % fixed kernel) for males (150.7 ha) were generally larger than those of females (90.2 ha). There was considerable inter-seasonal overlap in home ranges (approx 85 %) with less inter-sexual (12.0 %) or intra-sexual (11.8 %) overlap, although the sample size of individuals for comparison was small. Pine marten home ranges were stable from season to season. Core ranges varied in size from 10.6 to 104.1 ha, and as a mean percentage of home-range area were 22.9 and 42.5 % for males and females, respectively. In terms of forest management, potential under occupancy of available space by pine marten and vulnerability of very small core ranges to clear felling practices needs further research to determine any impacts on individuals and populations.