Using genetic techniques to quantify reinvasion,survival and in situ breeding rates during control operations

Determining the origin of individuals caught during a control/eradication programme enables conservation managers to assess the reinvasion rates of their target species and evaluate the level of success of their control methods. We examine how genetic techniques can focus management by distinguishing between hypotheses of ‘reinvasion’ and ‘survivor’, and defining kin groups for invasive stoats (Mustela erminea) on Secretary Island, New Zealand. 205 stoats caught on the island were genotyped at 16 microsatellite loci, along with 40 stoats from the opposing mainland coast, and the age and sex were determined for each individual. Using these data, we compare and combine a variety of genetic techniques including genetic clustering, population assignment and kinship‐based techniques to assess the origin of each stoat. The population history and individual movement could be described in fine detail, with results indicating that both in‐situ survival and breeding, and reinvasion are occurring. Immigration to the island was found to be generally low, apart from in 1 year where around 8 stoats emigrated from the mainland. This increased immigration was probably linked to a stoat population spike on the mainland in that year, caused by a masting event of southern beech forest (Nothofagus sp.) and the subsequent rodent irruption. Our study provides an example of some of the ways genetic analyses can feed directly into informing management practices for invasive species.     

Understanding contributions of cohort effects to growth rates of fluctuating populations

1. Understanding contributions of cohort effects to variation in population growth of fluctuating populations is of great interest in evolutionary biology and may be critical in contributing towards wildlife and conservation management. Cohort-specific contributions to population growth can be evaluated using age-specific matrix models and associated elasticity analyses. 2. We developed age-specific matrix models for naturally fluctuating populations of stoats Mustela erminea in New Zealand beech forests. Dynamics and productivity of stoat populations in this environment are related to the 3-5 year masting cycle of beech trees and consequent effects on the abundance of rodents. 3. The finite rate of increase (lambda) of stoat populations in New Zealand beech forests varied substantially, from 1.98 during seedfall years to 0.58 during post-seedfall years. Predicted mean growth rates for stoat populations in continuous 3-, 4- or 5-year cycles are 0.85, 1.00 and 1.13. The variation in population growth was a consequence of high reproductive success of females during seedfall years combined with low survival and fertility of females of the post-seedfall cohort. 4. Variation in population growth was consistently more sensitive to changes in survival rates both when each matrix was evaluated in isolation and when matrices were linked into cycles. Relative contributions to variation in population growth from survival and fertility, especially in 0-1-year-old stoats, also depend on the year of the cycle and the number of transitional years before a new cycle is initiated. 5. Consequently, management strategies aimed at reducing stoat populations that may be best during one phase of the beech seedfall cycle may not be the most efficient during other phases of the cycle. We suggest that management strategies based on elasticities of vital rates need to consider how population growth rates vary so as to meet appropriate economic and conservation targets.     

Selection of alpine grasslands over beech forest by stoats (

Predation by introduced stoats is now considered a major threat to the population viability of several New Zealand endemic bird species. Historically stoat research and management has focused on beech forests and little is known about the ecology of stoats in the alpine grasslands occurring above the natural altitudinal limit of beech forest. Several stoat control operations in beech forest valley floors in southern New Zealand assume that adjacent montane areas act as a barrier to stoat immigration. Stoats were live-trapped and radio-tracked in alpine grasslands above the Borland Burn, Fiordland National Park, during the summer and autumn of 2003 and 2004. Seventeen stoats were radio-collared and home ranges were estimated for 11 of them. These home ranges were used in a compositional analysis which showed that these stoats spent significantly more time in alpine grassland than in adjacent beech forest. Range cores calculated for six of these stoats were located high up in alpine grassland and contained very little beech forest. This means that montane areas that contain alpine grasslands are unlikely to be barriers to stoat immigration; rather they may be a source of dispersing stoats that reinvade control areas. Also, endemic animal species that inhabit alpine grasslands could be at risk from stoat predation.     

Managing an invasive predator pre-adapted to a pulsed resource: a model of stoat (Mustela erminea) irruptions in New Zealand beech forests

The stoat (Mustela erminea) is a specialist predator that evolved to exploit the unstable populations of northern voles and lemmings. It was introduced to New Zealand, where it is pre-adapted to respond with a population irruption to the resource pulses that follow a heavy seedfall of southern beech (Nothofagus spp.). Culling stoats during an irruption is necessary to reduce damaging predation on nesting endemic birds. Culling might not reduce the stoat population long term, however, if high natural mortality exceeds culling mortality in peak years. During other phases of the beech-mast cycle, culling might have a greater effect on a smaller stoat population, whether or not damage prevention is critical. We developed a 4-matrix model to predict the effects of culling on λ, the annual rate of change in the size of the stoat population, through the four annual phases of an average masting cycle, explicitly distinguishing between apparent and real culling. In the Post-seedfall phase of the cycle, large numbers of stoats are killed, but little of this extra mortality is additive; in other phases, culling removes larger proportions of smaller total numbers of stoats that would otherwise have lived. Culling throughout all phases is most effective at reducing stoat populations, but is also the most expensive option. Culling in Post-seedfall plus Seed or Crash years is somewhat less effective but better than culling in one phase only. Culling has different short-term effects on stoat age distribution depending on the phase of the cycle when culling begins.     

Stoat density, diet and survival compared between alpine grassland and beech forest habitats

In New Zealand, alpine grasslands occur above the treeline of beech forest. Historically stoat control paradigms in New Zealand?s montane natural areas have assumed alpine grassland is a marginal habitat that limits dispersal between beech forest stoat populations. We compared the summer-to-autumn (January?April) density, weight, diet and winter survival of stoats between these two habitatsduring years of low beech seedfall. Stoats were live-trapped, marked and released in alpine grassland and low-altitude beech forest in the Borland Valley, Fiordland National Park, during 2003 and 2004, and were caught and euthanased for necropsy in 2005. Stoat density was estimated using spatially explicit capture?recapture (SECR). The proportion of stoats marked in one year but recaptured in the next was used as a measure of ?observed survival?. Prey remains were identified from scats collected during 2003 and 2004 and stomachs from stoats killed in 2005. Stoat density was similar in both habitats over the two years, about one stoat per square kilometre. Observed survival from 2003?2004 was also similar, but survival from 2004?2005 was higher in alpine grassland than in beech forest. In 2003, male stoats were on average heavier in alpine grassland than in beech forest, although average weights were similar in the other years. Diet differed significantly between the two habitats, with stoats in alpine grasslands eating mainly ground weta (a large invertebrate) (72%) and hares (23%), while stoats in beech forest ate mainly birds (31%) and mice (19%). Collectively these results suggest that alpine grasslands are not a poor quality habitat for stoats. Traditionally it has been thought that stoats cannot survive on invertebrate prey alone. This research demonstrates that stoats relying largely on invertebrate prey can occur at similar densities and with equivalent survival to stoats relying on vertebrate prey.     

Using genetics and Bayesian modelling to evaluate the eradication of stoats (

The New Zealand Department of Conservation recently (May 2008) began a programme to eradicate stoats (Mustela erminea) from Resolution Island (Fiordland, New Zealand) using kill traps. In conjunction with this eradication effort we have the following 3 objectives: (1) to measure the population abundance of stoats prior to trapping using hair tubes and forensic DNA methods; (2) optimise techniques for detecting individual stoats, in order to quantify the probability of stoat persistence given no detections after several months of trapping; and (3) use genetic analyses to identify the possible origins (mainland incursions or in situ breeding) of new stoats captured in a control zone. We present Bayesian modelling techniques used to determine the probability of stoat persistence on the island after the initial population reduction, when individual stoats are no longer captured in traps. We also provide details on an effective level of monitoring and trapping effort required to maintain a comfortable level of confidence that stoats no longer persist on the island. Improving these techniques adds to variety of valuable tools for management of invasive mammal species in a range of natural environments worldwide.     

Large‐scale pest control in New Zealand beech forests

In 2014, baits laced with the poison sodium fluoroacetate (1080) were sown over 694 000 ha of mostly native beech forests in New Zealand to control rats, stoats and possums – a landscape‐scale pest control programme called ‘Battle for our Birds’. This large pest control operation was necessitated by the mast seeding of beech trees which led to irruptions of rodent and stoats which were predicted to lead to decreases in vulnerable native wildlife. In this article, we describe why and how this extensive pest control programme was developed and implemented. We describe the seedfall monitoring that was used to determine the need for large‐scale rodent and stoat control and the response of these predators to this control. We also provide a summary of the bird monitoring that was undertaken to demonstrate the effectiveness or otherwise of the programme.     

Do mallard ducks feature in the diet of stoats in an agricultural landscape?

ABSTRACT

Research on stoat diet composition in New Zealand has primarily focussed on consumption of indigenous fauna in largely unmodified landscapes. This study used stomach content and stable isotope (δ¹³C and δ¹⁵N) analysis to assess stoat diet in a highly modified agricultural landscape in Southland, New Zealand, focussing on stoat predation of the mallard duck. Stoats were captured in Lochiel, Southland during August–November 2016 and 2017. Stomach content analysis of 26 captured stoats revealed limited stoat predation of mallards (n?=?1) and mallard eggs (n?=?1). Using liver tissue, stable isotope mixing models suggested that bird eggs on average met between 73 and 85% of stoat metabolic requirements throughout the mallard breeding period. Furthermore, mixing model outputs suggested that bird eggs made up a substantial proportion (77–84%) of stoat assimilated diet early in the mallard breeding period, when mallard eggs are readily available. In contrast, isotope mixing models suggested that mallard ducks/ducklings did not make a large overall contribution to stoat diets (< 3%). This study shows that stoats are an egg predator in the Southland agricultural landscape and mallard eggs may contribute to stoat assimilated diet early in the mallard breeding season before alternative prey items become available.     

Variation in body size, sexual dimorphism and age-specific survival in stoats, Mustela erminea (Mammalia: Garnivora), with fluctuating food supplies

Most hypotheses attempting to explain the evolution of pronounced sexual dimorphism in body size in the three species of weasels (Mustela erminea, M. frenata, M. nivalis) assume that sexual dimorphism is a long-term adaptation, associated with the different reproductive strategies of the two sexes. We here examine an auxiliary hypothesis which predicts that the degree of sexual dimorphism may also vary over the short-term, because when food is temporarily abundant, sexual selection should favour a greater growth rate of males than of females. This hypothesis concerns a phenotypic response which could introduce temporarily increased variation into an existing genotypic trait. We document the present size and sexual dimorphism of stoats introduced last century to New Zealand from Britain in relation to between-year variation in food supply in a single habitat (forests of southern beech, Nothofagus sp.). Southern beech trees produce heavy crops of flowers and seed at 3–5 year intervals, which are associated with very variable supplies of important prey of stoats, including several species of seed-eating birds, litter-feeding insects, and feral house mice (Mus musculus). Alternative prey are scarce. Regressions of condylobasal length and head-body length on mouse population indices were significant in both sexes. Mean condylobasal length was larger in both male and female stoats born after a heavy seedfall compared with those born in non-seedfall years. However, the largest males born in years of heavy seedfall were removed by selective mortality before the age of 3 years, so the condylobasal lengths for old (≥ 3.0 yr) males converged on a common mean regardless of food supply in their birth year. Sexual dimorphism did not vary with food supplies (as reflected in seedfall records or mouse population indices) at any age. First-year survivorship, at least from the age of independence, was significantly negatively correlated with density of stoats in the summer of their birth year.     

Predicting the incidence of mohua predation from the seedfall,mouse, and predator fluctuations in beech forests

Abstract

Predator control will be required to save many mohua (Mohoua ochrocephala) populations from extinction. However, control may be required only in years when stoat (Mustela erminea) densities are high. To manage local stoat populations effectively, a reliable predictor of high risk years is required. We examined whether different levels of beech seedfall and mouse capture rates were related to the levels of mohua predation recorded in the Hawdon Valley, Arthur's Pass National Park, and the Eglinton Valley, Fiordland National Park, between 1989 and 1994. During this period there was only one full beech mast year in each study area during autumn. The full mast seedfall in Hawdon Valley was predominantly of mountain beech (Nothofagus solandri var. cliffortioides) and red beech (N. fused), and in Eglinton Valley it was predominantly silver beech (TV. menziesii). During the following summer, mouse and stoat densities, and the predation rate of adult mohua, all increased considerably. There was very little predation on adult mohua in the summers following poor seedfalls when mouse and predator densities remained low. In 1993, a partial mast did not trigger a mouse or stoat irruption.

We conclude that counts of beech seedfall and indices of mouse density are potential predictors of an impending irruption of key predators. Winter mouse density appeared to be the most reliable indicator, because neither stoats nor mice respond to seedfall alone. A combination of these indicators could be used as a basis for management decisions on whether to undertake stoat control to protect mohua populations in the future. However, more information is required on the seedfall thresholds that may trigger sufficient increases in mouse and stoat numbers and, consequently, bird predation.     

No evidence of past bottlenecks in two Danish mustelids: results of craniometric and genetic studies in time and space

A craniometric and molecular genetic investigation was conducted in Danish stoat (Mustela erminea) and weasel (Mustela nivalis) populations. Specimens used were collected over a wide time span (stoat: 1864–2002; weasel: 1863–1990) and from several geographical regions (Jutland peninsula and the two islands of Funen and Zealand). The study was made with a temporal and a spatial perspective, allowing the estimation of differences in genetic diversity and craniometrical trait means between geographical regions and through time with the use of ancient DNA techniques. Univariate statistics of 11 trait lengths did not reveal geographical differentiation in size and shape among the different regions for the stoat, but a geographical differentiation in shape was found for the weasel. There was evidence for reductions in skull size with the year of collection in male stoats, but not in females, which suggests that some selective pressures or environmental factors have affected male stoats to a greater extent than female stoats and the weasel. Relatively high values of heterozygosity were found in both the stoat and weasel, using microsatellite markers. The level of genetic variability of the stoat collected recently was compared with the level of genetic variability in the historical samples, demonstrating that the stoat has not suffered severe loss of genetic variability through the investigated period. A comparison of recent and historical genetic variability of the weasel was not possible because the ancient DNA extracted from the weasels was too degraded. Pairwise F_ST values and assignment tests showed small but significant genetic differentiation between the different geographical regions for both the stoat and weasel. No genetic differentiation between the recent and historical samples of the stoat was found. © 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88 , 541–553.     

The stoat Mustela erminea population decline in northern Belarus and its consequences for weasels Mustela nivalis

Abstract

In northern Belarus, we have documented a decline in the local stoat Mustela erminea population following the naturalisation of the American mink Mustela vison. The most likely cause is the reduction in the density and distribution of the main prey of stoats, the riparian voles (the water vole Arvicola terrestris and the root vole Microtus oeconomus), due to excessive predation by mink. Since the stoat population has declined, the number of weasels Mustela nivalis in marshlands has increased and their mean body mass has increased, correlated with the higher number and mean weights of rodents available for weasels in marshland compared with forest habitats.     

The biology of the stoat (Mustela erminea) in the National Parks of New Zealand VI. Infestation with Skrjabingylus nasicola

Abstract

The natural distribution of the parasite Skrjabingylus nasicola was surveyed in 1492 stoats from New Zealand’s National Parks. Infestation was rare in the young, so distribution was expressed as frequency of occurrence of skulls containing nematodes in samples of stoats more than 6 months old. Conservative estimates of incidence ranged from 0 to 37% in 27 local subsamples with at least 6 adults and subadults (mean 10%, n = 1005), sometimes varying substantially across short distances. Incidence was highest in beech forest and scrub/grassland habitats with annual rainfall less than 1600 mm. Subadult males (6–10 months old) were infested as frequently as adult males (older than 10 months), and there was no difference in incidence between the sexes. Worms recovered from 97 infested stoats occurred equally often in either side of the skull; were more often large (i.e., probably female) at all intensities of infestation; and numbered 1–73 per infested stoat (mean 12.9 in females, 14.2 in males; difference not significant). There was no evidence that infested stoats were smaller or lighter than uninfested onces.     

Change in Diet of Stoats Following Poisoning of Rats in a New- Zealand Forest

The abundance and diet of stoats (Mustela erminea) were compared before and after an aerial 1080-poison operation for possums (Trichosurus vulpecula) in a New Zealand podocarp- hardwood forest. Poisoning dramatically reduced ship rat (Rattus rattus) abundance. Although rats were the main prey item of stoats before the poisoning, stoat abundance was unaffected by the operation and there was a change in stoats' diet from rats to birds. The conservation benefits and risks of undertaking such operations are not clear. It is not known whether the predation risk for any particular species of bird (or other animal) will be higher or lower with fewer rats but the same density of stoats. As large-scale poison operations are now common in New Zealand forests, a better understanding of predator-prey relationships in these areas is required as soon as possible.     

The potential for biological control of stoats (Mustela erminea)

Abstract

Accelerating the mortality of stoats (Mustela erminea) using biological agents, or reducing their fertility using chemosterilants or biological agents, are increasingly seen as more sustainable and more humane than trapping and poisoning. Obligate delayed implantation in fertilised female stoats of all ages allows 10–11 months for an applied biological agent or chemosterilant to interfere with gestation. Two chemosterilants (cabergoline and mifepristone) disrupt pregnancy in some species and may be effective on stoats, although they are not species‐specific and are probably more expensive than poisoning. For the longer term, more recent fertility control research has explored potentially more species‐specific options for other species based on inducing an immune response to an animal's own reproductive hormones, gametes, or products from embryos. Conception will be difficult to disrupt in stoats because females are sexually mature and are mated in the nest during a short period before they are weaned. A large research effort will be required to determine which of the immunosterilants being developed could be suitable candidates for stoat control. There are fewer options apparent for using biological agents to increase stoat mortality, although species‐specific strains of canine distemper virus may be effective against stoats.

The greatest impediment to controlling stoat fertility will be effective delivery of sterilants. For the foreseeable future, it will probably be necessary to rely on baits, but they are unlikely to put all target stoats at risk, and will be incapable of delivery over larger scales than at present.

Before undertaking expensive field trials and development of anti‐fertility and biological agents, the effects of putative compensatory changes in demographics that may be associated with changes in stoat density should be modelled to see if the sterilisation and mortality rates that are required to achieve a given level of population control are realistic targets. Also, population control should be defined in terms of accrued benefit for wildlife by establishing the relationships between stoat densities and the viability of prey populations.

Biological control of fertility or mortality may never be suitable as stand‐alone control options for stoats, particularly when some native fauna survive only if stoats are reduced to very low densities. Biological control may have greater potential when integrated with conventional control.     

The biology of the stoat (Mustela erminea) in the National Parks of New Zealand III. Morphometric variation in relation to growth,geographical distribution,and colonisation

Abstract

A total of 1599 stoats were collected from 14 study areas (including all 10 National Parks) from 1972 to 1976. Samples were larger in summer, and contained more females. Young stoats are born in September-October, and females reach adult weight by the following March, though males not until after August. There was significant geographic variation in the body size of adult stoats sampled: males from lowland podocarp/broadleaved forests averaged 3% smaller than males from upland beech forests in skull length, and 4% smaller in head-and-body length. This pattern was repeated, less clearly, in females and in young (approximately 2–5 months old). In contrast with stoats in Britain, assumed to be still the same size as the colonising stock introduced into New Zealand in 1884 and subsequently, males from lowland podocarp forests were unchanged or possibly smaller, and males from upland beech forests were larger; females were larger in all habitats. In males, the extent of geographic variation is almost as great in New Zealand as in the whole of continental Europe. Possible explanations of this pattern are discussed.     

Preference and performance of a gall-inducing sawfly: plant vigor, sex, gall traits and phenology

Four hypotheses regarding the role of predation in the population dynamics of eruptive small mammal communities were tested using the small mammal assemblage found in mixed forests in New Zealand. Large-scale (750 ha) predator removal was conducted, targeting stoats ( Mustela erminea ). House mouse ( Mus musculus ) and ship rat ( Rattus rattus ) population dynamics during an eruption were compared in areas with and without predator reduction. The success of predator reduction was measured by comparing live-capture rates of predators on treatment and non-treatment areas, and by recruitment rates of the threatened northern brown kiwi ( Apteryx australis mantelli ). Overall, predator reduction was successful, although there was a continual low rate of reinvasion. The predictions and results were that 1) Predators can slow but not prevent a population eruption. Supported: Populations of mice and rats erupted to high densities in areas with and without predator reduction, following synchronous southern beech ( Nothofagus spp.) seeding. 2) Predators cannot truncate peak prey population size. Supported: Peak densities of mice and rats were not significantly different between treatment and non-treatment areas. 3) Predators can hasten the rate of decline in prey populations during the crash phase. Not supported: There was evidence of populations of mice and rats declining slower in areas with predators removed, but none of the trends were significant. 4) Predators can limit low-phase prey populations. Equivocal: Populations of rats in beech forest, and population of mice and rats in coastline habitats were significantly higher in areas with predators removed, but were not significantly different in tawa-podocarp forest. Therefore, the role of food in driving the early stages of the mouse and rat eruption was demonstrated, but the role of predation in the decline and low phases is unclear.     

Non-invasive methods for genotyping of stoats (

Stoats (Mustela erminea) are a significant pest in New Zealand. A critical aspect of their management is the ability to identify individuals in order to estimate abundance or to determine the origin of residual animals after control, particularly as the trap-shy nature of stoats reduces the utility of trapping to gain this information. We investigated non-invasive ?capture? methods as an alternative to live-trapping or removal methods for estimating stoat abundance. First we determined whether sufficient variability exists at six microsatellite DNA loci to reliably identify individuals in the potentially bottlenecked, introduced stoat populations of New Zealand. In December 2001 we conducted a 7-night pilot field experiment using a modified hair-tube design, where we obtained a total of 64 hair samples. Sufficient DNA was extracted from 3?6 hair follicles to genotype a total of 51 samples. DNA quality declined if samples were left in the field for several nights before being collected, and daily checks proved best for maximising the quality of DNA obtained, while minimising the risk of multiple ?captures? of stoats. Conclusions were that non-invasive molecular sampling is likely to be a viable technique for estimating population density of stoats in New Zealand beech forest but that additional variable loci are required.     

Losing anti‐predatory behaviour: A cost of translocation

Translocation of endangered species to habitats where exotic predators have been removed is now a common conservation practice around the world. Many of these translocated populations have thrived, and they are often used as sources for the harvesting of individuals for translocations to sites where exotic predators still exist, albeit at reduced densities. This study investigates how isolation from exotic predators affects the ability of individuals to recognize such predators using the North Island robin (Petroica longipes) as a model. The study was carried out in three robin populations in the North Island, New Zealand: a translocated population on Tiritiri Matangi Island, where exotic mammalian predators are absent; a population reintroduced from Tiritiri Matangi Island to Wenderholm Regional Park, a mainland site where these mammals are controlled to low densities; and a mainland population at Benneydale where exotic predatory mammals are common. The response intensity of robins to a model stoat was high at Benneydale and low at Tiritiri Matangi and Wenderholm. This result indicates that isolation from mammalian predators on Tiritiri Matangi has suppressed the ability of North Island robins to recognize these predators. It is possible that the low predatory mammal densities at Wenderholm have reduced robin contact with stoats, therefore reduced the opportunity for robins to learn to recognize stoats. Thus, translocation of individuals from populations without predators to places where key predators still exist could be unsuccessful if translocated individuals fail to perform appropriate anti‐predator behaviours.     

Cohort variation in the life-history parameters of stoatsMustela erminea in relation to fluctuating food resources: a challenge to boreal ecologists

This paper reviews field evidence suggesting that periodic temporary population irruptions of feral house miceMus musculus in New Zealand have a substantial effect on the reproductive success of stoatsMustela erminea Linnaeus, 1758. Stoats born during the summer of a peak in numbers of mice are more numerous and have higher fecundity (ovulation rate) but lower productivity (independent offspring per female) and shorter longevity than those born when mice are not abundant. This reversed silver-spoon effect is apparently correlated with intense competition for food within a much larger than usual cohort of young stoats. However, both stoats and mice are introduced in New Zealand, so it is possible that these effects are not natural. The question could be resolved by data demonstrating similar cohort effects in stoats in the northern hemisphere, living in areas with fluctuating vole populations and limited alternative prey.