Next Article in Journal
Optimal Methods of Documenting Analgesic Efficacy in Neonatal Piglets Undergoing Castration
Next Article in Special Issue
Evaluating the Impact of Wildlife Shelter Management on the Genetic Diversity of Erinaceus europaeus and E. roumanicus in Their Contact Zone
Previous Article in Journal
A Randomized, Placebo-Controlled Clinical Trial of Famciclovir in Shelter Cats with Naturally Occurring Upper Respiratory Tract Disease
Previous Article in Special Issue
DNA Footprints: Using Parasites to Detect Elusive Animals, Proof of Principle in Hedgehogs
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Animals
Volume 10
Issue 9
10.3390/ani10091449
animals-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Over-Winter Survival and Nest Site Selection of the West-European Hedgehog (Erinaceus europaeus) in Arable Dominated Landscapes

by
Lucy E. Bearman-Brown
1,*,
Philip J. Baker
2,
Dawn Scott
3,
Antonio Uzal
4,
Luke Evans
2 and
Richard W. Yarnell
4
1
Department of Animal & Agriculture, Hartpury University, Gloucestershire GL19 3BE, UK
2
School of Biological Sciences, University of Reading, Reading RG6 6AH, UK
3
School of Life Sciences, Keele University, Staffordshire ST5 5BG, UK
4
School of Animal, Rural & Environmental Sciences, Nottingham Trent University, Southwell, Nottinghamshire NG25 0QF, UK
*
Author to whom correspondence should be addressed.
Animals 2020, 10(9), 1449; https://doi.org/10.3390/ani10091449
Submission received: 22 July 2020 / Revised: 12 August 2020 / Accepted: 13 August 2020 / Published: 19 August 2020
(This article belongs to the Special Issue Applied Hedgehog Conservation Research)
Browse Figures
Review Reports Versions Notes

Abstract

:

Simple Summary

Hedgehogs (Erinaceus europaeus) have declined markedly in the UK in recent decades. One key stage that could affect their population dynamics is the annual winter hibernation period. Therefore, we studied two contrasting populations in England to examine patterns of winter nest use, body mass changes and survival during hibernation. On average, animals at both sites weighed the same prior to, and used the same number of nests, during hibernation. There was a marked difference in survival rates between the two sites, but no animals died during hibernation; all deaths occurred prior to or after the hibernation period, mainly from predation or vehicle collisions. Hedgehogs consistently nested in proximity to some habitats (hedgerows, roads, woodlands) but avoided others (pasture fields); the use of other habitats (arable fields, amenity grassland, buildings) varied between the two sites. These data suggest: (i) that hibernation was not a period of significant mortality at either site for individuals that had attained a sufficient weight (>600 g) in autumn; but that (ii) habitat composition did significantly affect the positioning of winter nests, such that different land management practices (historic and current) could influence hibernation success.

Abstract

The West-European hedgehog (Erinaceus europaeus) has declined markedly in the UK. The winter hibernation period may make hedgehogs vulnerable to anthropogenic habitat and climate changes. Therefore, we studied two contrasting populations in England to examine patterns of winter nest use, body mass changes and survival during hibernation. No between-site differences were evident in body mass prior to hibernation nor the number of winter nests used, but significant differences in overwinter mass change and survival were observed. Mass change did not, however, affect survival rates; all deaths occurred prior to or after the hibernation period, mainly from predation or vehicle collisions. Hedgehogs consistently nested in proximity to hedgerows, roads and woodlands, but avoided pasture fields; differences between sites were evident for the selection for or avoidance of arable fields, amenity grassland and buildings. Collectively, these data indicate that hibernation was not a period of significant mortality for individuals that had attained sufficient weight (>600 g) pre-hibernation. Conversely, habitat composition did significantly affect the positioning of winter nests, such that different land management practices (historic and current) might potentially influence hibernation success. The limitations of this study and suggestions for future research are discussed.

1. Introduction

Agricultural intensification and climate alteration are two anthropogenic processes that have profound impacts on natural ecological systems [1,2,3,4,5,6,7]. The effects arise from a wide range of underlying causal factors including: habitat destruction, fragmentation and degradation [8,9]; the introduction of livestock, diseases and non-native biological control agents [10,11,12,13,14]; the management of wildlife where they conflict with human interests [15,16,17,18]; the application of chemical biocides [19]; and changes in the phenology of key biological events [20,21]. Collectively, these factors have led to the decline, extirpation and extinction of large numbers of species [22,23,24,25,26,27], but also increases in the abundance and geographic range of others (e.g., [28,29]).
One group of species that might be expected to be particularly affected by agricultural practices and changing climatic conditions are hibernators [30,31,32,33]. Hibernation has typically evolved to enable species to survive periods of prolonged food shortages by dramatically reducing levels of energy expenditure [34,35]. One consequence of this is that hibernating species tend to have slower reproductive rates [36], potentially increasing their long-term vulnerability to human activities.
The West-European hedgehog (Erinaceus europaeus, hereafter ‘hedgehog’) is a medium-sized (<1.2 kg) insectivorous mammal found from the Iberian Peninsula and Italy northwards into Scandinavia [37]. In Britain, hedgehogs were historically found throughout a broad range of agricultural landscapes [38,39,40,41], but rural populations have declined markedly in recent decades [42,43,44]. Consequently, hedgehogs are now increasingly found within areas of human habitation in this country [45,46,47] and elsewhere [48,49]. Associated with this decline has been a substantial reduction in the availability [50] and quality [51,52,53] of hedgerows, an important habitat for foraging [54], dispersal [55] and refuge [56], and a substantive increase in the numbers of badgers (Meles meles) [57,58], an intra-guild predator [59].
During hibernation, hedgehogs face specific challenges. First, they need to accumulate sufficient fat reserves to survive for a period of many months; in Britain, hedgehogs typically hibernate from October/November to March/April [37], although the exact timing is dependent upon a combination of both temperature and food availability [60]. Second, they need to find enough appropriate building material(s) to construct a hibernaculum that will maintain the environment within the nest at an appropriate temperature; nests are preferentially constructed from the leaves of broadleaved trees [61]. Third, the habitat must be sufficiently diverse that it offers a range of nesting locations in close proximity to one another so that an individual can relocate safely if necessary. In addition, by nesting at ground level, hedgehogs are susceptible to a range of other factors such as flooding, trampling by livestock, and disturbance by e.g., land managers, walkers and domestic dogs (Canis familiaris). Finally, changes in temperature patterns throughout winter may cause hedgehogs to rouse from hibernation when natural food availability is limited.
Hibernation success is, therefore, dependent on several factors, all of which may be negatively affected by agricultural intensification and/or climate change. For example: hot dry summers, soil compaction from heavy machinery and the application of pesticides and molluscicides may all reduce food availability prior to hibernation and, therefore, limit the ability of animals to acquire sufficient fat reserves to successfully complete hibernation; habitat loss and degradation may limit the number of suitable sites for hibernacula, meaning that hedgehogs may be forced to use alternative locations/habitats where preferred nesting materials are not available or where the risk of disturbance is greater; and warmer, wetter and/or more variable winters may cause animals to rouse more often and move between nests more frequently thereby depleting fat reserves and increasing susceptibility to some forms of mortality. Ultimately, such effects would be evident as: reductions in body mass before, and increased mass loss during, hibernation; an increase in the number of winter nests used and their placement in the environment; and an increase in over-winter mortality rates. These parameters would be expected to vary between areas undergoing different types of land management practice, and potentially between sexes (e.g., females may enter hibernation in poorer condition because of the energetic burden of rearing offspring, whilst males may finish hibernating earlier so that they can put on weight before the mating season).
Given the wide range of ways in which human activities could affect this phase, hibernation could represent a key critical period in the dynamics of hedgehog populations [62,63]. Despite its potential importance, little research has been conducted on the hibernation behaviour of hedgehogs in Britain in the last 40 years [37,64]. Therefore, in this study, we radio-tracked hedgehogs at one arable-dominated and one pasture-dominated site in England over the hibernation period to quantify differences in: (i) the number of winter nest sites used; (ii) patterns of habitat selection for nests; (iii) over-winter survival rates; and (iv) over-winter changes in body mass.

2. Materials and Methods

Data were collected from: (1) the Brackenhurst Campus (332 ha) of Nottingham Trent University, Nottinghamshire, UK (National Grid reference: SK695523); and (2) Hartpury University and College campus (339 ha), Gloucestershire, UK (National Grid reference: SO785237). Both sites were mixed commercial farms alongside a university campus, managed under the Entry level Environmental Stewardship Scheme [65]. Brackenhurst is dominated by arable fields (68.7%), with pasture fields, amenity grassland and woodland covering 24.4%, 1.9% and 2.7% of total land area, respectively. In contrast, Hartpury is dominated by pasture (34.8%) and amenity grassland (16.8%), with higher woodland (8.0%) and lower arable (30.8%) coverage than at Brackenhurst. Hedgerow length at each site is 27.1 km (Brackenhurst) and 16.9 km (Hartpury). Badgers were present at both locations: based on the numbers of setts at each site, and the frequency with which they have been photographed on motion activated trail cameras, badger density was considered comparable between the two locations. Hedgehog densities estimated in 2017 using two different methods (random encounter model based on data from trail cameras; spatial capture-recapture based on the capture history of animals along standardized transect routes) were 5.6–9.4 km−2 at Brackenhurst and 4.3–12.5 km−2 at Hartpury [66].
Fieldwork was conducted from August 2015–May 2016 and August 2016–May 2017, inclusive. Hedgehogs were captured by hand at night under licence from Natural England (ref: 20130866-0-0-0-3) using a 1-million candlepower spotlight to systematically search arable fields, pasture fields and areas of amenity grassland. Sites were surveyed at least twice per week during August and September. Once captured, animals were sexed, given a visual health check and weighed using digital scales (Salter 1035 platform scales, Salter, UK). Healthy animals weighing ≥600 g were fitted with a VHF radio transmitter (10 g: <2% of body mass; Biotrack Ltd., Wareham, UK) glued to a region of clipped dorsal spines. All animals, regardless of body mass, were marked with coloured heat shrink tubing attached to 10 dorsal spines in a unique location; tubing was attached using a portable soldering iron. The capture location was recorded with a handheld GPS unit (Garmin GPS 60, Garmin, UK). Animals were released at the point of capture, typically within 15 min.

2.1. Nesting Behaviour

Determining the onset of hibernation for each individual using radio-tracking is difficult. Previous authors have tended to use either a criterion based on the number of successive days a single nest was used, although these have been variable (e.g., seven days [67], one month [68]), or based upon a defined time period [64]. In this study, the latter approach was used as it was not possible to definitively identify the onset of hibernation based upon patterns of nest use alone (see Results) and because it was plausible that hibernating animals may have moved nests following e.g., disturbance by human activities.
Consequently, radio-tracking data were divided into three phases in line with the time periods defined by Yarnell et al. [64]: August–October (pre-hibernation); November–March (hibernation period); and April (post-hibernation). In the pre-hibernation phase, animals were located one night each week to record body mass and check transmitter attachment, and once per week during the day to determine the position of nests. In the hibernation phase, animals were located two-three times each week to determine the position of nests: searches were a minimum of two days apart. Radio-tracking was conducted using a Sika radio-tracking receiver and handheld, three element Yagi antenna (Biotrack).
The location of nests was recorded with a GPS unit and marked with a cane close to the nest for future identification. The position of nests was considered in the context of its specific location (e.g., in an animal burrow, hedgerow, next to or underneath a building) and the surrounding habitats (e.g., gardens, pasture, woodland). Where possible, nests were examined once they had been vacated to identify the dominant and secondary nesting materials. After examination, all nest material was left in position for future use, as hedgehogs have been found to return to nests or to occupy those of other individuals [69].
The number of nests used by each hedgehog was calculated for the time period 1 November–31 March inclusive. Where an individual had not been tracked before 1 November (n = 3) or up to 31 March (n = 3), one extra nest was added to the actual number recorded in line with the pattern of nest use observed for other animals. Differences in the number of nests used by males and females within and between the two sites were analysed using a Kruskal–Wallis test as the data were not normally distributed.
Patterns of habitat selection for winter nests were quantified by comparing the characteristics of observed (used) nest locations with those of randomly selected locations within the area available to hedgehogs. Data for each site were analysed separately. The available area was defined as the minimum convex polygon (MCP) encompassing all the diurnal and nocturnal locations from all hedgehogs radio-tracked during the study period at that site; this was used to incorporate areas outside each individual’s home range [70], and is a more objective reflection of the area used by each hedgehog population collectively than an arbitrarily predefined study area [71]. Available nest locations were randomly sampled (10 times the number of used locations) within the MCP for each study area to create an available versus used dataset. The habitat characteristics of used and available nest locations were obtained by calculating the minimum Euclidian distances to each of the seven main land cover types (amenity grassland, arable fields, buildings and associated hard-standing (hereafter ‘buildings’), hedgerows, pasture fields, roads and road verges (hereafter ‘roads’), woodland) found in both areas. All GIS analyses were carried out using ArcMap 10.3.1 software [72].
Resource Selection Functions (RSFs, [73]) based on generalised linear models for each site were used to quantify habitat selection. A logistic regression for each site was fitted, with the response variable being the used (1: GPS nesting locations) and available locations (0: random location within the MCP area defined above). Collinearity among explanatory variables was assessed using the Pearson correlation coefficient. At Brackenhurst, but not Hartpury, the minimum distances to amenity grassland and buildings were highly correlated (r = 0.7). Therefore, two different RSFs were built: Model A included amenity grassland but not buildings; Model B included buildings but not amenity grassland. Both amenity grassland and buildings were included in the Hartpury model.
Akaike’s Information Criterion (AIC) [74,75] was used for model selection. Parameter values were averaged across models within two AIC units of the best fitting model [74].

2.2. Patterns of Survival

Survival rates were compared between sites using Kaplan–Meier analysis [76]. Sexes and years were combined because of relatively small sample sizes (Brackenhurst n = 10; Hartpury: n = 21), and because there was no apparent difference in the number of males and females that died at each site (see Results). Because animals were captured at different times, a staggered entry [77] design was used: the first animal was captured (Day 1) on 1 August. To avoid potential biases associated with the ad hoc recovery of untagged individuals, only radio-tagged individuals were included in this analysis. Differences in survival between the two sites were quantified using a log-rank test.

2.3. Body Mass Changes

Differences in overwinter changes in mass were compared between sites and sexes using a series of general linear models. Mass loss was calculated using each individual’s mass at capture as close to the start and end of the hibernation period as possible; on average, animals were captured 15.5 days before 1 November and 2.6 days after 31 March. Statistical models compared differences in body mass at the start of hibernation, and mass change and percentage mass change during hibernation. All models included SITE and SEX as fixed factors and included a SEX*SITE interaction term. Linear correlation was also used to compare the number of nest sites used during hibernation with mass change over the hibernation period.

2.4. Data Analysis

General linear modelling and Kruskal–Wallis analyses were conducted using MINITAB version 19.1.1 and SPSS version 25, respectively. Survival analysis and RSF analyses were undertaken in R 3.3.3 [78] using lme4 and MuMIn packages [79,80]. All data were checked to ensure they conformed to the underlying assumptions of the tests used. All results are presented as mean (±SD) unless otherwise specified. As it was not possible to e.g., re-capture all tagged animals or access all nest sites, and because some animals perished during the course of the study, sample sizes vary between analyses.

3. Results

Forty hedgehogs were found during nocturnal surveys: 33 were fitted with radio transmitters (Table 1). Data on nesting behaviour during the hibernation period were collected from 21 hedgehogs. In total, 448 nocturnal locations, 138 nests, and 1028 diurnal locations were recorded.

3.1. Nesting Behaviour

The pattern of nest use was highly variable, with several animals using the same nest site for extended periods before and/or during the hibernation period (Figure 1). There was no significant difference in the number of nests used by males and females within and between the two sites (Kruskal–Wallis test: H = 0.60, DF = 3, p = 0.896). Combining the data, hedgehogs used a median of five nests (mean ± SD = 5.5 ± 2.3) across the 151-day hibernation period. Thirteen animals (62%) used at least one site for ≥89 days.
RSF analyses indicated that woodland, roads, pasture and, to a lesser extent, hedgerows, were consistently included in the top (ΔAIC < 2) ranked models at both sites (Figure 2; Table 2). At both sites, hedgehogs selected nest locations closer to hedgerows, in vegetation alongside roads and in woodlands, but avoided pasture fields (Table 3). Between-site differences were evident for arable fields (neither selected nor avoided at Brackenhurst; avoided at Hartpury) and both amenity grassland and buildings (both selected for at Brackenhurst in each model where these habitats were included; neither selected nor avoided at Hartpury, or not retained in top-ranked models).
At both sites, winter nests were primarily constructed from broad leaves (major component in 45% and 51% of nests, respectively: Supplementary Table S1). Major differences in the relative proportion of nests containing different materials were, however, evident. For example, litter and/or plastic waste was present in 20 nests (24%) at Hartpury, although never as the dominant material, but was never recorded at Brackenhurst.

3.2. Patterns of Survival

Nine animals died during the study, with no apparent sex difference in mortality risk (Brackenhurst: 1♂; Hartpury: 4♀:4♂). The overall survival rate was significantly lower at Hartpury (Log-rank test: Χ21 = 9.46, p = 0.002). All deaths occurred before or after the hibernation period (Figure 3). The most common single known cause of death was predation by badgers (3 of 9 deaths; see Supplementary Table S2).

3.3. Body Mass Changes

Data on body mass changes across the study were available for 21 individuals. There was no significant SITE (F1,17 = 3.75, p = 0.069), SEX (F1,17 = 0.78, p = 0.389) or SITE*SEX (F1,17 = 3.75, p = 0.943) differences in mean body mass at the start of the hibernation period (Supplementary Table S3); collectively, hedgehogs weighed 869 ± 133 g (females: 843 ± 144 g; males: 898 ± 120 g). During hibernation, 16 individuals lost mass (Brackenhurst—5♀:3♂; Hartpury—5♀:3♂), whilst five (Brackenhurst—2♂; Hartpury—1♀:2♂) gained mass. Mass change (F1,17 = 4.65, p = 0.046) but not percentage mass change (F1,17 = 4.22, p = 0.056) differed significantly between the sexes at each site, although the latter was close to significance. At Brackenhurst, females lost 242 ± 150g on average whilst males gained a small amount of weight (4 ± 89 g; Figure 4); male and female hedgehogs at Hartpury lost 117 ± 121 g and 110 ± 141 g, respectively. These figures are equivalent to average percentage mass changes of −25%, +1%, −14% and −15%, respectively (Supplementary Figure S1).
There was a negative correlation between the number of nest sites used and the loss in body mass, although this was not significant (r = −0.409, n = 21, p = 0.066; Figure 5). However, this was dependent on the extreme loss exhibited by a single female at Brackenhurst (432 g); excluding this female, the relationship is significant (r = −0.561, n = 20, p = 0.010).

4. Discussion

In this study, we investigated four factors associated with the winter hibernation period of hedgehogs that could potentially be affected by agricultural land-use and climate change: (i) patterns of body mass change; (ii) frequency of winter nest use; (iii) habitat selection for winter nest sites; and (iv) over-winter survival. Between the two sites studied, one dominated by arable crop production and the other by pasture and amenity grasslands, there were no apparent differences in body mass at the start of hibernation, the number of nest sites used during winter, and the selection for and avoidance of many, but not all, major habitats as nesting locations. In contrast, there were significant differences between the study sites with respect to sex-specific changes in body mass, the use of hedgerows and buildings for nesting, and patterns of survival.

4.1. Change in Body Mass

Estimated body mass of radio-tagged animals at the outset of the hibernation period was not significantly different between Brackenhurst and Hartpury, with animals weighing, on average 869 ± 133 g. This is likely due, in part, to the fact that we only radio-tagged individuals ≥600 g in accordance with guidance relating to the release of rehabilitated hedgehogs by the major wildlife welfare organisation in the UK [81]. This reliance on radio-tagged individuals to ensure that individuals captured before hibernation could be re-captured afterwards does, however, preclude obtaining data on animals below this threshold weight.
Acknowledging this caveat, the general pattern of mass loss observed (mean of 100–240 g within most site-sex divisions, equivalent to a mean of 14–25% of pre-hibernation mass) is within the range recorded in previous studies (Table 4). However, there was a substantial difference in sex-specific patterns of mass change at the two sites. At Hartpury, both males and females lost approximately the same amount of weight (Figure 4). Conversely, females at Brackenhurst lost markedly more weight than any other division, whereas males, on average, gained a small amount of weight. In fact, five (23.8%) animals across both sites gained weight across the hibernation period. This could indicate that individuals may have been able to access sufficient food resources during the winter period to offset the fat reserves used during hibernation, or that some animals may have already stopped hibernating and resumed typical foraging activity before they were recaptured in March/April. Although we are not able to discriminate between these possibilities, it is clear that the magnitude of these average changes are within the survivable range documented for this species.
Mass loss was also negatively correlated with the number of nests used in the winter period (Figure 5), although not significantly (p = 0.066). The lack of significance may, in part, be attributable to the relatively small sample size (n = 21), the highly variable changes in mass recorded, and the presence of one female that lost >400 g (40% of her body mass). Although this is among one of the largest percentage mass losses ever recorded (Table 4) and was >100 g more than any other individual in this study, this individual survived to spring. As rousing from hibernation is energetically expensive [84], hedgehogs would be expected to avoid doing so unnecessarily to avoid depleting their fat reserves. Rousing is likely to occur in response to environmental fluctuations, including both rises or falls in temperature [60], but in anthropogenic landscapes, it may also occur in response to human disturbance. To date, however, there are very few data on the extent to which disturbances affect hedgehog hibernation, either by causing them to move nests or rouse but remain in the same nest [85], and what impacts these may have on energy consumption and mortality risk.

4.2. Nesting Behaviour

Hedgehogs used a median of 5 (mean: 5.5) nests during the 151-day hibernation period. This is markedly higher than that observed in other studies (Table 5). Drawing direct comparisons between the number of nests used in such studies is, however, problematic because of the methodological differences used to define the onset and duration of hibernation, coupled with latitudinal differences in weather and/or temperature which extend or shorten the overall length of the hibernation period. It is worth noting, however, that the mean number of nests used by the animals in this study was more than twice that (1.74 nests per 100 days = 2.6 nests over 151 days) recorded in the most recent study of hedgehogs in England and which utilized the same dates for defining the hibernation period [64].
The increased number of nests used in our study was associated with periods during November, December and/or January where several individuals used a series of nests in quick succession (Figure 1). Although some of these periods of frequent movements between nests could be interpreted as indicating that an individual had not yet started hibernating, the patterns of nest retention exhibited throughout the study as a whole were extremely variable such that it is difficult to identify clear general trends. The possible exception to this is that the majority (62%) of animals used a single nest location for >89 days, with many of these used for the first time in November or December; this is markedly higher than the 21% of nests (n = 167) occupied for ≥3 months reported by Morris [61] in west London.
Clear patterns in nest location were evident for most, but not all, habitats. Hedgehogs consistently avoided nesting near pasture fields, whilst favouring hedgerows, woodlands and roads. In contrast, differing patterns of selection were evident for arable fields, buildings and amenity grassland. At Brackenhurst, nests were preferentially located near to amenity grassland and near buildings, although these habitats were strongly correlated with one another, whereas arable fields were neither selected nor avoided. Conversely, at Hartpury, arable fields were avoided, buildings were neither selected nor avoided and amenity grassland was not retained in the top-ranked models. These data imply that agricultural habitats were generally unsuitable for hibernation, a finding consistent with behaviour outside the hibernation period that has been attributed to a combination of reduced food availability [86] and increased risk of predation from and competition with badgers [44,45,46,47,48,49,59,87].
Hedgerows and woodland were an important habitat for nesting, a pattern that is evident in both summer and winter seasons in other studies [47,68,82,88]. Similarly, the selection for roads in this study is also most probably associated with the presence of hedgerows as borders along roads at both sites. In addition to acting as nesting sites, hedgerows are also recognised as an important refuge habitat whilst foraging where badgers are present [47,56] and for orientation through fragmented landscapes [55]. As such, the general loss and degradation of hedgerows in the UK [50,89,90] is likely to have negatively affected hedgehog populations due to impacts at multiple stages in their annual cycle, although the exact mechanisms are unknown because of the relative paucity of data on rural hedgehog populations and behaviour since the 1950s [91].
Similarly, there are few data on the importance of woodlands for hedgehogs. For example, woodlands were not identified as a factor affecting patterns of occupancy in a national survey of England and Wales [44], they were the least selected habitat in a radio-tracking study in arable landscapes [47], and no hedgehogs were detected in woodland in a pilot project on the Hartpury campus investigating the efficacy of three different methods for surveying hedgehogs [92]: all these studies were, however, conducted in the summer. The preference for woodlands as sites for hibernation observed in this study, and the reliance on broad leaves as nesting material, may suggest that hedgehogs tend to avoid woodlands during the summer months but use them as sites for hibernating during the winter months. As outlined above, one possible reason for these seasonal differences is the presence of badgers, which favour woodlands and plantations as sites for their setts [93] but undergo a period of torpor in winter [94]. Consequently, hedgehogs could be avoiding woodlands during the summer when badgers are active but using them as hibernation sites in the winter when the risk from badgers is markedly lower. As such, woodlands may represent a key resource for hedgehogs but only during one phase of their annual cycle. The impact of historical changes in the coverage of different types of woodland [95,96], their management and their interaction with an increasing badger population [57,58] on hedgehog populations are unknown but require investigation. For example, in their recent report, Mathews et al. [43] estimated that 37% of the British hedgehog population was supported by broadleaved woodland.
The affinity for amenity grassland as a foraging habitat has been well documented in Britain, most notably in the context of responses to the culling of badgers as a means for managing bovine tuberculosis in cattle [45,46,59]. During winter these areas are likely to be associated with low levels of badger activity (due to torpor) but also possibly marginally higher average temperatures than surrounding areas due to their proximity to buildings, and provision of food either accidentally (discarded refuse) or deliberately (although we were not aware of anyone deliberately feeding hedgehogs on either campus). However, amenity areas on university campuses are likely to experience high levels of pedestrian activity except in particularly poor weather and over the Christmas holiday period. The presence of buildings on these two sites also enabled hedgehogs to use some unusual nest locations, including piles of building materials and underground heating tunnels.

4.3. Over-Winter Survival

Survival across the study period as a whole (August–April) was significantly lower at Hartpury versus Brackenhurst. However, this was not associated with differences in mortality during the hibernation period itself, but rather mortality prior to the onset of hibernation and in the period after animals had resumed foraging in spring: in fact, none of the tagged animals in this study (n = 31) died during the hibernation period itself (Figure 3). Consequently, mortalities were not related to body mass per se but stochastic events such as predation by badgers and road traffic accidents (although it could be argued that animals which have not yet accumulated sufficient fat reserves and/or those that leave hibernation having lost a large amount of might be expected to take greater risks when foraging). However, it must be emphasised that these survival data are based on animals that were in good physical condition (visually health-checked and ≥600 g) prior to hibernation in accordance with welfare guidelines; this is substantially higher than the minimum threshold of 450–513 g outlined in Table 4, and which would tend to elevate survival rates.
The survival rate observed at Hartpury, when measured from August to April (approximately 65%), was lower than that recorded in Sweden (57–96%, mean = 71%) over seven years in the 1970s [62], whereas the survival rates at both sites when measured from October to April were comparable to studies from England (83%) Ireland (100%), Denmark (89–90%) and Finland (100%) conducted between 2001 and 2017 [64,67,82,97]. Overall, this body of evidence suggests that, in general terms, the survival rate of animals that have accumulated sufficient fat reserves prior to hibernation is likely to be high, but that site-specific pressures associated with movements in autumn and spring can substantially increase mortality rates [64].

5. Conclusions

This study has identified key similarities and differences in four key parameters associated with the winter hibernation of hedgehogs across two sites associated with different patterns of land management. Most notably, the period of hibernation itself, when hedgehogs are generally inactive within hibernacula, is not associated with high levels of mortality. Conversely, it is the periods before and after entering hibernation that pose significant risks, predominantly from stochastic factors such as badger predation and vehicle collisions. In addition, hedgehogs at both sites consistently avoided nesting in proximity to pastoral fields during winter, but favoured locations near to hedgerows, woodlands and roads. Selection for or avoidance of arable fields, buildings, and amenity grasslands varied between the two sites.
However, this study was associated with several practical limitations. Data could only be reliably collected from radio-tagged individuals and radio-tags can only be fitted to animals weighing ≥600 g for welfare reasons. Radio-tracking is also limited in the extent to which the start and end of the hibernation period (for each individual) can be identified reliably, and the ease with which data on short-term patterns of movement between nests can be collected given that animals are inactive for many successive days. Future studies, therefore, need to consider the use of other technologies, such as GPS tracking devices [98] and animal-mounted bio-loggers [99], to overcome these constraints. In particular, such studies need to focus on: (i) quantifying patterns of survival of animals weighing <600 g; (ii) identifying factors associated with nest movements and whether this affects mass change during hibernation; and (iii) the role of woodlands in the annual cycle of hedgehogs in both arable and pastoral dominated landscapes.

Supplementary Materials

The following are available online at https://www.mdpi.com/2076-2615/10/9/1449/s1, Figure S1: Mean (±SD) (a) body mass (g) at the start of the hibernation season, and (b) percentage mass change during the hibernation period in relation to site and sex (Brackenhurst: n = 5♀:5♂; Hartpury: n = 6♀:5♂), Table S1: Summary of the dominant materials used in winter nest construction at Brackenhurst and Hartpury. Data for 2015–2016 and 2016–2017 combined. Figures in parentheses are the number of nests where the material was recorded as a secondary material. Sample sizes are less than the total number of nests used by study animals as not all nests were accessible, Table S2: Cause of death (n = 9) from a sample of 31 individuals followed over two winter hibernation periods (2015–2016 or 2016–2017), Table S3: General linear models comparing site and sex differences in (a) body mass (g) at the start of the hibernation season, and (b) mass change and (c) percentage mass change during the hibernation period (n = 21).

Author Contributions

Conceptualization, R.W.Y.; methodology, R.W.Y., D.S., A.U., L.E.B.-B., L.E. and P.J.B.; validation, R.W.Y., L.E.B.-B. and P.J.B.; formal analysis, R.W.Y., L.E.B.-B., A.U., L.E. and P.J.B.; investigation, R.W.Y., D.S., A.U. and L.E.B.-B.; resources, R.W.Y., and L.B.B.; data curation, R.W.Y., L.E.B.-B., and P.J.B.; writing—original draft preparation, L.E.B.-B., P.J.B.; writing—review and editing, all authors; visualization, R.W.Y., A.U., L.E., L.E.B.-B., P.B.; supervision, R.W.Y., P.J.B.; project administration, R.WY.; funding acquisition, R.W.Y., D.S., A.U., L.E.B.-B., P.J.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Peoples’ Trust for Endangered Species and British Hedgehog Preservation Society.

Acknowledgments

The authors would like to thank the volunteers who assisted with data collection, the land owners where data collection was undertaken and Vicky Boult who assisted with some GIS mapping. Particular thanks go to our funders; People’s Trust for Endangered Species and British Hedgehog Preservation Society.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

References

  1. Parmesan, C. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 2006, 37, 637–669. [Google Scholar] [CrossRef] [Green Version]
  2. Firbank, L.G.; Petit, S.; Smart, S.; Blain, A.; Fuller, R.J. Assessing the impacts of agricultural intensification on biodiversity: A British perspective. Philos. Trans. R. Soc. B Biol. Sci. 2008, 363, 777–787. [Google Scholar] [CrossRef]
  3. Tscharntke, T.; Clough, Y.; Wanger, T.C.; Jackson, L.; Motzke, I.; Perfecto, I.; Vandermeer, J.; Whitbread, A. Global food security, biodiversity conservation and the future of agricultural intensification. Biol. Conserv. 2012, 151, 53–59. [Google Scholar] [CrossRef]
  4. Tuck, S.L.; Winqvist, C.; Mota, F.; Ahnström, J.; Turnbull, L.A.; Bengtsson, J. Land-use intensity and the effects of organic farming on biodiversity: A hierarchical meta-analysis. J. Appl. Ecol. 2014, 51, 746–755. [Google Scholar] [CrossRef]
  5. Veach, V.; Moilanen, A.; Di Minin, E. Threats from urban expansion, agricultural transformation and forest loss on global conservation priority areas. PLoS ONE 2017, 12, 1–14. [Google Scholar] [CrossRef] [PubMed]
  6. Zabel, F.; Delzeit, R.; Schneider, J.M.; Seppelt, R.; Mauser, W.; Václavík, T. Global impacts of future cropland expansion and intensification on agricultural markets and biodiversity. Nat. Commun. 2019, 10, 1–10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  7. Firbank, L.G.; Attwood, S.; Eory, V.; Gadanaski, Y.; Lynch, J.M.; Sonnino, R.; Takahashi, T. Grand challenges in sustainable intensification and ecosystem services. Front. Sustain. Food Syst. 2018, 2, 7. [Google Scholar] [CrossRef] [Green Version]
  8. Ellis, E.C.; Goldewijk, K.K.; Siebert, S.; Lightman, D.; Ramankutty, N. Anthropogenic transformation of the biomes, 1700 to 2000. Glob. Ecol. Biogeogr. 2010, 19, 589–606. [Google Scholar] [CrossRef]
  9. Crooks, K.R.; Burdett, C.L.; Theobald, D.M.; Rondinini, C.; Boitani, L. Global patterns of fragmentation and connectivity of mammalian carnivore habitat. Philos. Trans. R. Soc. B Biol. Sci. 2011, 366, 2642–2651. [Google Scholar] [CrossRef]
  10. Robinson, T.P.; Wint, G.R.; Conchedda, G.; Van Boeckel, T.P.; Ercoli, V.; Palamara, E.; Cinardi, G.; D’Aietti, L.; Hay, S.I.; Gilbert, M. Mapping the global distribution of livestock. PLoS ONE 2014, 9. [Google Scholar] [CrossRef] [Green Version]
  11. Wiethoelter, A.K.; Beltrán-Alcrudo, D.; Kock, R.; Mor, S.M. Global trends in infectious diseases at the wildlife-livestock interface. Proc. Natl. Acad. Sci. USA 2015, 112, 9662–9667. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  12. Gordon, I.J. Review: Livestock production increasingly influences wildlife across the globe. Animal 2018, 12, S372–S382. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. Howell, H.J.; Mothes, C.C.; Clements, S.L.; Catania, S.V.; Rothermel, B.B.; Searcy, C.A. Amphibian responses to livestock use of wetlands: New empirical data and a global review. Ecol. Appl. 2019, 29, 1–15. [Google Scholar] [CrossRef] [PubMed]
  14. Öllerer, K.; Varga, A.; Kirby, K.; Demeter, L.; Biró, M.; Bölöni, J.; Molnár, Z. Beyond the obvious impact of domestic livestock grazing on temperate forest vegetation—A global review. Biol. Conserv. 2019, 237, 209–219. [Google Scholar] [CrossRef] [Green Version]
  15. Baker, P.J.; Boitani, L.; Harris, S.; Saunders, G.; White, P.C.L. Terrestrial carnivores and human food production: Impact and management. Mamm. Rev. 2008, 38, 123–166. [Google Scholar] [CrossRef]
  16. Eklund, A.; López-Bao, J.V.; Tourani, M.; Chapron, G.; Frank, J. Limited evidence on the effectiveness of interventions to reduce livestock predation by large carnivores. Sci. Rep. 2017, 7, 1–9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  17. van Eeden, L.M.; Eklund, A.; Miller, J.R.B.; López-Bao, J.V.; Chapron, G.; Cejtin, M.R.; Crowther, M.S.; Dickman, C.R.; Frank, J.; Krofel, M.; et al. Carnivore conservation needs evidence-based livestock protection. PLoS Biol. 2018, 16, 1–8. [Google Scholar] [CrossRef]
  18. van Eeden, L.M.; Crowther, M.S.; Dickman, C.R.; Macdonald, D.W.; Ripple, W.J.; Ritchie, E.G.; Newsome, T.M. Managing conflict between large carnivores and livestock. Conserv. Biol. 2018, 32, 26–34. [Google Scholar] [CrossRef]
  19. Garcês, A.; Pires, I.; Rodrigues, P. Teratological effects of pesticides in vertebrates: A review. J. Environ. Sci. Heal.Part. B Pestic. Food Contam. Agric. Wastes 2020, 55, 75–89. [Google Scholar] [CrossRef]
  20. Brown, D.D.; Kays, R.; Wikelski, M.; Wilson, R.; Klimley, A. Observing the unwatchable through acceleration logging of animal behavior. Anim. Biotelemetry 2013, 1. [Google Scholar] [CrossRef] [Green Version]
  21. Kharouba, H.M.; Ehrlén, J.; Gelman, A.; Bolmgren, K.; Allen, J.M.; Travers, S.E.; Wolkovich, E.M. Global shifts in the phenological synchrony of species interactions over recent decades. Proc. Natl. Acad. Sci. USA 2018, 115, 5211–5216. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Butchart, S.H.M.; Walpole, M.; Collen, B.; van Strien, A.; Scharlemann, J.P.W.; Almond, R.E.A.; Baillie, J.E.M.; Bomhard, B.; Brown, C.; Bruno, J.; et al. Global Biodiversity: Indicators of recent declines. Science 2010, 1164, 1164–1169. [Google Scholar] [CrossRef] [PubMed]
  23. Hoffmann, M.; Hilton-Taylor, C.; Angulo, A.; Böhm, M.; Brooks, T.M.; Butchart, S.H.M.; Carpenter, K.E.; Chanson, J.; Collen, B.; Cox, N.A.; et al. The impact of conservation on the status of the world’s vertebrates. Science 2010, 330, 1503–1509. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Di Marco, M.; Boitani, L.; Mallon, D.; Hoffmann, M.; Iacucci, A.; Meijaard, E.; Visconti, P.; Schipper, J.; Rondinini, C. A Retrospective evaluation of the global decline of carnivores and ungulates. Conserv. Biol. 2014, 28, 1109–1118. [Google Scholar] [CrossRef] [PubMed]
  25. Maxwell, S.L.; Fuller, R.A.; Brooks, T.M.; Watson, J.E.M. Biodiversity: The ravages of guns, nets and bulldozers. Nature 2016, 536, 143–145. [Google Scholar] [CrossRef]
  26. Dudley, N.; Alexander, S. Agriculture and biodiversity: A review. Biodiversity 2017, 18, 45–49. [Google Scholar] [CrossRef]
  27. Stanton, R.L.; Morrissey, C.A.; Clark, R.G. Analysis of trends and agricultural drivers of farmland bird declines in North America: A review. Agric. Ecosyst. Environ. 2018, 254, 244–254. [Google Scholar] [CrossRef]
  28. Clout, M.N.; Russell, J.C. The invasion ecology of mammals: A global perspective. Wildl. Res. 2007, 35, 180–184. [Google Scholar] [CrossRef] [Green Version]
  29. Long, J.L. Introduced Mammals of the World: Their History, Distribution and Influence; CSIRO Publishing: Victoria, Australia, 2003. [Google Scholar]
  30. Inouye, D.W.; Barr, B.; Armitage, K.B.; Inouye, B.D. Climate change is affecting altitudinal migrants and hibernating species. Proc. Natl. Acad. Sci. USA 2000, 97, 1630–1633. [Google Scholar] [CrossRef] [Green Version]
  31. Lane, J.E. Evolutionary Ecology of Mammalian Hibernation Phenology. In Living in a Seasonal World; Ruf, T., Bieber, C., Arnold, W., Millesi, E., Eds.; Springer: Berlin, Germany, 2012; pp. 51–61. ISBN 9783642286780. [Google Scholar]
  32. Lane, J.E.; Kruuk, L.E.B.; Charmantier, A.; Murie, J.O.; Dobson, F.S. Delayed phenology and reduced fitness associated with climate change in a wild hibernator. Nature 2012, 489, 554–557. [Google Scholar] [CrossRef]
  33. Geiser, F. Hibernation. Curr. Biol. 2013, 23, 188–193. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. Geiser, F. Hibernation: Endotherms. eLS 2011, 1. [Google Scholar] [CrossRef]
  35. Staples, J.F. Metabolic suppression in mammalian hibernation: The role of mitochondria. J. Exp. Biol. 2014, 217, 2032–2036. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Turbill, C.; Bieber, C.; Ruf, T. Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proc. R. Soc. B Biol. Sci. 2011, 278, 3355–3363. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  37. Morris, P.A.; Reeve, N.J. Hedgehog Erinaceus europaeus. In Mammals of the British Isles: Handbook; Harris, S.J., Yalden, D.W., Eds.; The Mammal Society: Southampton, UK, 2008; pp. 241–249. [Google Scholar]
  38. Burton, M. The Hedgehog; Andre Deutsch: London, UK, 1969. [Google Scholar]
  39. Tapper, S.S. Game Heritage: An Ecological Review from Shooting and Gamekeeping Records; Game Conservancy Ltd.: Fordingbridge, Hampshire, UK, 1992. [Google Scholar]
  40. Arnold, H.R. Atlas of Mammals of Britain; HMSO: London, UK, 1993. [Google Scholar]
  41. Lovegrove, R. Silent Fields: The Long Decline of a Nation’s Wildlife; Oxford University Press: Oxford, UK, 2007. [Google Scholar]
  42. Hof, A.R.; Bright, P.W. Quantifying the long-term decline of the West European hedgehog in England by subsampling citizen-science datasets. Eur. J. Wildl. Res. 2016, 62, 407–413. [Google Scholar] [CrossRef]
  43. Mathews, F.; Kubasiewicz, L.M.; Gurnell, J.; Harrower, C.A.; McDonald, R.A.; Shore, R.F. A Review of the Population and Conservation Status of British Mammals. A report by the Mammal. Society under contract to Natural England, Natural Resources Wales and Scottish Natural Heritage; Natural England: Peterborough, UK, 2018; ISBN 9781783544943. [Google Scholar]
  44. Williams, B.M.; Baker, P.J.; Thomas, E.; Wilson, G.J.; Judge, J.; Yarnell, R.W. Reduced occupancy of hedgehogs (Erinaceus europaeus) in rural England and Wales: The influence of habitat and an asymmetric intra-guild predator. Sci. Rep. 2018, 8, 12156. [Google Scholar] [CrossRef]
  45. Young, R.P.; Davison, J.; Trewby, I.D.; Wilson, G.J.; Delahay, R.J.; Doncaster, C.P. Abundance of hedgehogs (Erinaceus europaeus) in relation to the density and distribution of badgers (Meles meles). J. Zool. 2006, 269, 349–356. [Google Scholar] [CrossRef]
  46. Parrott, D.; Etherington, T.R.; Dendy, J. A geographically extensive survey of hedgehogs (Erinaceus europaeus) in England. Eur. J. Wildl. Res. 2014, 60, 399–403. [Google Scholar] [CrossRef]
  47. Pettett, C.E.; Moorhouse, T.P.; Johnson, P.J.; Macdonald, D.W. Factors affecting hedgehog (Erinaceus europaeus) attraction to rural villages in arable landscapes. Eur. J. Wildl. Res. 2017, 63, 54. [Google Scholar] [CrossRef] [Green Version]
  48. Hubert, P.; Julliard, R.; Biagianti, S.; Poulle, M.L. Ecological factors driving the higher hedgehog (Erinaceus europeaus) density in an urban area compared to the adjacent rural area. Landsc. Urban. Plan. 2011, 103, 34–43. [Google Scholar] [CrossRef]
  49. Van de Poel, J.L.; Dekker, J.; Langevelde, F.V. Dutch hedgehogs Erinaceus europaeus are nowadays mainly found in urban areas, possibly due to the negative effects of badgers Meles meles. Wildl. Biol. 2015, 21, 51–55. [Google Scholar] [CrossRef]
  50. Robinson, R.A.; Sutherland, W.J. Post-war changes in arable farming and biodiversity in Great Britain. J. Appl. Ecol. 2002, 39, 157–176. [Google Scholar] [CrossRef] [Green Version]
  51. Carey, P.D.; Wallis, S.M.; Emmett, B.; Maskell, L.C.; Murphy, J.; Norton, L.R.; Simpson, I.C.; Smart, S.M. Countryside Survey: UK Headline Messages from 2007; Centre for Ecology & Hydrology: Wallingford, UK, 2008. [Google Scholar]
  52. Wright, J. A Natural History of the Hedgerow and Ditches, Dykes and Dry Stone Walls; Profile Books Ltd.: London, UK, 2016. [Google Scholar]
  53. Dover, J.W. The Ecology of Hedgerows and Field Margins; Routledge: Abingdon, UK, 2019. [Google Scholar]
  54. Hof, A.R.; Bright, P.W. The value of agri-environment schemes for macro-invertebrate feeders: Hedgehogs on arable farms in Britain. Anim. Conserv. 2010, 13, 467–473. [Google Scholar] [CrossRef]
  55. Moorhouse, T.P.; Palmer, S.C.F.; Travis, J.M.J.; Macdonald, D.W. Hugging the hedges: Might agri-environment manipulations affect landscape permeability for hedgehogs? Biol. Conserv. 2014, 176, 109–116. [Google Scholar] [CrossRef]
  56. Hof, A.R.; Snellenberg, J.; Bright, P.W. Food or fear? Predation risk mediates edge refuging in an insectivorous mammal. Anim. Behav. 2012, 83, 1099–1106. [Google Scholar] [CrossRef]
  57. Judge, J.; Wilson, G.J.; Macarthur, R.; Delahay, R.J.; McDonald, R.A. Density and abundance of badger social groups in England and Wales in 2011-2013. Sci. Rep. 2014, 4, 3809. [Google Scholar] [CrossRef] [Green Version]
  58. Judge, J.; Wilson, G.J.; Macarthur, R.; McDonald, R.A.; Delahay, R.J. Abundance of badgers (Meles meles) in England and Wales. Sci. Rep. 2017, 7, 276. [Google Scholar] [CrossRef]
  59. Trewby, I.D.; Young, R.P.; McDonald, R.A.; Wilson, G.J.; Davison, J.; Walker, N.; Robertson, P.A.; Doncaster, C.P.; Delahay, R.J. Impacts of removing badgers on localised counts of hedgehogs. PLoS ONE 2014, 9, 2–5. [Google Scholar] [CrossRef]
  60. Morris, P.A. Hedgehog; HarperCollins: London, UK, 2018. [Google Scholar]
  61. Morris, P.A. Winter nests of the hedgehog. Oecologia 1973, 11, 299–313. [Google Scholar] [CrossRef]
  62. Kristiansson, H. Population variables and causes of mortality in a hedgehog (Erinaceus europaeus) population in Southern Sweden. J. Zool. 1990, 220, 391–404. [Google Scholar] [CrossRef]
  63. Morris, P.A. An estimate of the minimum body weight necessary for hedgehogs (Erinaceus europaeus) to survive hibernation. J. Zool. 1984, 203, 291–294. [Google Scholar]
  64. Yarnell, R.W.; Surgey, J.; Grogan, A.; Thompson, R.; Davies, K.; Kimbrough, C.; Scott, D.M. Should rehabilitated hedgehogs be released in winter? A comparison of survival, nest use and weight change in wild and rescued animals. Eur. J. Wildl. Res. 2019, 65. [Google Scholar] [CrossRef] [Green Version]
  65. Natural England Entry Level Stewardship; Natural England: Sheffield, UK, 2013; ISBN 978-1-84754-239-7.
  66. Schaus, J.; Uzal, A.; Gentle, L.K.; Baker, P.J.; Bearman-Brown, L.; Bullion, S.; Gazzard, A.; Lockwood, H.; North, A.; Reader, T.; et al. Application of the Random Encounter Model in citizen science projects to monitor animal densities. Remote Sens. Ecol. Conserv. 2020. [Google Scholar] [CrossRef] [Green Version]
  67. Haigh, A.; O’Riordan, R.M.; Butler, F. Nesting behaviour and seasonal body mass changes in a rural Irish population of the Western hedgehog (Erinaceus europaeus). Acta Theriol. 2012, 57, 321–331. [Google Scholar] [CrossRef]
  68. Rautio, A.; Valtonen, A.; Auttila, M.; Kunnasranta, M. Nesting patterns of European hedgehogs (Erinaceus europaeus) under northern conditions. Acta Theriol. 2014, 59, 173–181. [Google Scholar] [CrossRef]
  69. Morris, P.A. Hedgehogs, 4th ed.; Whittet Books: Stansted, UK, 2014. [Google Scholar]
  70. McClean, S.A.; Rumble, M.A.; King, R.M.; Baker, W.L. Evaluation of Resource Selection Methods with Different Definitions of Availability. J. Wildl. Manag. 1998, 62, 793. [Google Scholar] [CrossRef]
  71. Uzal, A.; Walls, S.; Stillman, R.A.; Diaz, A. Sika deer distribution and habitat selection: The influence of the availability and distribution of food, cover, and threats. Eur. J. Wildl. Res. 2013, 59, 563–572. [Google Scholar] [CrossRef]
  72. Environmental Systems Resource Institute. ArcGIS 2015; ESRI: Redlands, CA, USA, 2015. [Google Scholar]
  73. Manly, B.F.L.; McDonald, L.; Thomas, D.L.; McDonald, T.L.; Erickson, W.P. Resource Selection by Animals: Statistical Design and Analysis for Field Studies; Springer: London, UK, 2007. [Google Scholar]
  74. Burnham, K.P.; Anderson, D.R. Model. Selection and Multi-Model Inference: A Practical Information-Theoretic Approach; Springer: New York City, NY, USA, 2002. [Google Scholar]
  75. Zuur, A.F.; Ieno, E.N.; Walker, N.; Saveliev, A.A.; Smith, G.M. Mixed Effects Models and Extensions in Ecology with R; Springer Science & Business Media: London, UK, 2009. [Google Scholar]
  76. Kaplan, E.L.; Meier, P. Nonparametric estimation from incomplete observations. J. Am. Stat. Assoc. 1958, 53, 457. [Google Scholar] [CrossRef]
  77. Pollock, K.H.; Winterstein, S.R.; Bunck, C.M.; Curtis, P.D. Survival analysis in telemetry studies: The staggered entry design. J. Wildl. Manage. 1989, 53, 7–15. [Google Scholar] [CrossRef]
  78. R Core Team. R: A Language and Environment for Statistical Computing; R Core Team R: Vienna, Austria, 2016. [Google Scholar]
  79. Bates, D.; Machler, M.; Bolker, B.; Walker, S. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Softw. 2015, 67, 1–48. [Google Scholar] [CrossRef]
  80. Barton, K. Package “MuMIn”; R Package Version 1(6); CRAN: 2019. Available online: https://cran.r-project.org/web/packages/MuMIn/MuMIn.pdf (accessed on 19 August 2020).
  81. RSPCA. RSPCA Wildlife Rehabilitation Protocol: Hedgehogs; RSPCA: Southwater, UK, 2013. [Google Scholar]
  82. Jensen, A.B. Overwintering of European hedgehogs Erinaceus europaeus in a Danish rural area. Acta Theriol. 2004, 49, 145–155. [Google Scholar] [CrossRef]
  83. Rasmussen, S.L.; Berg, T.B.; Dabelsteen, T.; Jones, O.R. The ecology of suburban juvenile European hedgehogs (Erinaceus europaeus) in Denmark. Ecol. Evol. 2019, 9, 13174–13187. [Google Scholar] [CrossRef] [Green Version]
  84. Tähti, H.; Soivio, A. Respiratory and circulatory differences between induced and spontaneous arousals in hibernating hedgehogs (Erinaceus europaeus L.). Ann. Zool. Fenn. 1977, 14, 198–203. [Google Scholar]
  85. Walhovd, H. Partial arousals from hibernation in hedgehogs in outdoor hibernacula. Oecologia 1979, 153, 141–153. [Google Scholar] [CrossRef]
  86. Hof, A.R.; Bright, P.W. The impact of grassy field margins on macro-invertebrate abundance in adjacent arable fields. Agric. Ecosyst. Environ. 2010, 139, 280–283. [Google Scholar] [CrossRef]
  87. Pettett, C.E.; Johnson, P.J.; Moorhouse, T.P.; Hambly, C.; Speakman, J.R.; Macdonald, D.W. Daily energy expenditure in the face of predation: Hedgehog energetics in rural landscapes. J. Exp. Biol. 2017, 220, 460–468. [Google Scholar] [CrossRef] [Green Version]
  88. Riber, A. Habitat use and behaviour of European hedgehog Erinaceus europaeus in a Danish rural area. Acta Theriol. 2006, 51, 363–371. [Google Scholar] [CrossRef]
  89. Sutherland, W.J.; Armstrong-Brown, S.; Armsworth, P.R.; Brereton, T.; Brickland, J.; Campbell, C.D.; Chamberlain, D.E.; Cooke, A.I.; Dulvy, N.K.; Dusic, N.R.; et al. The identification of 100 ecological questions of high policy relevance in the UK. J. Appl. Ecol. 2006, 43, 617–627. [Google Scholar] [CrossRef]
  90. Cornulier, T.; Robinson, R.A.; Elston, D.; Lambin, X.; Sutherland, W.J.; Benton, T.G. Bayesian reconstitution of environmental change from disparate historical records: Hedgerow loss and farmland bird declines. Methods Ecol. Evol. 2011, 2, 86–94. [Google Scholar] [CrossRef]
  91. Harris, S.J.; Morris, P.A.; Wray, S.; Yalden, D.W. A Review of British Mammals: Population Estimates and Conservation Status of British Mammals Other than Cetaceans; JNCC: Peterborough, UK, 1995; ISBN 1-873701-68-3. [Google Scholar]
  92. Bearman-Brown, L.E.; Wilson, L.E.; Evans, L.; Baker, P.J. Comparing non-invasive surveying techniques for elusive, nocturnal mammals: A case study of the West European hedgehog (Erinaceus europaeus). J. Vertebr. Biol. in press.
  93. Wilson, G.; Harris, S.J.; McLaren, G. Changes in the British Badger Population, 1988 to 1997; Kerenza J Ltd.: London, UK, 1997. [Google Scholar]
  94. Roper, T.J. Badger; HarperCollins: London, UK, 2010. [Google Scholar]
  95. Hopkins, J.J.; Kirby, K.J. Ecological change in British broadleaved woodland since 1947. Ibis 2007, 149, 29–40. [Google Scholar] [CrossRef]
  96. Amar, A.; Smith, K.W.; Butler, S.; Lindsell, J.A.; Hewson, C.M.; Fuller, R.J.; Charman, E.C. Recent patterns of change in vegetation structure and tree composition of British broadleaved woodland: Evidence from large-scale surveys. Forestry 2010, 83, 345–356. [Google Scholar] [CrossRef] [Green Version]
  97. Rautio, A.; Valtonen, A.; Kunnasranta, M. The effects of sex and season on home range in European hedgehogs at the northern edge of the species range. Ann. Zool. Fenn. 2013, 50, 107–123. [Google Scholar] [CrossRef]
  98. Glasby, L.; Yarnell, R.W. Evaluation of the performance and accuracy of Global Positioning System bug transmitters deployed on a small mammal. Eur. J. Wildl. Res. 2013, 59, 915–919. [Google Scholar] [CrossRef]
  99. Chmura, H.E.; Glass, T.W.; Williams, C.T. Biologging physiological and ecological responses to climatic variation: New tools for the climate change era. Front. Ecol. Evol. 2018, 6. [Google Scholar] [CrossRef] [Green Version]
Animals 10 01449 g001 550
Figure 1. Pattern of occupation of winter nests by hedgehogs at Brackenhurst (ID numbers prefixed by “B”) and Hartpury (ID numbers prefixed by “H”). Figures in horizontal bars indicate the number of days that each nest was estimated to be occupied based upon the sampling regime (see text for details). Vertical blue columns indicate the start (1 November) and end (31 March) of the hibernation period: dark and light shaded bars indicate nests excluded from and included in the analysis of the number of nests used over the hibernation period, respectively.
Figure 1. Pattern of occupation of winter nests by hedgehogs at Brackenhurst (ID numbers prefixed by “B”) and Hartpury (ID numbers prefixed by “H”). Figures in horizontal bars indicate the number of days that each nest was estimated to be occupied based upon the sampling regime (see text for details). Vertical blue columns indicate the start (1 November) and end (31 March) of the hibernation period: dark and light shaded bars indicate nests excluded from and included in the analysis of the number of nests used over the hibernation period, respectively.
Animals 10 01449 g001
Animals 10 01449 g002 550
Figure 2. Position of hedgehog winter nest sites (blue dots) at (a) Brackenhurst and (b) Hartpury in relation to habitat composition.
Figure 2. Position of hedgehog winter nest sites (blue dots) at (a) Brackenhurst and (b) Hartpury in relation to habitat composition.
Animals 10 01449 g002
Animals 10 01449 g003 550
Figure 3. Kaplan–Meir survival functions for hedgehogs at Brackenhurst (n = 10) versus Hartpury (n = 21). Data from sexes and years (2015–2016 and 2016–2017) combined. Vertical blue lines indicate the start (1 November ) and end (31 March ) of the hibernation period.
Figure 3. Kaplan–Meir survival functions for hedgehogs at Brackenhurst (n = 10) versus Hartpury (n = 21). Data from sexes and years (2015–2016 and 2016–2017) combined. Vertical blue lines indicate the start (1 November ) and end (31 March ) of the hibernation period.
Animals 10 01449 g003
Animals 10 01449 g004 550
Figure 4. Mean (±SD) mass change during the hibernation period (1 November–31 March) in relation to site and sex (Brackenhurst: n = 5♀:5♂; Hartpury: n = 6♀:5♂).
Figure 4. Mean (±SD) mass change during the hibernation period (1 November–31 March) in relation to site and sex (Brackenhurst: n = 5♀:5♂; Hartpury: n = 6♀:5♂).
Animals 10 01449 g004
Animals 10 01449 g005 550
Figure 5. Relationship between number of nests used during the hibernation period (1 November –31 March) and the corresponding change in mass (g) over the hibernation period (n = 21).
Figure 5. Relationship between number of nests used during the hibernation period (1 November –31 March) and the corresponding change in mass (g) over the hibernation period (n = 21).
Animals 10 01449 g005
Table
Table 1. Number of hedgehogs captured and radio-tagged at each site, the total number of nocturnal and diurnal locations recorded, and the number of nest sites identified.
Table 1. Number of hedgehogs captured and radio-tagged at each site, the total number of nocturnal and diurnal locations recorded, and the number of nest sites identified.
BrackenhurstHartpuryTotal
2015–20162016–20172015–20162016–2017
No. captured & marked7 (4♀:3♂)3 (2♀:1♂)22 (12♀:10♂)8 (3♀: 5♂)40 (21♀:19♂)
No. radio-tagged7 (4♀:3♂)3 (2♀:1♂)18 (9♀:9♂)5 (3♀:2♂)33 (18♀:15♂)
No. tracked during hibernation7 (4♀:3♂)3 (2♀:1♂)7 (4♀:3♂)4 (2♀:2♂)21 (12♀:9♂)
Total no. of nests recorded (% accessible for recording composition)54 (59%)12 (100%)50 (66%)16 (75%)138 (65%)
No. of nocturnal locations recorded1037421061448
No. of diurnal locations recorded4081143601461028
Table
Table 2. Results of the top five a-priori models for predictors of habitat selection of hedgehog winter nests. Models are ranked based on their AIC values. Null model is also provided for comparison. Models indicated in bold were selected to build average models. Brackenhurst had two alternative maximal models, one including distance to amenity grassland (Brackenhurst Model A) and another including distance to buildings (Brackenhurst Model B). Habitats included in each of the top-ranking models are indicated by the “✓” symbol. Bold indicates top ranked models at each site (ΔAIC < 2).
Table 2. Results of the top five a-priori models for predictors of habitat selection of hedgehog winter nests. Models are ranked based on their AIC values. Null model is also provided for comparison. Models indicated in bold were selected to build average models. Brackenhurst had two alternative maximal models, one including distance to amenity grassland (Brackenhurst Model A) and another including distance to buildings (Brackenhurst Model B). Habitats included in each of the top-ranking models are indicated by the “✓” symbol. Bold indicates top ranked models at each site (ΔAIC < 2).
Brackenhurst Model A
Models (N = 64)
Amenity grasslandBuildingsHedgerowsPasturesRoadsWoodlandArableAICΔAICAICw
✓Not included✓✓✓✓ 357.50.000.38
✓Not included✓✓✓✓✓358.20.750.26
✓Not included ✓✓✓✓359.41.940.14
✓Not included ✓✓✓✓360.83.330.07
✓Not included✓✓ ✓✓362.24.670.04
NULL491.2134.00<0.01
Brackenhurst Model B
Models (N = 64)
Amenity grasslandBuildingsHedgerowsPasturesRoadsWoodlandArableAICΔAICAICw
Not included✓✓✓✓✓ 350.20.000.41
Not included✓✓✓✓✓✓351.10.900.26
Not included✓ ✓✓✓ 352.11.890.16
Not included✓ ✓✓✓✓352.63.440.07
Not included✓✓✓ ✓✓354.34.090.05
NULL491.2141.00<0.01
Hartpury
Models (N = 128)
Amenity grasslandBuildingsHedgerowsPasturesRoadsWoodlandArableAICΔAICAICw
✓✓✓✓✓395.60.000.49
✓✓✓✓✓✓397.41.800.20
✓ ✓✓✓✓✓397.62.040.18
✓✓✓✓✓✓✓399.43.840.07
✓✓ ✓✓401.25.610.03
NULL464.468.8<0.01
Table
Table 3. Model averaged values of the best a-priori models (ΔAIC < 2) investigating habitat selection for winter nest sites. SE = standard error. Brackenhurst had two alternative models, one including distance to amenity grassland but excluding buildings (Brackenhurst Model A) and another including distance to buildings but excluding amenity grassland (Brackenhurst Model B). Negative values indicate a higher probability of nesting closer to that specific habitat.
Table 3. Model averaged values of the best a-priori models (ΔAIC < 2) investigating habitat selection for winter nest sites. SE = standard error. Brackenhurst had two alternative models, one including distance to amenity grassland but excluding buildings (Brackenhurst Model A) and another including distance to buildings but excluding amenity grassland (Brackenhurst Model B). Negative values indicate a higher probability of nesting closer to that specific habitat.
VariableBrackenhurst Model A (3 Best a-priori Models)Brackenhurst Model B (3 Best a-priori Models)Hartpury (2 Best a-priori Models)
EstimateSEzp-ValueEstimateSEzp-ValueEstimateSEzp-Value
(Intercept)−0.2810.4390.6400.522−0.1130.4320.2610.794−2.5140.5154.879<0.001
Hedgerows−0.0130.0062.000<0.05−0.0130.0062.000<0.05−0.0080.0033.204<0.01
Pasture0.0170.0062.942<0.010.0170.0062.877<0.010.0100.0033.748<0.001
Roads−0.0120.0052.544<0.05−0.0100.0042.443<0.05−0.0160.0062.590<0.01
Woodland−0.0200.0035.919<0.001−0.0200.0035.607<0.001−0.0130.0033.774<0.001
Arable0.0020.0021.1270.2600.0020.0021.0620.2880.0050.0013.436<0.001
Buildings Not included−0.010.0033.412<0.0010.0010.0010.4880.626
Amenity grassland−0.0080.0032.527<0.05Not includedNot included
Table
Table 4. Summary of body mass changes recorded in previous studies of the West-European hedgehog over the winter hibernation period.
Table 4. Summary of body mass changes recorded in previous studies of the West-European hedgehog over the winter hibernation period.
CountryHabitatYears StudiedSample Size& CompositionMass Loss Recordedover WinterMinimum Weightto SurviveHibernationReference
EnglandUrban parkland1963–196810525%Recommends 450 g (550 g in more northern areas)[63]
DenmarkRural2001–200210 (5♀:5♂); (3A:7J)30.2 ± 7.1% (A)
22.1 ± 10.1% (J)		513 g[82]
IrelandRural2008–20098 (7A:1J)301 ± 3.9g (♀) (range: 15–38%)
108 ± 2.6g (♂) (range: 3–6%)		475 g in Nov[67]
DenmarkSuburban2014–20158 (8J)16 ± 2.9% (J)-[83]
EnglandVarious2010–201455 (19♀:30♂:16?); (20A:35J)98.6 ± 35.6 g (♀)
160.8 ± 40.5 g (♂)
111.4 ± 33.0 g (A)
162.2 ± 43.3 g (J)
14.1 ± 3.1% (All animals)		Recommends >600 g for release, but one individual weighing 391 g survived release and hibernation[64]
EnglandVarious2015–201721 (11♀:10♂)Site 1: 240 ± 150 g (25 ± 13%) (♀)
Site 1: −4 ± 89 g (1 ± 9%) (♂)
Site 2: 117 ± 121 g (14 ± 16%) (♀)
Site 2: 110 ± 141 g (15± 19%) (♂)		-Present study
Table
Table 5. Summary of over-winter nesting behaviour in previous studies of the West-European hedgehog. Studies are listed in chronological order.
Table 5. Summary of over-winter nesting behaviour in previous studies of the West-European hedgehog. Studies are listed in chronological order.
CountryHabitatYears StudiedSample Size& Composition 1Duration of Hibernation(Days)Number of Nests UsedReference
EnglandUrban park1963–1967167 nestsNot recordedMean occupation time = 1.4 months (range 0–6 months)[61]
DenmarkRural2001–200210 (3A:7J)197.7 ± 2.2 (A)
178.8 ± 13.1 (J)		2.2 (range: 1–4)[82]
IrelandRural2008–20108 (7A:1J)167.3 ± 10.5 (♀)
148.6 ± 10.2 (♂)
155.4 ± 9.0 (A)
157 (J)		2.0 ± 0.6 (♀)
3.2 ± 0.6 (♂)
2.4 ± 0.7 (A)
5.0 (J)		[67]
FinlandUrban2004–200611 (11A) (5♀:6♂)223 ± 2.5 (♀)
224 ± 4.8 (♂)		1.0 (♀)
1.0 (♂)		[68]
DenmarkUrban2014–20158 (8J)138.0 ± 5.6 (J)1.8 ± 0.14 (J)[83]
EnglandVarious2010–201455 (20A:35J); (19♀:30♂:16?)Not recorded2.2 ± 0.5 (♀) 2
1.7 ± 0.4 (♂) 2
1.8 ± 0.4 (A) 2
2.6 ± 0.6 (J) 2		[64]
EnglandArable2015–201721A (12♀:9♂)Not recorded5.8 ± 2.6 (♀)
5.0 ± 1.9 (♂)		Present study
1 Data were recorded by the authors either in terms of the number of nests studied or the number of individuals studied: A = adult; J = juvenile; ? = unknown sex. 2 The number of nests used per 100 days.

Share and Cite

MDPI and ACS Style

Bearman-Brown, L.E.; Baker, P.J.; Scott, D.; Uzal, A.; Evans, L.; Yarnell, R.W. Over-Winter Survival and Nest Site Selection of the West-European Hedgehog (Erinaceus europaeus) in Arable Dominated Landscapes. Animals 2020, 10, 1449. https://doi.org/10.3390/ani10091449

AMA Style

Bearman-Brown LE, Baker PJ, Scott D, Uzal A, Evans L, Yarnell RW. Over-Winter Survival and Nest Site Selection of the West-European Hedgehog (Erinaceus europaeus) in Arable Dominated Landscapes. Animals. 2020; 10(9):1449. https://doi.org/10.3390/ani10091449

Chicago/Turabian Style

Bearman-Brown, Lucy E., Philip J. Baker, Dawn Scott, Antonio Uzal, Luke Evans, and Richard W. Yarnell. 2020. "Over-Winter Survival and Nest Site Selection of the West-European Hedgehog (Erinaceus europaeus) in Arable Dominated Landscapes" Animals 10, no. 9: 1449. https://doi.org/10.3390/ani10091449

APA Style

Bearman-Brown, L. E., Baker, P. J., Scott, D., Uzal, A., Evans, L., & Yarnell, R. W. (2020). Over-Winter Survival and Nest Site Selection of the West-European Hedgehog (Erinaceus europaeus) in Arable Dominated Landscapes. Animals, 10(9), 1449. https://doi.org/10.3390/ani10091449

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop