Hibernation is critical for the overwinter survival of a range of vertebrate and invertebrate species [1
]. A reduced core body temperature and lowered metabolic rate allows individuals to conserve energy during periods of harsh environmental conditions and low food supply at the cost of becoming physically inactive for periods lasting days, weeks, or months [5
]. To ensure success, mammalian hibernators must increase food intake prior to entering hibernation to accumulate sufficient fat reserves which will later provide energy for day-to-day body maintenance and inducing arousal [5
]. If too little fat is accumulated, individuals are in danger of depleting their reserves before the hibernation season is over [7
]. In addition, survival during hibernation is also likely to be linked to nest quality [10
] and local environmental conditions [11
The West European hedgehog (Erinaceus europaeus
) is a small (<1.5 kg) winter-hibernating mammal that is thought to be in decline in the UK [12
]. The specific drivers of this decline are unclear, although a wide range of threats can be recognized, including the following: habitat loss, fragmentation, and degradation [14
]; road traffic accidents [19
]; the application of chemical herbicides, pesticides, and molluscicides, as well as the use of anticoagulant rodenticides [6
]; competition with and predation by badgers (Meles meles
], and climate-driven changes in invertebrate prey availability and hibernation success [7
Although timings differ in relation to climate, sex, body size, and condition, hedgehogs typically hibernate between November and April in the UK [6
]. It is not unusual for hedgehogs to temporarily rouse during the hibernation period and active individuals may relocate to alternative nests [6
]. These partial arousals can last anywhere from several hours to several days [7
]. Since hedgehog hibernation timings are variable, it is difficult to pinpoint which factors trigger the process of entering and arousing from hibernation, although it is likely to involve environmental and hormonal cues related to lower ambient temperatures, shorter days, and reduced invertebrate prey availability [7
Evidence suggests that hedgehogs are increasingly associated with areas of human habitation [26
] with substantially higher densities observed in towns and cities than in rural habitats [31
]. Despite a relative plethora of studies on the winter activity of captive, rehabilitated or rural-dwelling hedgehogs [9
], our understanding of the behaviour of urban-dwelling hedgehogs during this period is limited [11
Urban areas are associated with a range of factors that could potentially positively or negatively affect patterns of hibernation. For example, in addition to potential nesting sites in patches of remnant natural or semi-natural vegetation, hedgehogs can access cavities beneath buildings, gardens sheds, or decking within residential gardens; urban residents may also supply artificial refugia in the form of homemade or commercially available “hedgehog houses” [7
]. However, within each of these habitats/locations, hedgehogs are exposed to different levels of disturbance from humans or companion animals [39
], road traffic [19
], and artificial light [41
] and sound. Similarly, temperatures within different microhabitats are likely to vary in relation to, for example, the density and composition of surrounding buildings and associated structures [31
]. It is possible that such ”urban-associated” factors could have direct impacts upon the onset of and patterns of arousal during hibernation. For example, warmer temperatures in urban areas [43
] may stimulate early arousal from hibernation which, in turn, could increase fat consumption, thereby posing a risk to overwinter survival [7
It has been suggested that supplementary feeding could, in particular, negatively affect natural patterns of hibernation behaviour in hedgehogs [44
]. In the UK, many wildlife organisations actively encourage householders to leave out food for hedgehogs in gardens during the colder months in an effort to aid the accumulation of fat prior to hibernation but also to provide sustenance during periodic arousals when natural food availability is low (e.g., [45
]). The effects of anthropogenic feeding on some aspects of the ecology of urban wildlife (e.g., density, health, and reproductive output) have been investigated extensively (e.g., [48
]), but data on the impacts on hibernating species are limited. Key observations are that overwinter supplementary feeding is linked to the increased probability of sighting animals [51
], interruptions to denning behaviour [52
], and accelerated telomere attrition [53
]. Conversely, artificial food sources could provide invaluable additional sustenance for individuals in need [6
Overall, urban areas act as significant strongholds for the UK hedgehog population and expanding our knowledge of overwinter activity and the parameters affecting it is fundamental to developing robust conservation management strategies. Therefore, studies are needed which investigate the following: (a) the activity patterns of urban hedgehogs throughout the hibernation season and (b) how these are affected by external factors. In this study, we quantified patterns of hedgehog occupancy within residential gardens before, during, and after the winter season (see Methods for our definition of the winter season) in relation to within garden and surrounding habitat characteristics, environmental conditions (e.g., daylength and temperature), and patterns of anthropogenic feeding.
Hibernation is an adaptive physiological response to reduce energetic requirements during periods of low food availability. Hedgehogs, therefore, need to accumulate sufficient fat reserves prior to hibernation, and then minimize expenditure of energy during this period. In behavioural terms, this essentially means that hedgehogs need to avoid rousing unnecessarily from hibernation. However, they do need to retain the ability to be able to respond if environmental conditions become unfavourable or, for example, if they are detected by predators or disturbed. Consequently, individuals need to find locations that afford them protection, but which are also in proximity to alternative locations, with appropriate building materials, if they need to move.
In this study, hedgehog occupancy and detection in autumn were significantly linked to the area of woodland habitat within 500 m (WOOD 500 m) of focal gardens and the number of potential nest sites available within gardens (NESTSITES), respectively. Previous studies have reported that a significant proportion of winter nests are constructed in wooded areas [9
] and the nearby woodland measured in this study area may have provided valuable pockets of semi-natural nesting habitat within an otherwise built-up area. However, the relative qualities of woodland and within-garden nesting sites are unknown. For example, wooded areas can be associated with a higher abundance of favoured building materials (the leaves of broadleaved trees: [7
]) but urban woodlands are often open to the public and are likely to be associated with high levels of disturbance by walkers and especially their dogs. Alternatively, gardens offer potentially advantageous nesting sites such as beneath sheds and decking, but where natural nesting materials could be scarce. Future studies of urban hedgehog populations, therefore, need to focus on quantifying where hibernacula are located and if this is linked to over-winter survival rates.
Urban areas also pose one additional challenge. Research to date has indicated that hedgehogs tend to enter hibernation in response to the combination of a reduction in temperatures and a decline in food availability [7
]. This was also evident in this study, with hedgehog detection during winter reduced as grass and air temperatures declined. In urban areas, however, food supplied by householders was not directly linked to prevailing temperatures. As a result, hedgehogs could be getting “mixed messages”, that is, food availability is still high even though temperatures are low. Ultimately, this could result in maladaptive responses leading to reduced over-winter survival rates and longevity.
In autumn, hedgehog occupancy was correlated with whether they had been fed in the previous season. Hedgehogs were detected in 54.0% of gardens overall, with a marked difference between those houses where they had (84.0%) and had not (34.2%) been fed. Similarly, occupancy in winter (30.2% of gardens overall) was also correlated with the pattern of feeding at the outset of the study, with an increase in the disparity between gardens where they had (64.0%) and had not been fed (7.9%). This was consistent with the radio-tracking data reported by Rasmussen et al. [11
] which indicated that urban-dwelling hedgehogs tended to stay in the vicinity of local feeding stations during both active and inactive seasons, but also potentially suggested that patterns of feeding prior to hibernation could increase the likelihood that hedgehogs visited gardens during the hibernation period. In contrast, in spring, hedgehog occupancy tended to be associated with the frequency with which animals were being fed in that season, with occupancy higher where they were being fed more frequently.
Winter activity is, however, not unusual, and hedgehogs typically relocate nests at least once during the hibernation period [6
]. As we used footprint tunnels to record hedgehog activity on a weekly basis, it was not possible to determine if detections during the winter season reflected individual animals in the normal process of relocating nests, or if they reflected the behaviour of several animals in the same garden. For example, the continued use of a single garden by individual hedgehogs overwinter has been recorded previously [9
]. That being said, hedgehogs were detected for an average of 2.6 weeks in winter in gardens where they had been fed previously (n
= 16) as compared with 2.0 weeks in other gardens (n
= 3). Again, this is suggestive of the fact that householder feeding patterns could be influencing over-winter activity.
However, although anthropogenic feeding could negatively affect hedgehogs during hibernation [52
], it is possible that it could be beneficial [9
]. For example, it could enable animals that have not accumulated sufficient body fat to delay the point at which they enter hibernation [6
], especially juveniles born in late summer [7
]. Similarly, it could also help animals that have roused from hibernation to replenish some of their reserves. This could be important for animals that experience an increasing number of arousal events in relation to changing climatic conditions and anthropogenic influences.
Conversely, as hedgehogs are capable of surviving losses of up to 44% of their pre-hibernation weight [9
], it is not clear if access to food during winter is beneficial. For example, it has been suggested that hedgehogs might only enter into a ”partial hibernation” where food is available [7
]. Since even a single rousing can consume the same amount of energy required to survive 3–4 days of hibernation [36
], animals can experience proportionately larger losses in mass overwinter if they cannot access sufficient food [7
]. Furthermore, animals that are active during the winter also face the additional risks associated with, for example, road traffic, companion animals, and domestic gardens [11
]. ”Shortenings” of the hibernation period, caused by increased arousals or a delay in hibernation commencement, have also been linked to accelerated cellular aging in mammals [53
], thereby potentially having implications for longevity [73
]. In addition, there is a need to consider the nutritional value of foods being provided by householders. For example, should animals come to rely on non-natural foods as a principal source of energy, it is possible that these do not fulfill their nutritional requirements and could compromise their condition [50
]. Therefore, additional information is required on the types of food used by householders and its nutritional content relative to the needs of hedgehogs at this time.
Despite the absence of any definitive data that feeding hedgehogs overwinter is beneficial, it is encouraged by several wildlife organisations in Britain [45
]. Given that arguments can be made that overwinter feeding could negatively impact hedgehogs, there is an urgent need to study its effects in more detail so that accurate advice can be given to householders. Such investigations will require the study of the activity and movement patterns, body mass changes, reproductive success, and longevity of individual hedgehogs before, during, and after the hibernation period in an experimental framework (i.e., controlling the frequency and volume of food supplied by randomly selected householders). These studies are, however, likely to be associated with significant challenges since they would require the cooperation of large numbers of householders for extended periods of time.