Predation of wood mice (Apodemus sylvaticus) on hibernating bats

Predation is considered a nearly universal pressure affecting individual animals and has, through evolutionary history, shaped the morphology, behavior and life history traits of prey species. Since bats are very fast in flight, predation pressure on bat populations is likely to be a minor cause of mortality. Indeed, bats usually consist of less than 1 % of the prey of owls (Ruprecht 1979; Mikkola 1983; Kasprzyk et al. 2004). Nonetheless, large aggregations of bats may provide a viable resource for predators (e.g., raptors and owls) and may even become the dominant prey, comprising up to 39 % of the diet of individual predators (Julian and Altringham 1994; Lesinski et al. 2009; Sommer et al. 2009). Since bats and their roosts are protected by European legislation, large aggregations of bats are often found in protected sites. Although these sites may attract flying and non-flying predators and become high-risk areas, studies on predation of bats from this perspective are very limited.

Underground structures and their immediate surroundings often serve as mating sites, hibernacula, and sometimes even maternity roosts for bats. In these areas, bats are frequently reported among the mammalian prey of owl species during summer and autumn, such as barn owl, Tyto alba (Forster and Fairley 1975; Ruprecht 1979, Mertens 1997; Sommer et al. 2009) and tawny owl, Strix aluco (Rackow 1992; Kowalski and Lesiński 1990; Lesiński et al. 2009). Other occasional scavengers and hunters include the otter, Lutra lutra (Forman et al. 2004), kestrel, Falco tinnunculus (Negro et al. 1992) and hobby, Falco subbuteo (Speakman 1991; Fenton et al. 1994). Observations of predators hunting bats in winter roosts are surprisingly scarce. Torpid bats are vulnerable to scavengers and predators. During winter, uninterrupted torpor bouts can last 2 weeks (Daan 1972; Park et al. 2000) and sometimes up to 14 weeks (Harmata 1985). Known predators of hibernating bats include great tit, Parus major (Bogdanowicz 1990; Radzicki et al. 1999; Estók et al. 2010), stone marten, Martes foina (Bekker 1989; Romanowski and Lesiński 1991; Kokurewicz 2004), red fox, Vulpes vulpes (Kokurewicz 2004), and wood mouse, Apodemus sylvaticus (Bekker and Mostert 1991; Mostert 1996).

In order to manage underground structures registered as protected sites for bats effectively, predation risk should be quantitatively assessed at those sites. In this study, we surveyed for, and collected the remains of, predated bats in 12 hibernacula systems to investigate the effect of predation on hibernating bats. This paper has five objectives: (1) to identify the predator; (2) to analyse the frequency and seasonality of predation; (3) to identify the characteristics of a hibernaculum that could increase the risk of predation; (4) to test whether bats show an anti-predator behavioural response; and (5) to estimate the annual mortality caused by predators in The Netherlands during various winters.

The study was conducted in the province of Zuid-Holland, between the cities of Den Haag (The Hague), Leiden and the town of Wassenaar (between 52°07′ and 52°09′N, 4°18′ and 4°21′E, Fig. 1). The study site consisted of 12 bunker complexes. These belong to the “Atlantic Wall”, an extensive system of coastal fortifications built by the German army during World War II (Saunders 2001). After the war the fortifications were abandoned and were gradually overgrown by vegetation such as European beachgrass, Ammophila arenaria, sea buckthorn, Hippophae rhamnoides, European black elderberry, Sambucus nigra, common oak, Quercus robur, and European Spindle-Tree, Euonymus europaeus. All bunkers are closed to the public by a steel door, with one or two entrances (14 × 20 cm) for bats. Mice can enter freely through small gaps to the side of the doorframe. The bunkers vary in size, underground layout, and the number of entrances. All have underground corridors made of brick connected to one or several concrete bunkers. The corridors are typically approximately 2.0 m high and 1.2 m wide, with an arched ceiling. The size and shape of the bunkers vary according to their original function (e.g., command post, troop quarters, ammunition storage, and garage for searchlight). The first records of bats occupying the bunkers in winter date from the early 1980s (A.-J. Haarsma, unpublished data). The ceilings and walls of both the bunkers and the corridors have numerous crevices and cavities suitable for hibernating bats. Bats also hibernate in the sealed ventilation shafts and metal pipework.

Between the winters of 2003 and 2015, we found 214 bats killed by predators in 12 hibernacula in the province of Zuid-Holland. Judging by the typical pattern of lesions, their deaths were the result of predation by wood mice. In a similar study in the province of Gelderland, The Netherlands, a total of more than 300 bat remains were found in the period of 1987–2013 (R. Kaal, unpublished data). Since these data were collected only once per winter (and not during all winters), they were not included in the analysis. In this area the number of predated bats varied from 1 to 120 individuals per winter (9 sites, maximum 24.3 % of the local hibernating population). The high numbers of predated bats, both in Zuid-Holland and in Gelderland, show that predation of bats by wood mice is more common than is generally assumed and the effects of predation in hibernacula may be significant. We further suspect that the effect of predation is more severe in isolated sites than in clustered sites, as isolated sites may take longer to become (re)colonized by bats.

Although wood mice are generally considered scavengers (Montgomery and Montgomery 1990), our study reveals that predation on hibernating bats was not incidental, but that wood mice actively searched for bats (Fig. 4). Mouse-related mortality was estimated to kill between 5.4 and 8.8 % of the hibernating population in years with high predation. This may be an underestimation, as mice tend to take their prey to concealed and safe places. Another factor causing underestimation of the actual numbers of predated bats may be fungal decay. In the humid conditions of the hibernacula, remains of dead bats tend to decay rather quickly.

Unlike other authors (e.g., Julian and Altringham 1994; Petrželková and Zukal 2003; Sommer et al. 2009), who found that high predation mainly occurs at sites with high population densities, our results indicate that population density is only one of the factors influencing predation risk by wood mice. In addition, we found that large sites constitute a higher predation risk. In our study, with only 12 sites, we found no significant effect of the vegetation near the entrance of the hibernacula. Further research is needed, as wood mouse densities differ between woodland and other types of habitat (Tellería et al. 1991; Todd et al. 2000).

The seasonality of mortality was rather similar to that found in other studies (Kokurewicz 2004; Ruczyński et al. 2005). We found a peak in predation-dependent mortality in April. In other hibernacula timing of peak mortality may differ due to differences in predator species, climate (e.g., maritime climate versus continental climate) or other local conditions (such as the size of hibernacula and vegetation type near the entrance).

An increase in mortality of hibernating bats at the end of the winter is often explained by exhaustion of fat reserves or a weakened physical condition as a result of progressing disease (Luis and Hudson 2006). Our study suggests that most deaths at the end of the winter are caused by predators; occupation of more exposed hibernation positions of weakened may increase the risk of predation. Moreover, bats tend to move progressively closer the entrance of a hibernaculum towards the end of the winter (Daan and Wichers 1968; Siivonen and Wermundsen 2008), further increasing their susceptibility to predation.

Winters near the coast of The Netherlands are generally mild, with an average temperature of 5.9 °C across the entire winter period. During mild winter weather, bats are easily disturbed (Haarsma and de Hullu 2012) and as a consequence tend to use more energy than during (mild) frost periods. Thus, in terms of fitness, Dutch bats may benefit from more severe winters. Hence, we suspect that the increase in wood mouse predation during colder winters following a low mast production of common oak is caused by higher energy demands and greater difficulty to find food for wood mice.

By hiding deep in crevices bats can reduce their risk of an encounter with a predator (Barclay and Harder 2003). Although this general behavior may be associated with predator avoidance, bats often appear to lack a perception of risk (Lima and O’Keefe 2013). Bats show little to no behavioral reaction to sound and scent associated with owls and mammalian carnivores (Kalcounis and Brigham 1994; Driessens and Siemers 2010). Some studies (Bekker and Mostert 1991; Ruczyński et al. 2005) postulate that hiding, or using concealed resting positions, can prevent predation. However, we found no relationship between the proportion of hiding bats and the availability of crevices, and our results indicate that the chance of being predated is not affected by the number of available crevices in a hibernaculum. We think that all bats, both in crevices and along the wall, can be predated as long as wood mice can reach those places. In this context, we note that other mammalian/reptilian predators of bats are larger and will not be able to reach bats in crevices.