Hibernating in large underground cavities seems to offer bats all the prerequisites for a safe passage against the cold outside and the general lack of food resources throughout the boreal winter. Here bats have access to stable climatic conditions, reduced disturbance and relative lack of predation pressure (Furey & Racey, 2016; Hall, 1982; Raesly & Gates, 1987). However, there are several risks bats may face inside subterranean roosts, too. The most important among these is the risk of depleting energetic resources due to frequent arousal (Bachorec et al., 2021; Blažek et al., 2019; McGuire et al., 2021). Arousal is a energetically costly and stressful process (Lee et al., 2002), which may be caused by hypothermia, overheating, accidental disturbance or parasites (Meier et al., 2022). Bat species roosting in tight-knit groups may balance the risk of thermic eccentricities by adapting group size (smaller/larger) and inside-group position (central/on the edge, see also Fig. 1) and most species do so (Boratyński et al., 2012; Brown, 1999; Hall, 1982). Large clusters may erode the possibility of a dynamic control of thermal conditions inside the group. Moreover, chances of accidental arousal due to overheating or caused by an active individual (aroused by overheating) are high inside crowded groups, especially in the more central part of the cluster (Boyles et al., 2020; Boyles & McKechnie, 2010). Thus, roosting in large, crowded groups bear several risks, too.
Interestingly, bent-winged bats prefer to congregate into larger groups, even in periods when thermal conditions do not force them (for example in migratory periods, but also while pup-rearing). Our results suggest that active tick-avoidance behaviour may have a role in cluster formation, in order to reduce the risk posed by blood-feeding ectoparasites (ticks). Tick parasitism is present in hibernating colonies of common bent-winged bats and ticks attack the more exposed individuals (located at the cluster’s border, Fig. 2.). Tick-infested individuals were located significantly closer to the cluster’s edge, than non-infested ones. This pattern was observed both in small and large groups, indicating a constant phenomenon. Group size was also important, as smaller groups were more infested than large ones, thus providing more evidence for beneficial role of larger clusters (Fig. 3.). The larger the cluster, the more individuals may stay in the inner, more safe area.
Ectoparasites in general and ticks in special are important blood feeders and may have detrimental effect on vertebrate populations. Generalist ticks feeding on ungulates may cause anaemia (Teel et al., 1990), irregular migrations (DeIgiudice et al., 1997), habitat aversion (Samuel & Welch, 1991) or even may cause death to hosts (Jones et al., 2019). Host specific ticks of birds may cause nest site desertion, colony site abandonment or breeding failure in colonial birds (Duffy, 1983; Heath, 2006; Mckilligan, 1987; Rataud et al., 2020), but they may have detrimental effects on solitary breeders, too (Gauthier-Clerc et al., 1998; Hoodless et al., 2003).
Short-legged bat ticks are important ectoparasites of common bent-winged bats and infestation prevalences may reach high values (range: 11–43%, see Lourenço & Palmeirim, 2008; Sándor et al., 2019, but may reach up to 87% in a population freshly arrived to the hibernating area in 2021, Sándor AD, unpublished observation). While in most cases ticks on bats do not show high intensity and the hosts do tolerate tick presence, in certain cases this impact may have detrimental effects on hosts (Péter et al., 2021; Sándor et al., 2019). High tick burdens are suspected to exert an important effect on the energy balance of hibernating bat populations. Hibernating bats regularly host ticks, as exemplified by common bent-winged bats predominantly infested by I. simplex females (largest among blood-feeding stages) in winter (Beaucournu, 1962, 1967; Hornok, 2017; Lourenço & Palmeirim, 2008). In addition to blood-loss, ticks may have an indirect effect on hosts. Bat specialist ticks are suspected vectors and were found to harbor different pathogenic bacteria like Borrelia, Bartonella, Rickettsia (Hornok et al., 2019; Leulmi et al., 2016; Lv et al., 2018) or protozoa like Polychromophilus spp. and Babesia spp. (Hornok et al., 2016; Sándor et al., 2021), thus may pose an epidemiologic risk, too. Other than these, we failed to find any quantification of ectoparasite impact on hibernating bats, likely due to lack of studies. While short-legged ticks may be common all year long, another important group of blood-feeding bat ectoparasites, the nycteribiid flies (Diptera: Nycteribiidae) show low frequencies in winter (lowest in early spring), as pupal emergence requires active host movements, thus new individuals are rarely replacing the naturally disappearing active flies (adult flies live generally a few days to a few weeks) in this period (Ryberg, 1947; Sándor et al., 2024). Thus, any mechanism through which hibernating bent-winged bats are grouping into large clusters is likely targeting the avoidance of tick infestation.
The fact that bat individuals on the edge of hibernating colonies have a higher chance of being infested by ticks leads to a trade-off between maintaining energetic balance vs. parasite-infestation risk. Bent-winged bats are clustering in large tight-knit groups likely to reduce the risk of tick infestation, even if this means a higher chance of thermal instability and energetically demanding arousal in the inner part of the roosting cluster.