Acta Theriologica 50 (2): 161–166, 2005. PL ISSN 0001–7051 Winter mortality rates of bats inhabiting man-made shelters (northern Poland)
Ireneusz RUCZYÑSKI, Iwona RUCZYÑSKA and Krzysztof KASPRZYK
Ruczyñski I., Ruczyñska I. and Kasprzyk K. 2005. Winter mortality rates of batsinhabiting man-made shelters (northern Poland). Acta Theriologica 50: 161–166.
Non-predator and non-accidental mortality rates of bats inside the city of Toruñ’s
fortification system (northern Poland) were studied over winter periods from 1995 to2000. The bats were counted and dead bats collected at 1-month intervals from Octoberto April. In total, thirty four dead bats were found. The percentage of dead individualsof the surveyed bats was low: Myotis daubentonii (0.6%), M. nattereri (0.4%), Plecotusauritus (0.4%), M. myotis (0.1%), and zero for Barbastella barbastellus. There was noclear difference in the species ratio of the observed and dead bats. The percentage of the dead to surveyed bats was lower in November (0.07%) and December (0.07%), andhigher in September (3.3%) and April (1.3%). Temperature explained 84% of variationof the differences in mortality rates. Observations suggest that non-predator andnon-accidental mortality inside the fortifications was extremely low and non-linearlycorrelated with the ambient temperature measured outside the fortifications.
Mammal Research Institute, Polish Academy of Sciences, Bia³owie¿a, Poland, e-mail:[email protected] (IR, IR); Department of Vertebrates Zoology, Insti-tute of Ecology and Environment Protection, Nicholas Copernicus University, Toruñ,Poland (KK)
Key words: Chiroptera, bats, hibernation, temperature, casualties
Bats are small, long-living animals, with low fecundity (Barclay and Harder
2003). Low reproductive rates result in a slow population growth. The inability ofa population to recover from population crashes increases the risk of localextinctions (Racey and Entwistle 2000). Therefore the knowledge about mortalityfactors is important for understanding the population dynamics of bats.
The comparative analysis of life span in bats reveals that longevity is in-
fluenced by reproductive rate, tendency to hibernate, body mass and use of caveroosts (Wilkinson and South 2002). Hibernating bats have prolonged lifespancompared with those not hibernating. Prolonged lifespan can be caused by lowerpredator and famine mortality (Wilkinson and South 2002). Increasing longevitycan be also explained by disposable soma theory (Kirkwood and Austad 2000) anda restricted intake of calories (Kirk 2001, Lin et al. 2002). Calorie restrictedanimals shift resources to somatic maintenance rather than to reproduction(Shanley and Kirkwood 2000), which can reduce the accumulation of oxidativedamage (Austad 1997) and prolong the life of animals.
During hibernation, bats are exposed to various mortality factors, such as:
predation (eg Romanowski and Lesiñski 1988, Bogdanowicz 1994, Radzicki et al. 1999), human disturbance (Thomas 1995), adverse weather conditions (Ryberg1947, Davis and Hitchcock 1965, Speakman and Rowland 1999), and accidents(Gilette and Kimbrough 1970). In temperate zones the effects of such factors arehighly variable and often unpredictable (Tuttle and Stevenson 1982). Unfortu-nately, there is a lack of quantitative information to estimate the significance ofparticular factors. Survival probability is mainly based on capture/recapturemodels, and is not very useful in estimating the role of mortality factors. Thismethod is time consuming, requires handling of bats, and causes temporal disturb-ance of these animals. In this paper we propose to focus on measuring non-predatorand non-accidental mortality inside hibernacula, by systematic collection of deadanimals and comparing frequencies of deaths with the number of live bats. Limitingthe observation to hibernacula (like fortifications or caves) allows for the compari-son of mortality in different types of shelters, in different regions. Untill now suchresults have not been published due to the small number of detected dead bats.
We hypothesise that non-predator and non-accidental mortality inside the
fortifications caused by a disease, parasites, or starvation is low, as predicted bythe disposable soma theory (Kirkwood and Austad 2000), restricted calorie intake(Shanley and Kirkwood 2000), and correlated with the ambient temperature. Thus, the aim of the study was to find out whether non-predator and non-accidentalmortality rates of bats inside the fortifications varied throughout the Septemberto April period, and if they were dependent on the ambient temperature measured outside the fortifications. Material and methods
The study was conducted in the city of Toruñ (approx. 200 000 inhabitants), located in northern
Poland (53°01’N, 18°35’E). The investigation area consisted of five systems of Prussian militaryfortifications dating back to the 19th century. The fortifications surround the city and in many places are overgrown by trees. Shelter is provided for the bats in a system of corridors and large quarters,some of which are well-protected from weather conditions, others only partly. One system of thequarters was regularly flooded by water, while others were dry or flooded temporarily. The batsstayed on the walls, in choked ventilation canals, within holes in the walls, crevices, and metal pipes.
The bats were counted in the fortifications at 1-month intervals from October to March, from
1995/1996 to 1999/2000. In the years 1995/1996 and 1996/1997, inspections were also performed inSeptember and April. The period from September to April will be further referred as the winter orcold season. The period from November to March was recognized as a hibernal period, preceded by apre-hibernal and followed by a post-hibernal period (estimation from Lesiñski 1986, Kokurewicz2004). The same parts of a given hibernaculum were inspected. In total, during the five studyperiods, each fortification system was visited 15 to 31 times. The bats that may have died in theprevious winter were excluded from the analysis.
Live bats species were identified and counted without handling. Only individuals that did not
hang in a natural position, hung in the same position on two consecutive controls and dried out, orwhen their fur had changed its colour were handled (all controlled bats were dead). All the dead batswhich were not found in water or did not bear any visible injuries attributable to predators or otheraccidents were taken for post-mortem analyses, however, cause of death were not investigated in
detail. The age of the bats was estimated on the base of canines’ tooth wear: sub-adults – lack ofwear, adults – slight detritions or a complete lack of enamel.
Mortality rates were estimated for the 5 most common bat species for the months during the
study period (September–April). Test G was used for estimating differences in the species ratio of the living and dead bats (Sokal and Rohlf 1981). The data concerning the ambient temperature wereprovided by the Meteorological Station in Toruñ.
On average 64.2 (SE ± 33.9) bats were observed inside each fortification system
during the 5 study periods. Eight species of bats were found: Myotis nattereri(40.4%) and M. daubentonii (34.3%) dominated, M. myotis (11.5%), Plecotus auritus(7.6%) and Barbastella barbastellus (5.8%) were less common (Fig. 1), Eptesicusserotinus, E. nilsonii and M. brandtii/M. mystacinus were found sporadically(< 0.5% of bats).
During the research thirty four dead bats were found: M. daubentonii (17), M.nattereri (13), P. auritus (2), M. myotis (1), and 1 unidentified specimen. Amongthe 28 bats whose age was estimated, 21 were adults and 7 sub-adults. On average 0.3 of a dead bat per fortification system on one inspection was detected: M. daubentonii 0.13, M. nattereri 0.10, M. myotis 0.01, and P. auritus 0.02 (Fig. 1). Dead bats of B. barbastellus were not found. Differences in the species ratio of theobserved and dead bats were insignificant (G = 9.3, df = 4, p = 0.05).
The percentage of the dead individuals to the surveyed bats, calculated as a
mean number of the observed (live and dead) and dead bats during all inspections, was low for all species: M. daubentonii (0.6%), M. nattereri (0.4%), P. auritus(0.4%), and M. myotis (0.1%).
The mean number of the observed bats increased through the study period,
September (15.0, SE ± 4.3), January (77.5 ± 9.0), and was the highest in February(76.1 ± 11.3). The figure was still high in March (64.4 ± 12.0) but droppedhereafter and was at its lowest inApril (33.2 ± 10.1; Fig. 2). The mean
and was the highest in March (0.6± 0.2) and April (0.4 ± 0.4). The
Fig. 1. Mean number (± SE) of observed and dead
bats of the respective species during controls (totally5 winters). Mn – M. nattereri, Md – M. daubentonii,
Mm – M. myotis, Pa – P. auritus, Bb – B. barbastellus.
was positively correlated with the meantemperature measured outside the hi-
rates (Y = 0.032 x – 0.120x + 0.206, n =
8, R = 0.84, p < 0.05). Discussion bentonii, M. nattereri, and P. auritus
side the fortifications than M. myotis
and B. barbastellus, however the differ-
ences were statistically insignificant.
not clear. Bats hibernating in the forti-
Fig. 2. Variation in numbers of bats and mortality
rate during the hibernation period (totally 5winter seasons).
in the external weather conditions ortheir energy reserves (Bogdanowicz and
Urbañczyk 1983, Valenciuc 1989, Jurczyszyn and Bajarczyk 2001, Kokurewicz2004). This enables for the bats to choose an optimal temperature. Possibly thequality of hides available in the fortifications are more suitable for M. myotis andB. barbastellus than M. daubentonii, M. nattereri, and P. auritus.
The proportion of the dead to live bats was higher in September and October
than in November and December. The higher mortality rate in the first month ofthe study period could be attributed to weak animals that arrive first to thefortifications, where they die quickly. Ransome (1990) also suggests that inOctober late-born juveniles with low body food reserves leave the sampling sitesor die. In Warsaw, in similar structures and climate as Toruñ, M. daubentoniireaches its maximum weight in September (Lesiñski 1986), and reaches its bestcondition. On the other hand, daily decreases in body weight during the first partof the study period (until mid-November) were more than twice as high as in theremaining period (Lesiñski 1986), so energy expenditure is much higher thenthan during deep hibernation. It is possible that the higher energetic costs of lifeduring the transitory period (pre-hibernal and beginning of hibernation) correlate
with the ambient temperature and reduce the survival rate of weak or sickanimals. The lowest mortality in November and December suggest that benefits of energy preservation and somatic maintenance one the highest.
The dead bats were also found more often from January onwards and mortality
increased until April (post-hibernal period). This might be explained by theweakened physical condition (eg Lesiñski 1986, Koteja et al. 2001), and be a result of deteriorations of physical functions (eg disease progress). We observed that themortality rate of bats positively correlated with the mean monthly temperature. Park et al. (1999) noted a positive correlation between the number of daily batpasses monitored and cave temperature and an increase in diurnal activity at theend of winter. Because arousal involves high energy consumption (Thomas et al. 1990), we believe that most bats die inside the fortifications when the frequency of arousals increases, and as they grow active, because it reduces fat reserves. Atthis time progressive deterioration of body condition (due to the exhaustion of fatreserves) may also contribute to further problems. Whether the lowest monthlyambient temperatures increased the mortality inside the fortifications is notclear. It seems that the fortifications protect bats well from external weatherconditions, and even the lowest ambient temperatures do not or rarely reducetemperatures in the whole fortification below the ones to which bats are adapted.
The presented results show that non-predator and non-accidental mortality
(probably caused by a disease, parasites, or starvation) measured inside thefortifications is higher during transitory periods preceding and following the periodof deep hibernation, in which mortality was the lowest. The results also indicatethat both entering and exiting from hibernation are more risky periods for batsthan the period of deeper hibernation. The slowdown of life processes decreases therisk of non-predator and non-accidental mortality per unit time. For endothermicmammals the coldest month of the year usually causes a growth in mortality due tofamine or diseases (eg Pucek et al. 1993, Jêdrzejewska and Jêdrzejewski 1998),alternatively bats take advantage of low temperatures by slowing down their lifeprocesses and minimizing non-predator and non-accidental mortality.
Acknowledgements: Our thanks go to M. Wojciechowski, E. Szyp, I. Szyp, S. Bonin, J. Trochimiuk for assisting with the census of bats in the fortifications. We are very grateful to B. Jêdrzejewska,Z. Pucek, L. Rychlik for comments on earlier drafts of the article, two anonymous reviewers forcritical remarks on the manuscript, and S. Prior for language correction. References
Austad S. N. 1997. Comparative aging and life histories in mammals. Experimental Gerontology 32:
Barclay R. M. R. and Harder L. D. 2003. Life histories of bats: Life in the slow lane [In: Bat ecology.
T. H. Kunz and M. B. Fenton, eds]. The University of Chicago Press, Chicago and London: 209–253.
Bogdanowicz W. 1994. Myotis daubentonii. Mammalian Species 475: 1–9. Bogdanowicz W. and Urbañczyk Z. 1983. Some ecological aspect of bats hibernating in city of Poznañ.
Davis W. H. and Hitchcock H. B. 1965. Biology and migration of the bat, Myotis lucifugus, in New
England. Journal of Mammalogy 46: 296–313.
Gilette D. D. and Kimbrough J. D. 1970. Chiropteran mortality. [In: About bats: A Chiropteran
Biology Symposium. B. H. Slaughter and D. W. Walton, eds]. Southern Methodist UniversityPress, Dallas, Texas: 262–283.
Jêdrzejewska B. and Jêdrzejewski W. 1998. Predation in vertebrate communities: the Bia³owie¿a
Primeval Forest as a case study. Springer, Berlin Heidelberg: 1–450.
Jurczyszyn M. and Bajaczyk R. 2001. Departure dynamics of Myotis daubentonii (Kuhl, 1817)
(Mammalia, Chiroptera) from their hibernaculum. Mammalia 65: 121–130.
Kirk K. L. 2001. Dietary restriction and aging: comparative tests of evolutionary hypotheses. Journal
Kirkwood T. B. L. and Austad S. N. 2000. Why do we age? Nature 408: 233–238. Kokurewicz T. 2004. Sex and age related habitat selection and mass dynamics of Daubenton’s bats
Myotis daubentonii (Kuhl, 1817) hibernating in natural conditions. Acta Chiropterologica 6: 121–144.
Koteja P., Jurczyszyn M. and Wo³oszyn B. 2001. Energy balance of hibernating mouse-eared. Myotismyotis: a study with a TOBEC instrument. Acta Theriologica 46: 1–12.
Lesiñski G. 1986. Ecology of bats hibernating underground in Central Poland. Acta Theriologica 31:
Lin S. J., Kaeberlein M., Andalis A. A., Sturtz L. A., Defossez P. A., Culotta V. C., Fink G. R. and
Guarente L. 2002. Calorie restriction extends Saccaromeces cerevisiae lifespan by increasingrespiration. Nature 418: 344–348.
Park K. J., Jones G. and Ransome R. D. 1999. Winter activity of a population of greater horseshoe
bats (Rhinolophus ferrumequinum). Journal of Zoology, London 248: 419–427.
Pucek Z., Jêdrzejewski W., Jêdrzejewska B. and Pucek M. 1993. Rodent population dynamics in a
primeval deciduous forest (Bia³owie¿a National Park) in relation to weather, seed crop, andpredation. Acta Theriologica 38: 199–232.
Racey P. A. and Entwistle A. C. 2000. Life history and reproductive strategies of bats. [In: Repro-
ductive biology of bats. Crighton E. G. and P. H. Krutzsch, eds]. Academic Press, New York:363–414.
Radzicki G., Hejduk J. and Bañbura J. 1999. Tits (Parus major and Parus caeruleus) preying upon
hibernating bats. Ornis Fennica 76: 93–94.
Ransome R. 1990. The natural history of hibernating bats. Christpher Helm, London: 1–235. Romanowski J. and Lesiñski G. 1988. [Martens hunt bats]. Wszechœwiat 89: 210. [In Polish]Ryberg O. 1947. Studies on bats and bat parasites. Svensk Natur, Stockholm: 1–329. Shanley D. P. and Kirkwood T. B. L. 2000. Calorie restriction and aging: a life history analysis.
Sokal R. R. and Rohlf F. J. 1981. Biometry. W. H. Freeman and Company, New York: 1–859. Speakman J. R. and Rowland A. 1999. Preparing for inactivity: how insectivorous bats deposit a fat
store for hibernation. Proceedings of the Nutrition Society 58: 123–131.
Thomas D. W. 1995. Hibernating bats are sensitive to nontactile human disturbance. Journal of
Thomas D. W., Dorais M. and Bergeron J. M. 1990. Winter energy budgets and cost of arousal for
hibernating little brown bats, Myotis lucifugus. Journal of Mammalogy 71: 475–479.
Tuttle M. D. and Stevenson D. E. 1982. Growth and survival of bats [In: Ecology of bats.T. H. Kunz,
ed].Plenum Press, New York: 105–150.
Valenciuc N. 1989. Dynamics of movements of bats inside some shelters. [In:European bat research.
V. Hanák, I. Horáèek and J. Gaisler, eds]. Charles University Press, Praha: 511–517.
Wilkinson G. S. and South J. M. 2002. Life history, ecology and longevity in bats. Aging Cell 1:
Received 8 September 2004, accepted 7 February 2005.Associate Editor was Andrzej Zalewski.
LE ORIGINI DELLA LETTERATURA La nascita del e lingue romanze Le lingue volgari hanno origine in un periodo, durato oltre cinque secoli, che va dal crol o del ’Impero romano (476 DC) al 'anno 1000 circa. In quel periodo il latino, parlato da tutte le genti romanizzate, si trasforma di continuo poiché entra in contatto con i dialetti germanici (Franchi, Goti, Longobardi), il greco