653
Reproduction affects flight activity in female and male Daubenton’s bats, Myotis daubentoni M. Dietz and E.K.V. Kalko
Abstract: Nearly all mammals in the temperate zone breed in spring and summer when climatic conditions are favourable and food is abundant. Similar to other mammals, food requirements of female bats are particularly high during pregnancy and lactation and of males during spermatogenesis. Seasonal changes in energy demand and reproductive condition should therefore result in different foraging activity within and between sexes. This assumption was tested on 16 adult females and 13 adult males of the Palaearctic Daubenton’s bat, Myotis daubentoni (Kuhl, 1817), that were radio-tracked during pregnancy, lactation, and post-lactation periods. Pregnant females, as hypothesized, flew significantly longer (mean: 358.9 min; 70% of the night length) than males (mean: 228.5 min; 42.4% of the night length) during spring. In contrast, nightly flight time of lactating females decreased and was significantly less than that of pregnant females, but was similar to that of males during the same period. The longest flight times of males were registered during late summer when spermatogenetic activity is high. However, there were distinct differences in the use of foraging areas between female and male Daubenton’s bats. Female bats used small, individual foraging areas during pregnancy and lactation. The pattern was reversed in females after the young had been weaned and in males after they entered spermatogenesis. Overall, the results confirmed our proposition that flight activity reflects the higher energy demand and nutrition requirements in the different reproductive periods. Re´sume´ : Presque tous les mammife`res de la zone tempe´re´e se reproduisent au printemps et a` l’e´te´ lorsque les conditions climatiques sont favorables et la nourriture abondante. Comme chez les autres mammife`res, les besoins alimentaires des chauves-souris sont particulie`rement e´leve´s durant la grossesse et l’allaitement chez les femelles et la spermatogene`se chez les maˆles. Les changements saisonniers des besoins e´nerge´tiques et de la condition reproductrice devraient ainsi entraıˆner des modifications dans les activite´s de recherche de nourriture chez chacun des sexes et entre les sexes. Nous avons ve´rifie´ cette pre´supposition chez 16 femelles adultes et 13 maˆles adultes du murin de Daubenton, Myotis daubentoni (Kuhl, 1817), une espe`ce pale´arctique; les animaux ont e´te´ suivis par radio durant les pe´riodes de grossesse, d’allaitement et de post-allaitement. Conforme´ment a` l’hypothe`se, au printemps, les femelles enceintes volent significativement plus longtemps (moyenne : 358,9 min; 70 % de la dure´e de la nuit) que les maˆles (moyenne : 228,5 min; 42,4 % de la dure´e de la nuit). En revanche, la dure´e du vol de nuit des femelles allaitantes diminue et est significativement infe´rieure a` celle des femelles enceintes, mais semblable a` celle des maˆles durant la meˆme pe´riode. Les dure´es de vol les plus longues des maˆles ont lieu a` la fin de l’e´te´ lorsque la spermatogene`se est tre`s active. Il y a, cependant, de nettes diffe´rences dans l’utilisation des zones de recherche de nourriture entre les murins de Daubenton maˆles et femelles. Les murins femelles utilisent de petites zones individuelles de recherche de nourriture durant la grossesse et l’allaitement. Ce patron s’inverse chez les femelles apre`s le sevrage des jeunes et chez les maˆles apre`s le de´but de la spermatogene`se. Dans leur ensemble, ces re´sultats confirment notre e´nonce´ qui veut que l’activite´ de vol refle`te la demande accrue d’e´nergie et les besoins alimentaires plus importants au cours des diffe´rentes pe´riodes du cycle reproductif. [Traduit par la Re´daction]
Introduction Mammals are characterized by a diverse array of lifehistory strategies that are strongly influenced by body size and environmental conditions. The size of a mammal has an important effect on its energy demand for homeothermy. Small mammals have higher mass-specific metabolic rates Received 29 October 2006. Accepted 1 May 2007. Published on the NRC Research Press Web site at cjz.nrc.ca on 19 June 2007. M. Dietz. Institute of Experimental Ecology, University of Ulm, Albert-Einstein Allee 11, D-89069 Ulm, Germany. E.K.V. Kalko.1,2 Smithsonian Tropical Research Institute, Balboa, Panama´. 1Corresponding
author (e-mail:
[email protected]). address: Institute of Experimental Ecology, University of Ulm, Albert-Einstein Allee 11, D-89069 Ulm, Germany.
2Present
Can. J. Zool. 85: 653–664 (2007)
than larger mammals to compensate for the higher rate of heat loss in relation to the larger surface area per unit mass (Speakman and Thomas 2003). In addition to the general costs of homeothermy, the expensive reproductive period requires specific physiological and behavioural adaptations. Females must balance their investment in gestation and lactation to sustain the development of their young and to secure a successful reproductive period. For this, in the temperate zone, bats like almost all other mammals synchronize the period of gestation and lactation with high food availability in spring and summer (Racey and Swift 1985; Rydell 1992; Hickey and Fenton 1996; Racey and Entwistle 2000). In bats, the increased energy demand during reproduction, particularly during lactation (Kurta et al. 1989), is well reflected in higher rates of food consumption by lactating females that may increase up to 45% (Myotis lucifugus
doi:10.1139/Z07-045
#
2007 NRC Canada
654
(LeConte, 1831), Myotis velifer (J.A. Allen, 1890); Kunz 1974; Anthony and Kunz 1977) from pregnancy to lactation. However, food availability and thus energy intake varies with weather conditions (Lewis and Taylor 1964; Racey and Swift 1985; Peng et al. 1992), which may in turn affect reproduction. It has also been shown that the timing and pace of reproduction are influenced by the amount of prey and thus energy intake (Arlettaz et al. 2001). Parturition of two mouse-eared bats was synchronous in Myotis blythii (Tomes, 1857) and its congener Myotis myotis (Borkhausen, 1797), in years with abundant cockchafers (Melolontha melolontha (L., 1758); Scarabaeidea). Cockchafers are one of the main prey items early in the year for M. blythii. In years without cockchafers, M. blythii gave birth 10 days later than M. myotis, which mainly feeds on carabid beetles. Because of its higher fat and protein contents, milk of lactating insectivorous bats is considerably more nutritious than milk of frugivorous bats (Kunz and Stern 1995). This results in a notably shorter, but for females far more energy demanding lactation period (Kunz and Hood 2000). The increased physiological stress on females during reproduction has led to mechanisms that compensate for this increased energy demand. One of these strategies is roosting in colonies where social thermoregulation is thought to improve conditions for pregnancy and post-partum care (Kurta et al. 1987; Audet 1992). Lowering body temperature is seen as the most effective way to save energy when food supply is poor. During reproduction, however, lowering of body temperature is at the expense of fetal growth and development of young (Wilde et al. 1995, 1999). Consequently, maximum reduction of body temperature in reproductively active female Daubenton’s bats (Myotis daubentoni (Kuhl, 1817)) is only 2–4 8C in the day roost, and deep torpor is avoided (Dietz and Kalko 2006). In contrast, male Daubenton’s bats that roost separately from females regularly enter torpor for several hours during this time, which is similar to that of other bat species like the big brown bat, Eptesicus fuscus (Beauvois, 1796) (Grinevitch et al. 1995). Male bats experience less physiological stress during this period than females, since they have no offspring to care for. However, in mid-summer, energy requirements of males increase because of spermatogenesis and the beginning of the mating period (Racey and Tam 1974). Recent studies on body mass changes, reproductive condition, and nocturnal activity of adult male Daubenton’s bats suggest that their food demand is highest in mid-summer during the period of high spermatogenetic activity and steep increase in body mass (Encarnac¸a˜o et al. 2004a, 2004b). From that time on, we noted distinct changes in thermoregulatory behaviour as female Daubenton’s bats became torpid during daytime after the young were fledged, whereas males remained homeothermic (Dietz and Kalko 2006). As a consequence of higher energy demands to reach and maintain homeothermic body conditions during pregnancy, lactation, and high spermatogenetic activity, intake of food should increase accordingly and distinct differences in flight activity between female and male bats are probable. Individuals with a higher food intake should have longer flight times per night than individuals with a reduced energy demand. This assumption is supported by a study of free-ranging
Can. J. Zool. Vol. 85, 2007
E. fuscus, where pregnant and lactating females showed a trend for longer foraging periods per night compared with males (Wilkinson and Barclay 1997). Based on those observations, we tested in our study the assumption that males and females of the trawling bat M. daubentoni should differ in foraging behaviour in relation to higher energy demands during the reproductive period. We compared nightly flight time, number of foraging areas, and site fidelity of free-ranging females and males. For pregnant and lactating females, we expected a concentrated use of small, highly profitable and individual foraging areas to optimize energy intake. We also predicted that the bats minimize time for commuting between foraging areas. During pregnancy and lactation, the nightly flight time of females should be longer than that of males. Subsequent to the lactation period, however, flight time of female Daubenton’s bats should be less than that of males because of the males’ increased energy demand during maturation of the spermatozoa in the epididymis and during the mating period.
Materials and methods Study site and animals The study area was located in the vicinity of the city of Giessen in central Germany (Hessen; 50.358N, 8.408E). It included the Philosopher’s Forest, a small (20 ha) deciduous forest bordered by buildings. We radio-tracked 16 adult female and 13 adult male Daubenton’s bats (Table 1). The females were part of a maternity colony in the small forest. The males roosted in tree holes in the same forest, either singly or in small groups. The feeding sites of the bats consisted of two ponds at a distance of a few hundred metres to the day roost; the bats also used the brook Wieseck, which is close to the two ponds, and the river Lahn, which is about 2.5 km distant from the ponds, as feeding sites (Dietz and Fitzenra¨uter 1996). Population structure and feeding ecology of Daubenton’s bats in the study area have been investigated since 1992, therefore seasonality and habitat use are well known. To attach radio transmitters, we caught bats with mist nets set in their flight path or at their roosts. All animals were studied with permits from the state agency of Hessen, Germany, and cared for in accordance with the local laws for animal care. Bats were aged (adult and juvenile) by evaluating the closure of the phalangeal epiphysis (Anthony 1988) and by subsequent banding. Reproductive status of females was classified as pregnant, nonpregnant, lactating, and post lactating according to the methods described by Racey (1988). Males were classified according to their epididymal distension (0%, 25%, 50%, 75%, and 100%) following Encarnac¸a˜o et al. (2004a). Telemetry We used 0.5 g LB-2 radio transmitters (Holohil Systems Ltd., Carp, Ontario) that weighed between 4.6% and 6.8% of the bat’s body mass (7.7–12.1 g). This is below or only slightly above the 5% threshold suggested by Aldridge and Brigham (1988) as a limit for radio-tracking of small insectivorous bats to avoid negative short- and long-term effects like failure to reproduce (e.g., Neubaum et al. 2005). Kurta and Murray (2002) used transmitters for Indiana bats (Myotis sodalis Miller and Allen, 1928) that weighed around #
2007 NRC Canada
Dietz and Kalko
655
Table 1. Summary of radio-tracking data of 16 adult female and 13 adult male Daubenton’s bats (Myotis daubentoni) tracked in Giessen, Germany. Sex
Bat
Mass (g)
Reproductive status*
Pregnancy period (period 1) Female 1 9.0 Pregnant 2 12.1 Pregnant 3 8.5 Pregnant 4 10.4 Pregnant 5 8.6 Pregnant 6 7.8 Pregnant 7 8.9 Pregnant 8 9.4 Pregnant Male 9 8.4 0 10 7.7 0 11 10.8 0 12 7.3 0 13 7.2 0 Lactation Female Male Female Male Female Male
period (period 2) 14 8.9 15 8.1 16 8.7 17 9.5 18 8.0 19 9.6 20 8.9 21 7.4
Post-lactation period (period Female 22 10.2 23 8.0 24 11.5 25 8.8 Male 26 7.4 27 7.9 28 8.6 29 7.5
Lactating 0 Lactating Lactating 0 0 Lactating 0 3) Post Post Post Post 25 50 25 0
lactating lactating lactating lactating
Total
Recording nights
Tracking date
Nights without gaps
First half of May Second half of May Second half of May Second half of May Second half of May Second half of May Second half of May Second half of May First half of May First half of May Second half of May Second half of May Second half of May
3 4 3 2 5 5 5 5 4 5 5 5 4
2 4 2 2 4 4 4 4 2 3 5 3 3
Second Second Second Second Second Second Second Second
5 5 3 5 3 3 5 5
4 4 2 4 3 3 4 4
3 4 6 8 7 4 6 5
2 3 3 4 4 3 3 2
132
94
half half half half half half half half
of of of of of of of of
June June June June June June June June
Second half of July First half of September First half of September First half of September Second half of July Second half of July First half of July First half of September
*The reproductive status of males is represented by the percentage of epididymal filling.
8% of the bats’ body mass and found no noticeable negative effects. As all of our radio-tagged bats were banded, we were able to check on their condition shortly after the tracking period. We recaptured most of the bats after the tracking period and found no negative effects such as mass loss or failure to reproduce. All transmitters were attached between the shoulder blades without clipping the fur using Skin-Bond1 (Smith & Nephew, Inc., Largo, Florida). The transmitters fell off after 3–8 days. During the tracking period, we monitored the bats’ behaviour continuously by homing in on the animals (White and Garrott 1990). This practice combined with previous experience allowed us to locate tagged bats. We observed all radio-tracked individuals with an infrared night scope (Filin 1 BN 2.5 56, Kiev, Ukraine) throughout the night to document flight time, as well as the number and location of individual foraging areas, within the feeding sites (Table 1). We visually classified about 70% of the in-
dividual foraging areas into five size classes (
