Nina I. Becker

Insectivorous Bats Digest Chitin in the Stomach Using Acidic Mammalian Chitinase

The gastrointestinal tract of animals is adapted to their primary source of food to optimize resource use and energy intake. Temperate bat species mainly feed on arthropods. These contain the energy-rich carbohydrate chitin, which is indigestible for the endogenous enzymes of a typical mammalian gastrointestinal tract. However, the gastrointestinal tract of bat species should be adapted to their diet and be able to digest chitin. We hypothesized that (i) European vespertilionid bat species have the digestive enzyme chitinase and that (ii) the chitinolytic activity is located in the intestine, as has been found for North American bat species. The gastrointestinal tracts of seven bat species (Pipistrellus pipistrellus, Plecotus auritus, Myotis bechsteinii, Myotis nattereri, Myotis daubentonii, Myotis myotis, and Nyctalus leisleri) were tested for chitinolytic activity by diffusion assay. Gastrointestinal tracts of P. pipistrellus, P. auritus, M. nattereri, M. myotis, and N. leisleri were examined for acidic mammalian chitinase by western blot analysis. Tissue sections of the gastrointestinal tract of P. pipistrellus were immunohistochemically analyzed to locate the acidic mammalian chitinase. Chitinolytic activity was detected in the stomachs of all bat species. Western blot analysis confirmed the acidic mammalian chitinase in stomach samples. Immunohistochemistry of the P. pipistrellus gastrointestinal tract indicated that acidic mammalian chitinase is located in the stomach chief cells at the base of the gastric glands. In conclusion, European vespertilionid bat species have acidic mammalian chitinase that is produced in the gastric glands of the stomach. Therefore, the gastrointestinal tracts of insectivorous bat species evolved an enzymatic adaptation to their diet.

Balancing the Energy Budget in Free-Ranging Male Myotis daubentonii Bats

Mammals use five main, mutually nonexclusive mechanisms to balance energy budgets: torpor, metabolic compensation, change in activity patterns, change in ingested energy, and/or variability in digestive efficiency. Bats, as small and actively flying mammals, have a high mass-specific energy demand; therefore, balancing mechanisms should be pronounced in this group. We found that male Myotis daubentonii exhibited marked variation in the relative importance of these different mechanisms during their period of seasonal activity in response to extrinsic (ambient temperature, insect abundance) and intrinsic (reproduction, body condition) factors. Cold ambient temperatures in spring facilitated long and frequent daily torpor bouts, whereas in early summer, increased energy intake was the dominant factor in energy balancing. Intake was further increased in late summer, when insect abundance was highest, and daily torpor bouts were shorter and less frequent than in early summer. In autumn, males used metabolic compensation to reduce their resting metabolic rate in addition to daily torpor. Metabolic compensation might be one of the mechanisms that allow males to maintain high body temperature during the day while decreasing the need for foraging time at night, thus maximizing their opportunities to mate.

Energetics and life-history of bats in comparison to small mammals

Mammals can be aligned along a slow-fast life-history continuum and a low–high metabolic rate continuum based on their traits. Small non-volant mammals occupy the fast/high end in both continua with high reproductive rates and short life spans linked with high mass-specific metabolic rates. Bats occupy the high end of the metabolic continuum, but the slow end of the life-history continuum with low reproductive rates and long life spans. Typically, both continua are linked, and similar life-history traits of species are reflected in more similar metabolic rates. We therefore hypothesized that metabolic rates are similar in species with similar life-history traits. Resting metabolic rates (RMR) were measured for three ecologically and morphologically similar sympatric bat species (Myotis nattereri, M. bechsteinii, and Plecotus auritus; Vespertilionidae) and compared to data from other similar-sized, temperate insectivorous mammals with other life-history strategies. The bat species share similar life-histories and RMRs, both of which differ from the remaining mammals and therefore supporting our hypothesis. To verify that bats are similar in RMR, two energetically contrasting periods were compared. RMRs in post-lactating females did not differ between bat species. It was, however, positively correlated with parasite load in both Myotis species. However, RMRs differed during energy-demanding pregnancy where M. nattereri had the significantly lowest RMR, suggesting metabolic compensation as an energy-saving strategy. We conclude that the energy requirements of bat species with similar life-history traits resemble each other during periods of low energetic demands and are more similar to each other than to other small temperate mammals.

Seasonal Variations of Wing Mite Infestations in Male Daubenton'S Bats (Myotis daubentonii) in Comparison to Female and Juvenile Bats

In this study, the physiological and behavioural factors that influence infestation levels of wing mites on a large sample of Daubentons bat (Myotis daubentonii) were investigated. This is the first study to present a comprehensive data set that includes male M. daubentonii over the entire seasonal activity period. In males, parasite load increased during spermatogenesis, which can be explained by high testosterone levels acting as an immunosuppressant. Prevalence rates and infestation levels in males were always lower than those of females and juveniles, possibly due to grooming behaviour which may be energetically restricted in females and inefficient in juveniles. Colony size did not appear to influence parasite load in males, but was found to have an influence in females and juveniles. Larger group sizes in males might not increase parasite load since grooming behaviour and roost switching are frequent. This study showed that parasite load in free-ranging Daubentons bats is sex-, season- and age-specific due to variations in behaviour and physiology.

The effects of reproductive state on digestive efficiency in three sympatric bat species of the same guild

The functional link between food as an energy source and metabolizable energy is the digestive tract. The digestive organs may change in size, structure, or retention time in response to energetic demands of the animal. Very efficient digestive tracts may be better at processing food but require higher energetic investments for maintenance even when post-absorptive. These costs influence the resting metabolic rate (RMR) that is defined as the energy necessary to fuel vital metabolic functions in a resting animal. In bats a trade-off between the necessity for a highly efficient digestive tract and moderate energetic maintenance costs may be particularly important. We hypothesized that low RMR coincides with low digestive efficiency (defined as apparent metabolizable energy coefficient (MEC)) and that phases of increased energetic demand are compensated for by increased digestive efficiency. We measured RMR and apparent MEC in the bats species Myotis nattereri, M. bechsteinii, and Plecotus auritus. In support of our hypothesis, M. nattereri has the lowest mass-specific RMR of the three species and the lowest apparent MEC. However, apparent MEC did not change during phases with differing energetic demands in any of the bat species, probably because bats operate at the limit of their sustainable energy demand.

Importance of multi-dimensional analyses of resource partitioning in highly mobile species assemblages

Resource partitioning is an essential mechanism enabling species coexistence. The resources that are used by an animal are linked to its morphology and ecology. Therefore, similar species should use similar resources. The ecological niche of an individual summarizes all used resources and is therefore composed of several dimensions. Many methods are established to study different dimensions of an animal’s niche. The aim of this study was to demonstrate that a combination of suitable methods is needed to study spatial and dietary resource partitioning of sympatric species in detail. We hypothesized that, while each individual method might identify differences between species, the combined results of several methods will lead to a more complete picture of spatial and dietary resource partitioning. As model organisms we chose the sympatric insectivorous bat species Myotis bechsteinii, M. nattereri, and P. auritus. We examined horizontal habitat use by telemetry, vertical habitat use by measuring δ13C, trophic position by measuring δ15N in wing membrane, and diet composition by molecular fecal analysis. Our results show that each method is able to provide information about spatial/dietary resource partitioning. However, considering further dimensions by combining several methods allows a more comprehensive assessment of dietary and spatial resource partitioning in bats.

Roost characteristics as indicators for heterothermic behavior of forest-dwelling bats

Many forest-dwelling bats spend their diurnal inactivity period in tree cavities. During this time bats can save energy through heterothermy. A heterothermic response (torpor) is characterized by a lowered body temperature, reduced metabolic rate, and reduction of other physiological processes, and can be influenced by the microclimatic conditions of roost cavities. The thermal and physical characteristics of roosts used by the sympatric, ecologically, and morphologically similar bat species Myotis bechsteinii, M. nattereri, and Plecotus auritus were compared. These three species differ in their heterothermic behavior, with the lowest skin temperatures observed for P. auritus. Therefore, we hypothesized that roosts occupied by the three species should differ in roost characteristics and microclimatic conditions, whereby P. auritus should select colder and thermally less stable roosts. The results showed that horizontal depth of the cavity, diameter of the roost tree, and microclimatic conditions within roosts differed among species. Roosts of P. auritus had the lowest horizontal depth, lowest thermal stability, and lowest mean minimum roost temperatures. Height of the roost, diameter of the roost tree, and vertical depth were also shown to influence microclimatic conditions. With increasing diameter of the tree and increasing horizontal depth, mean minimum roost temperature increased and thermal stability improved. Furthermore, with ascending height above ground insulation and mean roost temperatures increased. Our results imply that species such as P. auritus, which use pronounced torpor as a primary energy saving strategy, prefer colder cavities that support their heterothermic strategy.

Histological and histochemical analysis of the gastrointestinal tract of the common pipistrelle bat ( Pipistrellus pipistrellus)

Bats have a very high mass-specific energy demand due to small size and active flight. European bat species are mostly insectivorous and the morphology of the gastrointestinal (GI) tract should be adapted accordingly. This study investigated the general anatomy by histology and the function by analysing carbohydrate distribution in particular of the mucus of the GI tract of the insectivorous bat Pipistrellus pipistrellus. The GI tracts of three individuals were dissected, fixed in formaldehyde, and embedded in paraffin wax. The tissues and cells of the GI tract of P. pipistrellus were analysed by classical (acid alizarin blue, haematoxylin-eosin, and Masson Goldner Trichrome), histochemical (periodic acid-Schiff, Alcian blue at pH 2.5) and lectin histochemical (lectins WGA and HPA) staining procedures. The GI tract of P. pipistrellus is organised into the typical mammalian layers. The short, narrow, and thin-walled esophagus is simple with a folded stratified squamous epithelium without glands but mucous surface cells secreting neutral mucus. The stomach is globular shaped without specialisation. Mucous surface cells produced neutral mucus whereas neck and parietal cells secreted a mixture of neutral and acid mucus. Chief cell surface was positive for N-acetylglucosamine and the cytoplasm for N-acetylgalactosamine residues. The intestine lacked a caecum and appendix. The small intestine was divided into duodenum, jejunum-ileum and ileum-colon. The epithelium consisted of columnar enterocytes and goblet cells. The large intestine is short, only represented by the descending colon-rectum. It lacked villi and the mucosa had only crypts of Lieberkühn. Towards the colon-rectum, goblet cells produced mucus with N-acetylglucosamine residues increasing in acidity except in colon-rectum where acidity was highest in the base of crypts. Along the tube the surface of enterocytes was positive for N-acetylglucosamine and N-acetylgalactosamine. All over the mucus filling the lumen of the GI tract was positive for N-acetylglucosamine and increased in acidity in all parts except of the stomach. In conclusion, the simple GI tract showed an anatomical reduction of tissue enabling for a short retention time and a reduction of the load carried during flight: short GI tract, lack of lymphoid tissue, missing of glands in certain regions, and a distinct pattern of mucus distribution, indicating different physiological functions of these areas. The GI tract of P. pipistrellus was typical for an insectivorous species probably representing the ancestral condition.

LANDSCAPE FEATURES AND RESERVOIR OCCURRENCE AFFECTING THE RISK FOR EQUINE INFECTION WITH BORNA DISEASE VIRUS

Abstract Borna disease (BD) is a severe endemic and fatal disorder caused by the neurotropic Borna disease virus (BDV) which mainly occurs in horses and sheep. Borna disease virus belongs to the order Mononegavirales, which includes many reservoir-bound viruses with high zoonotic and pathogenic properties including the filoviruses and lyssaviruses. Clinically manifest BD occurs in endemic areas of Germany, Switzerland, Liechtenstein, and Austria. A seasonal accumulation of cases in spring and summer, incidences that vary from year to year, and the recent detection of BDV in bicolored shrews (Crocidura leucodon) in Swiss endemic areas argue for a natural reservoir. We established a geographic information system analysis of the distribution of 485 equine BD cases in Bavarian (Germany) endemic areas and of the occurrence of 285 records of C. leucodon captured in Bavaria. Boosted regression trees were used to identify driving factors of habitat choice and virus prevalence. The distribution model of C. leucodon and the prevalence model for BDV had very good accuracy. Mean annual precipitation <900 mm, mean annual temperatures of 8 C, elevation <350 m, low forest cover, and a high percentage of urban fabric and arable land describe the optimal habitat for C. leucodon. Occurrence probability of C. leucodon was significantly higher in Bavarian BDV-endemic areas than in random areas in Bavaria. The prevalence of BD was higher in urban areas with annual mean precipitation of 800–900 mm, annual mean temperature of 8 C, and elevation >500 m. Our results indicate that the distribution model can accurately predict BD occurrence. Based on these results, practical safety precautions could be derived. The BDV model represents a suitable system for reservoir-bound, neurotropic Mononegavirales because it allows analyzing ecologic and biologic aspects that determine virus abundance, maintenance in reservoir species, and transmission to end host species.

Silvicolous on a small scale: possibilities and limitations of habitat suitability models for small, elusive mammals in conservation management and landscape planning.

Species distribution and endangerment can be assessed by habitat-suitability modelling. This study addresses methodical aspects of habitat suitability modelling and includes an application example in actual species conservation and landscape planning. Models using species presence-absence data are preferable to presence-only models. In contrast to species presence data, absences are rarely recorded. Therefore, many studies generate pseudo-absence data for modelling. However, in this study model quality was higher with null samples collected in the field. Next to species data the choice of landscape data is crucial for suitability modelling. Landscape data with high resolution and ecological relevance for the study species improve model reliability and quality for small elusive mammals like Muscardinus avellanarius. For large scale assessment of species distribution, models with low-detailed data are sufficient. For regional site-specific conservation issues like a conflict-free site for new wind turbines, high-detailed regional models are needed. Even though the overlap with optimally suitable habitat for M. avellanarius was low, the installation of wind plants can pose a threat due to habitat loss and fragmentation. To conclude, modellers should clearly state the purpose of their models and choose the according level of detail for species and environmental data.