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Bats belong to the most gregarious and diverse mammals with highly complex social behaviors. Despite extensive research on their ecology and social behavior in some bat species, gained insights are restricted to only few of the more than 1300 species. In the recent past, bats have also become a central topic of a different branch of research: Since the 1990s bats came to the fore of virologists and immunologists due to the bats’ apparent importance as reservoir hosts and vectors of several (mostly tropical) diseases. While this research is focused mainly on emerging infectious diseases linked to bats, and their zoonotic potential, little has been invested regarding the link between disease transmission and bat social systems.
In my work, I aim at filling this gap by merging automated daily roosting observations, social network analysis, and a virological screening in Natterer’s bats (Myotis nattereri). In a collaborative approach, my co-workers and I analyzed the social structure of individually marked Natterer’s bats, their astrovirus detection rate and transmission pathways within their colony, as well as roosting interactions between different co-occurring con- and heterospecific bat colonies.
We discovered Natterer’s bats to display a very divergent social network structure that contradicts the findings of previous studies on large fission-fusion groups. Contrary to the modular social network structure found in e.g. primates or other bats species, the social network of Natterer’s bats consists of only one highly interconnected community. Moreover, although the close proximity between bat hosts in the colony should strongly promote direct transmission, we found indications that astrovirus infections follow at least partly an indirect transmission pathway via contaminated roost use. Lastly, our results prove that co-occurring con- and heterospecific bat colonies, e.g. as in this study Natterer’s bats, brown long-eared bats and Bechstein’s bats, can influence each other in their roost use by avoiding conspecific roosts and by being attracted towards those of heterospecifics. This holds implication for the transmission of parasites and pathogens within and between different colonies with opportunities for spillovers. To conclude, this multidisciplinary study led to valuable insights in the hitherto hidden mechanisms within and among bat colonies.
Lebenslang persistierende Neurogenese ist ein fester Bestandteil des olfaktorischen Systems bei reptanten Dekapoden („Panzerkrebse“; lat. reptans – kriechend; griech. deca – zehn, podes – Füße). Dabei generiert das deutocerebrale proliferative System über die Larvalphase hinaus neue Neuronen, die in die bestehenden neuronalen Netzwerke der deutocerebralen chemosensorischen Loben (auch „olfaktorische Loben“) integriert werden. Während in zahlreichen Studien die phänotypische Ausprägung, der zelluläre Mechanismus zur Umsetzung adulter Neurogenese und deren regulierende Faktoren umfassend untersucht und zum Teil kontrovers diskutiert wurden, ist über die phylogenetische Verbreitung in anderen Taxa der Malacostraca („Höhere Krebse“; griech. malakos – weich, ostrakon – Schale) nichts bekannt. Daher wurden im Rahmen der vorliegenden Arbeit verschiedene Vertreter aus Malakostrakentaxa mit unterschiedlicher phylogenetischer Position untersucht und unter evolutionären Aspekten diskutiert. Wie gezeigt werden konnte, ist adulte Neurogenese vermutlich ein plesiomorphes Merkmal der Eumalacostraca, welches in Vertretern der Euphausiacea („Leuchtgarnelen“; griech. phausis – Leuchten) und Peracarida („Ranzenkrebse“; griech. pera – Ranzen, karides – kleine Seekrebse) reduziert wurde. In Abhängigkeit von der zugrunde gelegten Verwandtschaftshypothese ist die Reduktion der persistierenden Neurogenese entweder mehrfach unabhängig (konvergent) erfolgt oder ein apomorphes Merkmal eines Monophylums aus Euphausiacea und Peracarida. Dagegen ist innerhalb der Decapoda eine Ausdehnung und strukturelle Erweiterung des deutocerebralen proliferativen Systems feststellbar. Um einen möglichen Zusammenhang zur Komplexität und Bedeutung des olfaktorischen Systems zu überprüfen, wurden zusätzlich die neuroanatomischen Merkmale von Vertretern der Decapoda und der Peracarida (am Beispiel der Amphipoda) vergleichend betrachtet. Dabei konnte innerhalb der Decapoda eine Korrelation zwischen der Entwicklung des deutocerebralen proliferativen Systems und der Evolution des akzessorischen Lobus bei Vertretern der Reptantia sowie dessen Reduktion in der Gruppe der Meiura, zu denen die Vertreter der Brachyura („Echte Krabben“; griech. brachys – kurz, oura – Schwanz) und Anomura („Mittelkrebse“; griech. anomalos – ungleich) gehören, festgestellt werden. Basierend auf diesen Ergebnissen wurden Vermutungen über die im Adultus neu generierten Neuronenklassen und somit über die Funktion adulter Neurogenese aufgestellt. In allen anderen untersuchten Taxa der Malacostraca konnte dagegen keine Korrelation mit der Komplexität des olfaktorischen Systems festgestellt werden.
Culicidae, auch bekannt als Stechmücken, sind medizinisch bedeutsame Zweiflügler, die als Vektoren eine Vielzahl von Krankheitserregern auf Menschen und Tiere übertragen können. Die vorliegende Arbeit beschäftigt sich einerseits mit der Verbreitung von zwei seltenen Stechmückenarten, welche im Rahmen eines Monitoringprojekts gefangen wurden, und andererseits mit der Ökologie der Asiatischen Tigermücke. Bei allen Arten handelt es sich um thermophile Arten, bei denen angenommen wird, dass der Klimawandel ihre Verbreitung Richtung Norden begünstigt. Dies konnte vor allem für die Art Uranotaenia unguiculata gezeigt werden, da sie an zwei Orten gefunden wurde, die ausgesprochen weit entfernt waren von der einzigen jemals zuvor beschriebenen Nachweisstelle in Deutschland. Obwohl an beiden Fundorten jeweils nur ein einziges adultes Individuum gefangen werden konnte, ergab eine Beprobung von potenziellen Bruthabitaten im darauffolgenden Jahr, dass lokale Reproduktion stattfand. Somit konnte eine ausschließliche Verschleppung von adulten Einzelindividuen weitgehend ausgeschlossen werden. Eine weitere seltene Stechmückenart, die im Zuge des Monitorings nachgewiesen werden konnte, ist Anopheles algeriensis. Diese Art wurde an drei Standorten gefangen, an zwei von ihnen mit einer viel höheren Abundanz als Ur. unguiculata.
Den ökologischen Teil dieser Arbeit machen Feld- und Laborexperimente mit Aedes albopictus aus. Sie dienten der Ermittlung der Kältetoleranz der Eier dieser Spezies, die als Vektor für eine Vielzahl von Viren und andere Pathogene gilt. Drei verschiedene Stämme, die aus tropischen, subtropischen und gemäßigten Breiten stammen, wurden niedrigen Temperaturen, welche typischerweise im Winter herrschen, unter Feld- und Laborbedingungen ausgesetzt. Die Experimente belegen, dass alle untersuchten Stämme prinzipiell einen Winter mit einem Temperaturminimum von –8 °C im Feld überleben konnten. Die Laborexperimente konnten hingegen zeigen, dass alle Stämme in der Lage waren, Temperaturen von –10 °C für eine gewisse Zeit zu ertragen. Die Überlebensfähigkeit schwankte je nach Stamm zwischen 2 und 20 Tagen. Dabei hatte der Stamm aus den gemäßigten Breiten eine Kältetoleranz, die nur wenig höher lag als die des subtropischen Stammes. Der tropische Stamm hingegen besaß die geringste Toleranz gegenüber niedrigen Temperaturen, sowohl in den Freiland- als auch in den Laborexperimenten. Diapausierende Eier zeigen nur eine höhere Kältetoleranz nahe den physiologischen Grenzen der jeweiligen Stämme. Weiterhin konnte festgestellt werden, dass Eier unter fluktuierenden Temperaturen eine bestimmte Minimaltemperatur länger aushalten konnten als unter konstanten Temperaturen. Somit zeigen beide Experimente, dass gewisse Stämme von Ae. albopictus eine sehr hohe Toleranz gegenüber niedrigen Temperaturen haben. Das macht es sehr wahrscheinlich, dass diese invasive Art Winter in Deutschland oder anderen mitteleuropäischen Ländern überleben und ihre Ausbreitung weiter fortschreiten werden. Diese Entwicklung wird epidemiologische Auswirkungen auf die Human- und Veterinärmedizin haben.
Abstract
While chemical communication has been investigated intensively in vertebrates and insects, relatively little is known about the sensory world of spiders despite the fact that chemical cues play a key role in natural and sexual selection in this group. In insects, olfaction is performed with wall–pore and gustation with tip‐pore sensilla. Since spiders possess tip‐pore sensilla only, it is unclear how they accomplish olfaction. We scrutinized the ultrastructure of the trichoid tip‐pore sensilla of the orb weaving spider Argiope bruennichi—a common Palearctic species the males of which are known to be attracted by female sex pheromone. We also investigated the congener Argiope blanda. We examined whether the tip‐pore sensilla differ in ultrastructure depending on sex and their position on the tarsi of walking legs of which only the distal parts are in contact with the substrate. We hypothesized as yet undetected differences in ultrastructure that suggest gustatory versus olfactory functions. All tarsal tip‐pore sensilla of both species exhibit characters typical of contact‐chemoreceptors, such as (a) the presence of a pore at the tip of the sensillum shaft, (b) 2–22 uniciliated chemoreceptive cells with elongated and unbranched dendrites reaching up to the tip‐pore, (c) two integrated mechanoreceptive cells with short dendrites and large tubular bodies attached to the sensillum shaft's base, and (d) a socket structure with suspension fibres that render the sensillum shaft flexible. The newly found third mechanoreceptive cell attached to the proximal end of the peridendritic shaft cylinder by a small tubular body was likely overlooked in previous studies. The organization of tarsal tip‐pore sensilla did not differ depending on the position on the tarsus nor between the sexes. As no wall‐pore sensilla were detected, we discuss the probability that a single type of sensillum performs both gustation and olfaction in spiders.
Abstract
Spiders of the genus Micaria are ground‐living mimics of ants. Species delineation in these spiders is challenging, mainly because of exceptional high levels of intraspecific variation masking species boundaries. As implied by preliminary DNA barcode data from Central Europe, the Holarctic and very widely distributed glossy ant‐spider M. pulicaria shows cryptic diversity. Here, we disentangle the hidden diversity by means of an integrative taxonomy approach, using mitochondrial DNA, morphometrics, traditional genitalic characters and ecology. Our data suggest the clear delineation of two distinct species, which supports the conception of 19th century taxonomists. These early naturalists distinguished M. pulicaria and a second closely related species based on morphology and natural history, which were synonymized in subsequent taxonomic studies. Therefore, we re‐circumscribe M. pulicaria and revalidate the long forgotten M. micans. These two Micaria species co‐occur sympatrically in vast areas of the western Palearctic, while the Nearctic region is populated by M. pulicaria alone. Male genitalic traits are more dissimilar in the area of sympatry than in allopatry, suggesting a decisive role of reproductive character displacement in species diversification. Our study emphasizes the value of the early taxonomic literature in integrative taxonomic studies, as it may contain crucial information on natural history that are not regularly recorded by modern taxonomists.
Changes in food characteristics reveal indirect effects of lake browning on zooplankton performance
(2020)
Abstract
Browning caused by colored dissolved organic matter is predicted to have large effects on aquatic ecosystems. However, there is limited experimental evidence about direct and indirect effects of browning on zooplankton in complex field settings. We used a combination of an ecosystem‐scale enclosure experiment and laboratory incubations to test how prolonged browning affects physiological and life‐history traits of the water flea Daphnia longispina, a key species in lake food webs, and whether any such effects are reversible. Daphnids and water were collected from enclosures in a deep clear‐water lake, where the natural plankton community had been exposed for 10 weeks to browning or to control conditions in clear water. Daphnid abundance was much lower in the brown than in the clear enclosure. Surprisingly, however, daphnids continuously kept in brown enclosure water in the laboratory showed increased metabolic performance and survival, and also produced more offspring than daphnids kept in clear enclosure water. This outcome was related to more and higher‐quality seston in brown compared to clear water. Moreover, daphnids transferred from clear to brown water or vice versa adjusted their nucleic acid and protein contents, as indicators of physiological state, to similar levels as individuals previously exposed to the respective recipient environment, indicating immediate and reversible browning effects on metabolic performance. These results demonstrate the importance of conducting experiments in settings that capture both indirect effects (i.e., emerging from species interactions in communities) and direct effects on individuals for assessing impacts of browning and other environmental changes on lakes.
In a changing world, phytoplankton communities face a large variety of challenges including altered light regimes. These alterations are caused by more pronounced stratification due to rising temperatures, enhanced eutrophication, and browning of lakes. Community responses toward these effects can emerge as alterations in physiology, biomass, biochemical composition, or diversity. In this study, we addressed the combined effects of changes in light and nutrient conditions on community responses. In particular, we investigated how light intensity and variability under two nutrient conditions influence (1) fast responses such as adjustments in photosynthesis, (2) intermediate responses such as pigment adaptation and (3) slow responses such as changes in community biomass and species composition. Therefore, we exposed communities consisting of five phytoplankton species belonging to different taxonomic groups to two constant and two variable light intensity treatments combined with two levels of phosphorus supply. The tested phytoplankton communities exhibited increased fast reactions of photosynthetic processes to light variability and light intensity. The adjustment of their light harvesting mechanisms via community pigment composition was not affected by light intensity, variability, or nutrient supply. However, pigment specific effects of light intensity, light variability, and nutrient supply on the proportion of the respective pigments were detected. Biomass was positively affected by higher light intensity and nutrient concentrations while the direction of the effect of variability was modulated by light intensity. Light variability had a negative impact on biomass at low, but a positive impact at high light intensity. The effects on community composition were species specific. Generally, the proportion of green algae was higher under high light intensity, whereas the cyanobacterium performed better under low light conditions. In addition to that, the diatom and the cryptophyte performed better with high nutrient supply while the green algae as well as the cyanobacterium performed better at low nutrient conditions. This shows that light intensity, light variability, and nutrient supply interactively affect communities. Furthermore, the responses are highly species and pigment specific, thus to clarify the effects of climate change a deeper understanding of the effects of light variability and species interactions within communities is important.
Recent climate change and its consequences for living organisms constitute one of the greatest problems of our century. Global warming entails an increase in mean temperature and the frequencies of extreme weather events. Those changes in environmental conditions affect both plants and animals. Because of their inability to escape from unsuitable environments, plants have evolved a wide spectrum of molecular programs to protect themselves against changing conditions. Responding on altered environmental conditions will change plants chemical composition and therefore also affect plants interaction with other species (e.g., predator-prey or symbiotic relationships). For instance, changes in the chemical composition of plants may influence the survival of associated herbivores. In other words, these herbivores will be affected indirectly by climate change due to changes in the suitability / quality of their food. The aim of this doctoral thesis was to discover the effects of climate change within the relationship of the butterfly Pieris napi and its host plant (Sinapis alba used here as host plant), including individual conditions (e.g. chemical compositions of plants; morphology, physiology of the butterfly) and behavior of female butterflies and larvae. In the first experiment, the influence of simulated climate change on the chemical composition of the plant Sinapis alba was investigated. The second experiment aimed to examine the influence of changes in plant composition on the butterfly P. napi. Glucosinolates (secondary compound of plants) are known to have an important effect on the preference and performance of herbivores. Therefore, in the third experiment, the impact of glucosinolates on the preference and performance of P. napi was investigated in order to see if these plant compounds had the most important influence on this butterfly. Furthermore, in the fourth experiment, it was explored whether there is a latitudinal gradient within the species´ responses to changes in its host plant. The fifth and last experiment aimed to examine, if there are general principles across species regarding indirect effects of climate change.
Climate change, simulated by different combinations of temperature and water regimes, had an effect on the plant chemistry. The combination of temperature and water availability changed plant composition substantially. Especially the amount of carbon and glucosinolates (here above all sinalbin) in S. alba plants varies between the different treatments and therefore between the different combinations of temperature and water regimes. Regarding glucosinolates, elevated temperatures increased their concentration in leaves, whereas water deficit in combination with higher temperature reversed this pattern. For carbon content, all plants, except those of the control group, showed a decreased amount of total carbon. However, simulated heat waves had no effect on plants, leading to the assumption that the plants were able to recover from heat stress sufficiently during the control phases. Changes in plant composition affected both larvae and females of the butterfly P. napi. Therefore, changed host-plant chemistry alters the plant quality for this herbivore, meaning that plants of different treatments represent different plant qualities defined by their composition. Females of P. napi may be able to differentiate between plant qualities and even show a direct preference. Therefore, glucosinolates seem to act as oviposition stimulants. However, preferring another plant quality with lower amount of glucosinolates suggest that females of this butterfly species were attracted by more than high levels of glucosinolates alone. Larvae fed with different plant qualities performed differently, indicated by smaller wings (lighter bodies) and prolonged development when fed with plants contained higher amount of the glucosinolate sinalbin. It can be assumed that a higher amount of sinalbin decreases the quality of the host plant and therefore lead to these responses. Probably larvae need to shift their resources from growth to detoxification and therewith survival. Furthermore, drought conditions during plant growth seem to reduce the overall negative effects of higher temperatures, lead to an increase of host plant quality. Larvae seem to benefit from feeding on these “double-stressed” plants. Comparison between the results of the preference and performance tests suggests that there might be a mismatch between female preference and larval performance. It seems that the stimulating effect of high concentration of glucosinolates, in this case sinalbin, misdirects females´ decision to less suitable host plants, meaning that the advantage of less competition for larvae come at costs through detoxification. Using Brassica napus plants with genetically fixed glucosinolate levels, it could be demonstrate that there must be other plant components influencing females´ oviposition behavior been seen in the choice experiment with S. alba. The comparison of German and Italian populations to changes in host-plant quality showed fewer differences between countries as expected. However, German and Italian individuals differed in their reaction to altered plant quality, at least in developmental time and larval growth rate. It seems that Italian larvae benefitted from plants grown under higher temperatures, whereas drought-stressed plants affected them negatively. German individuals in contrast seem to benefit only from water stress during plant growth. With regard to the sexes of P. napi, it seems that females respond differently than males to changes in plant quality. Furthermore, the results of the performance test on Bicyclus anynana showed that there might be some general principles for the respond of butterflies to changes of its host plant. B. anynana responded in a similar way to different host plant qualities as P. napi did, meaning that plants grown under higher temperatures and drought conditions seem to be beneficial for the larval performance.
In summary, these findings may have important implications for the indirect effects of climate change on this butterfly in natural environments. First, climate change seems to have an impact on the chemical composition of plants. Second, changes in plants caused by increasing temperature and droughts seem to influence the preference and performance of this butterfly. However, there are differences between populations, which seem to be induced by former adaptation. And third, there might be some general principles for the respond of butterflies to changes in their host plants. This thesis focuses only on possible indirect effects of climate change. However, there are direct effects, which may alter the responses of herbivores to changes in their host plant as well. Therefore, further investigations in this linkage and in other plant-herbivore relationships will be necessary to explore how climate change may alter the relationship between herbivores and their hosts.
Abstract
Improving our sparse knowledge of the mating and reproductive behaviour of white rhinoceros (Ceratotherium simum Burchell, 1817) is essential for the effective conservation of this iconic species. By combining morphological, physiological and habitat data with paternity assignments of 104 known mother–offspring pairs collected over a period of 13 years, we provide the most comprehensive analysis of the mating system in this species. We show that while the overall mating system was promiscuous, and both males and females produced more offspring when mating with several partners, half of all females with multiple offspring were monogamous. Additionally, we find that mating and reproductive success varied significantly among territorial males in two independent sets of males. In females, however, variation in the mating and the reproductive success was not larger than expected by random demographic fluctuations. Horn size, testosterone metabolite concentration, territory size, habitat openness and the volume of preferred food within the territory did not seem to influence male mating or reproductive success. Moreover, there was no sign of inbreeding avoidance: females tended to mate more frequently with closely related males, and one daughter produced a progeny with her father. The lack of inbreeding avoidance, in combination with the skew in male reproductive success, the partial monogamy in females and the territorial‐based mating system, jeopardizes the already low genetic variation in the species. Considering that the majority of populations are restricted to fenced reserves and private farms, we recommend taking preventive measures that aim to reduce inbreeding in white rhinoceros. A video abstract can be viewed here.
Differences in salinity are boundaries that act as barriers for the dispersal of most aquatic organisms. This creates distinctive biota in freshwater and brackish water (mesohaline) environments. To test how saline boundaries influence the diversity and composition of host-associated microbiota, we analyzed the microbiome within the digestive tract of Theodoxus fluviatilis, an organism able to cross the freshwater and mesohaline boundary. Alpha-diversity measures of the microbiome in freshwater and brackish water were not significantly different. However, the composition of the bacterial community within freshwater T. fluviatilis differed significantly compared with mesohaline T. fluviatilis and typical bacteria could be determined for the freshwater and the mesohaline digestive tract microbiome. An artificial increase in salinity surrounding these freshwater snails resulted in a strong change in the bacterial community and typical marine bacteria became more pronounced in the digestive tract microbiome of freshwater T. fluviatilis. However, the composition of the digestive tract microbiome in freshwater snails did not converge to that found within mesohaline snails. Within mesohaline snails, no cardinal change was found after either an increase or decrease in salinity. In all samples, Pseudomonas, Pirellula, Flavobacterium, Limnohabitans, and Acinetobacter were among the most abundant bacteria. These bacterial genera were largely unaffected by changes in environmental conditions. As permanent residents in T. fluviatilis, they may support the digestion of the algal food in the digestive tract. Our results show that freshwater and mesohaline water host-associated microbiomes respond differently to changes in salinity. Therefore, the salinization of coastal freshwater environments due to a rise in sea level can influence the gut microbiome and its functions with currently unknown consequences for, e.g., nutritional physiology of the host.