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Extra-organismal DNA (eoDNA) from material left behind by organisms (noninvasive DNA, e.g., feces, hair) or from environmental samples (eDNA, e.g., water, soil) is a valuable source of genetic information. However, the relatively low quality and quantity of eoDNA, which can be further degraded by environmental factors, results in reduced amplification and sequencing success. This is often compensated for through cost- and time-intensive replications of genotyping/sequencing procedures. Therefore, system- and site-specific quantifications of environmental degradation are needed to maximize sampling efficiency (e.g., fewer replicates, shorter sampling durations), and to improve species detection and abundance estimates. Using 10 environmentally diverse bat roosts as a case study, we developed a robust modeling pipeline to quantify the environmental factors degrading eoDNA, predict eoDNA quality, and estimate sampling-site-specific ideal exposure duration. Maximum humidity was the strongest eoDNA-degrading factor, followed by exposure duration and then maximum temperature. We also found a positive effect when hottest days occurred later. The strength of this effect fell between the strength of the effects of exposure duration and maximum temperature. With those predictors and information on sampling period (before or after offspring were born), we reliably predicted mean eoDNA quality per sampling visit at new sites with a mean squared error of 0.0349. Site-specific simulations revealed that reducing exposure duration to 2–8 days could substantially improve eoDNA quality for future sampling. Our pipeline identified high humidity and temperature as strong drivers of eoDNA degradation even in the absence of rain and direct sunlight. Furthermore, we outline the pipeline's utility for other systems and study goals, such as estimating sample age, improving eDNA-based species detection, and increasing the accuracy of abundance estimates.
BatNet: a deep learning-based tool for automated bat species identification from camera trap images
(2023)
Automated monitoring technologies can increase the efficiency of ecological data collection and support data-driven conservation. Camera traps coupled with infrared light barriers can be used to monitor temperate-zone bat assemblages at underground hibernacula, where thousands of individuals of multiple species can aggregate in winter. However, the broad-scale adoption of such photo-monitoring techniques is limited by the time-consuming bottleneck of manual image processing. Here, we present BatNet, an open-source, deep learning-based tool for automated identification of 13 European bat species from camera trap images. BatNet includes a user-friendly graphical interface, where it can be retrained to identify new bat species or to create site-specific models to improve detection accuracy at new sites. Model accuracy was evaluated on images from both trained and untrained sites, and in an ecological context, where community- and species-level metrics (species diversity, relative abundance, and species-level activity patterns) were compared between human experts and BatNet. At trained sites, model performance was high across all species (F1-score: 0.98–1). At untrained sites, overall classification accuracy remained high (96.7–98.2%), when camera placement was comparable to the training images (<3 m from the entrance; <45° angle relative to the opening). For atypical camera placements (>3 m or >45° angle), retraining the detector model with 500 site-specific annotations achieved an accuracy of over 95% at all sites. In the ecological case study, all investigated metrics were nearly identical between human experts and BatNet. Finally, we exemplify the ability to retrain BatNet to identify a new bat species, achieving an F1-score of 0.99 while maintaining high classification accuracy for all original species. BatNet can be implemented directly to scale up the deployment of camera traps in Europe and enhance bat population monitoring. Moreover, the pretrained model can serve as a baseline for transfer learning to automatize the image-based identification of bat species worldwide.
Introduction: At the cellular level, acute temperature changes alter ionic conductances, ion channel kinetics, and the activity of entire neuronal circuits. This can result in severe consequences for neural function, animal behavior and survival. In poikilothermic animals, and particularly in aquatic species whose core temperature equals the surrounding water temperature, neurons experience rather rapid and wide-ranging temperature fluctuations. Recent work on pattern generating neural circuits in the crustacean stomatogastric nervous system have demonstrated that neuronal circuits can exhibit an intrinsic robustness to temperature fluctuations. However, considering the increased warming of the oceans and recurring heatwaves due to climate change, the question arises whether this intrinsic robustness can acclimate to changing environmental conditions, and whether it differs between species and ocean habitats.
Methods: We address these questions using the pyloric pattern generating circuits in the stomatogastric nervous system of two crab species, Hemigrapsus sanguineus and Carcinus maenas that have seen a worldwide expansion in recent decades.
Results and discussion: Consistent with their history as invasive species, we find that pyloric activity showed a broad temperature robustness (>30°C). Moreover, the temperature-robust range was dependent on habitat temperature in both species. Warm-acclimating animals shifted the critical temperature at which circuit activity breaks down to higher temperatures. This came at the cost of robustness against cold stimuli in H. sanguineus, but not in C. maenas. Comparing the temperature responses of C. maenas from a cold latitude (the North Sea) to those from a warm latitude (Spain) demonstrated that similar shifts in robustness occurred in natural environments. Our results thus demonstrate that neuronal temperature robustness correlates with, and responds to, environmental temperature conditions, potentially preparing animals for changing ecological conditions and shifting habitats.
Background
Haemosporidian parasites of the genus Polychromophilus infect bats worldwide. They are vectored by obligate ectoparasitic bat flies of the family Nycteribiidae. Despite their global distribution, only five Polychromophilus morphospecies have been described to date. The two predominant species, Polychromophilus melanipherus and Polychromophilus murinus, are broadly distributed and mainly infect miniopterid and vespertilionid bats, respectively. In areas where species from different bat families aggregate together, the infection dynamics and ability of either Polychromophilus species to infect other host families is poorly characterized.
Methods
We collected 215 bat flies from two bat species, Miniopterus schreibersii and Rhinolophus ferrumequinum, which sometimes form mixed clusters in Serbia. Miniopterus schreibersii is known to be frequently infected with P. melanipherus, whereas R. ferrumequinum has been observed to be incidentally infected with both Polychromophilus species. All flies were screened for Polychromophilus infections using a PCR targeting the haemosporidian cytb gene. Positive samples were subsequently sequenced for 579 bp of cytochrome b (cytb) and 945 bp of cytochrome oxidase subunit 1 (cox1).
Results
Polychromophilus melanipherus DNA was detected at six out of nine sampling locations and in all three examined bat fly species collected from M. schreibersii (Nycteribia schmidlii, n = 21; Penicillidia conspicua, n = 8; Penicillidia dufourii, n = 3). Four and five haplotypes were found for cytb and cox1, respectively. Evidence for multiple Polychromophilus haplotypes was found in 15 individual flies. These results point to a high diversity of P. melanipherus parasites in Miniopterus hosts and efficient transmission throughout the study area. A single Phthiridium biarticulatum bat fly collected from R. ferrumequinum screened positive for P. melanipherus, but only yielded a partial cox1 sequence fragment. Nevertheless, this result suggests that secondary hosts (both bat and fly species) are regularly confronted with this parasite.
Conclusions
The results of this study provide new insights into the prevalence and distribution of Polychromophilus parasites in European bats and their nycteribiid vectors. The use of bat flies for the non-invasive investigation of Polychromophilus infections in bat populations has proven to be efficient and thus represents an alternative for large-scale studies of infections in bat populations without the need to invasively collect blood from bats.
Lacewings (Neuroptera) have predatory larvae with highly specialised mouthparts. Larvae of many groups within Neuroptera are well represented as fossils preserved in ambers; however, larvae of some groups are less often reported in the literature. Here we report such a rare case, a larva of the group Hemerobiidae, an aphidlion, preserved in a piece of Eocene Baltic amber (about 40 million years old). It is preserved together with three possible prey items, wingless aphids, most likely representatives of Germaraphis (or at least closely related to this group). The aphidlion can be identified based on the morphology of the antennae, simple curved and toothless stylets, well developed labial palps, and the absence of other mouth-part structures such as a protruding labrum or maxillary palps. A long, club-shaped distal element of the labial palps identifies the specimen as a larva of Hemerobiidae. The aphids can be identified based on their very long, beak-like mouth parts. This find is, to our knowledge, the first example of a lacewing larva preserved together with its potential prey. We briefly discuss other cases in which fossils preserved in amber allow us to reconstruct aspects of behaviour and interactions of fossil lacewing larvae.
Copulatory mechanics of ghost spiders reveals a new self-bracing mechanism in entelegyne spiders
(2023)
Spiders evolved a distinctive sperm transfer system, with the male copulatory organs located on the tarsus of the pedipalps. In entelegyne spiders, these organs are usually very complex and consist of various sclerites that not only allow the transfer of the sperm themselves but also provide a mechanical interlock between the male and female genitalia. This interlocking can also involve elements that are not part of the copulatory organ such as the retrolateral tibial apophysis (RTA)—a characteristic of the most diverse group of spiders (RTA clade). The RTA is frequently used for primary locking i.e., the first mechanical engagement between male and female genitalia. Despite its functional importance, some diverse spider lineages have lost the RTA, but evolved an apophysis on the femur instead. It can be hypothesized that this femoral apophysis is a functional surrogate of the RTA during primary locking or possibly serves another function, such as self-bracing, which involves mechanical interaction between male genital structures themselves to stabilize the inserted pedipalp. We tested these hypotheses using ghost spiders of the genus Josa (Anyphaenidae). Our micro-computed tomography data of cryofixed mating pairs show that the primary locking occurs through elements of the copulatory organ itself and that the femoral apophysis does not contact the female genitalia, but hooks to a projection of the copulatory bulb, representing a newly documented self-bracing mechanism for entelegyne spiders. Additionally, we show that the femoral self-bracing apophysis is rather uniform within the genus Josa. This is in contrast to the male genital structures that interact with the female, indicating that the male genital structures of Josa are subject to different selective regimes.
Geometric regularity of spider webs has been intensively studied in orb‐weaving spiders, although it is not exclusive of orb weavers. Here, we document the geometrically regular, repetitive elements in the webs of the non‐orb‐weaving groups Leptonetidae and Telemidae for the first time. Similar to orb weavers, we found areas with regularly spaced parallel lines in the webs of Calileptoneta helferi, Sulcia sp., and cf. Pinelema sp. Furthermore, we provide a detailed account of the regular webs of Ochyrocera (Ochyroceratidae). The sections of the web with regularly disposed parallel lines are built as U‐shaped modules reminiscent of orb webs. It has been suggested that the regularly spaced parallel lines in the webs of Ochyroceratidae and Psilodercidae may be produced in a single sweep of their posterior lateral spinnerets, which have regularly spaced aciniform gland spigots, perhaps involving expansion of the spinnerets. To test this hypothesis, we compared the spacing between parallel lines with the spacing between spigots, searched for expansible membranes in the spinnerets, and examined the junctions of regularly spaced lines. The distance between parallel lines was 10–20 times the distance between spigots, and we found no expansible membranes, and the intersection of parallel lines are cemented, which opposes the single sweep hypothesis. Furthermore, we found cues of viscid silk in the parallel lines of the psilodercid Althepus and broadened piriform gland spigots that may be responsible of its production. Finally, we evaluated the presence or absence of geometrically regular web elements across the spider tree of life. We found reports of regular webs in 31 spider families, including 20 families that are not orb weavers and hypothesize that the two basic aspects of regularity (parallel lines spaced at regular intervals, and radial lines spaced at regular angles) probably appeared many times in the evolution of spiders.
Background
Hibernation allows species to conserve energy and thereby bridge unfavorable environmental conditions. At the same time, hibernation imposes substantial ecological and physiological costs. Understanding how hibernation timing differs within and between species can provide insights into the underlying drivers of this trade-off. However, this requires individualized long-term data that are often unavailable. Here, we used automatic monitoring techniques and a reproducible analysis pipeline to assess the individualized hibernation phenology of two sympatric bat species. Our study is based on data of more than 1100 RFID-tagged Daubenton’s bats (Myotis daubentonii) and Natterer’s bats (Myotis nattereri) collected over seven years at a hibernaculum in Germany. We used linear mixed models to analyze species-, sex- and age-specific differences in entrance, emergence and duration of the longest continuous period spent in the hibernaculum.
Results
Overall, Daubenton’s bats entered the hibernaculum earlier and emerged later than Natterer’s bats, resulting in a nearly twice as long hibernation duration. In both species, adult females entered earlier and emerged from hibernation later than adult males. Hibernation duration was shorter for juveniles than adults with the exception of adult male Natterer’s bats whose hibernation duration was shortest of all classes. Finally, hibernation timing differed among years, but yearly variations in entrance and emergence timing were not equally shifted in both species.
Conclusions
Our results suggest that even in sympatric species, and across sex and age classes, hibernation timing may be differentially affected by environmental conditions. This highlights the necessity of using individualized information when studying the impact of changing environments on hibernation phenology.
Background
Pycnogonida (sea spiders) is the sister group of all other extant chelicerates (spiders, scorpions and relatives) and thus represents an important taxon to inform early chelicerate evolution. Notably, phylogenetic analyses have challenged traditional hypotheses on the relationships of the major pycnogonid lineages (families), indicating external morphological traits previously used to deduce inter-familial affinities to be highly homoplastic. This erodes some of the support for phylogenetic information content in external morphology and calls for the study of additional data classes to test and underpin in-group relationships advocated in molecular analyses. In this regard, pycnogonid internal anatomy remains largely unexplored and taxon coverage in the studies available is limited.
Results
Based on micro-computed X-ray tomography and 3D reconstruction, we created a comprehensive atlas of in-situ representations of the central nervous system and midgut layout in all pycnogonid families. Beyond that, immunolabeling for tubulin and synapsin was used to reveal selected details of ganglionic architecture. The ventral nerve cord consistently features an array of separate ganglia, but some lineages exhibit extended composite ganglia, due to neuromere fusion. Further, inter-ganglionic distances and ganglion positions relative to segment borders vary, with an anterior shift in several families. Intersegmental nerves target longitudinal muscles and are lacking if the latter are reduced. Across families, the midgut displays linear leg diverticula. In Pycnogonidae, however, complex multi-branching diverticula occur, which may be evolutionarily correlated with a reduction of the heart.
Conclusions
Several gross neuroanatomical features are linked to external morphology, including intersegmental nerve reduction in concert with trunk segment fusion, or antero-posterior ganglion shifts in partial correlation to trunk elongation/compaction. Mapping on a recent phylogenomic phylogeny shows disjunct distributions of these traits. Other characters show no such dependency and help to underpin closer affinities in sub-branches of the pycnogonid tree, as exemplified by the tripartite subesophageal ganglion of Pycnogonidae and Rhynchothoracidae. Building on this gross anatomical atlas, future studies should now aim to leverage the full potential of neuroanatomy for phylogenetic interrogation by deciphering pycnogonid nervous system architecture in more detail, given that pioneering work on neuron subsets revealed complex character sets with unequivocal homologies across some families.
Whether species can cope with environmental change depends considerably on their life history. Bats have long lifespans and low reproductive rates which make them vulnerable to environmental changes. Global warming causes Bechstein’s bats (Myotis bechsteinii) to produce larger females that face a higher mortality risk. Here, we test whether these larger females are able to offset their elevated mortality risk by adopting a faster life history. We analysed an individual-based 25-year dataset from 331 RFID-tagged wild bats and combine genetic pedigrees with data on survival, reproduction and body size. We find that size-dependent fecundity and age at first reproduction drive the observed increase in mortality. Because larger females have an earlier onset of reproduction and shorter generation times, lifetime reproductive success remains remarkably stable across individuals with different body sizes. Our study demonstrates a rapid shift to a faster pace of life in a mammal with a slow life history.
Background
Pholcidae represent one of the largest and most diverse spider families and have been subject to various studies regarding behavior and reproductive biology. In contrast to the solid knowledge on phylogeny and general reproductive morphology, the primary male reproductive system is strongly understudied, as it has been addressed only for few species. Those studies however suggested a high diversity of sperm and seminal secretions across the family. To address this disparity and reconstruct the evolution of sperm traits, we investigate the primary male reproductive system of pholcid spiders by means of light, X-ray, and transmission electron microscopy using a comprehensive taxon sampling with 46 species from 33 genera, representing all five subfamilies.
Results
Our data show a high disparity of sperm morphology and seminal secretions within pholcids. We document several sperm characters that are unique for pholcids, such as a helical band (Pholcinae) or a lamellate posterior centriolar adjunct material (Modisiminae). Character mapping revealed several putative synapomorphies for individual taxa. With regard to sperm transfer forms, we found that synspermia occur only in the subfamily Ninetinae, whereas the other subfamilies have cleistospermia. In several species with cleistospermia, we demonstrate that spermatids remain fused until late stages of spermiogenesis before ultimately separating shortly before the coiling process. Additionally, we explored the previously hypothesized correlation between sperm size and minimum diameter of the spermophor in the male palpal organ. We show that synspermia differ strongly in size whereas cleistospermia are rather uniform, but neither transfer form is positively correlated with the diameter of the spermophor.
Conclusions
Our data revealed a dynamic evolution of sperm characters, with convergences across all subfamilies and a high level of homoplasy. The present diversity can be related to subfamily level and allows for assignments of specific subtypes of spermatozoa. Our observations support the idea that Ninetinae are an ancestral clade within Pholcidae that have retained synspermia and that synspermia represent the ancestral sperm transfer form of Pholcidae.
Background
Phylogenomic studies over the past two decades have consolidated the major branches of the arthropod tree of life. However, especially within the Chelicerata (spiders, scorpions, and kin), interrelationships of the constituent taxa remain controversial. While sea spiders (Pycnogonida) are firmly established as sister group of all other extant representatives (Euchelicerata), euchelicerate phylogeny itself is still contested. One key issue concerns the marine horseshoe crabs (Xiphosura), which recent studies recover either as sister group of terrestrial Arachnida or nested within the latter, with significant impact on postulated terrestrialization scenarios and long-standing paradigms of ancestral chelicerate traits. In potential support of a nested placement, previous neuroanatomical studies highlighted similarities in the visual pathway of xiphosurans and some arachnopulmonates (scorpions, whip scorpions, whip spiders). However, contradictory descriptions of the pycnogonid visual system hamper outgroup comparison and thus character polarization.
Results
To advance the understanding of the pycnogonid brain and its sense organs with the aim of elucidating chelicerate visual system evolution, a wide range of families were studied using a combination of micro-computed X-ray tomography, histology, dye tracing, and immunolabeling of tubulin, the neuropil marker synapsin, and several neuroactive substances (including histamine, serotonin, tyrosine hydroxylase, and orcokinin). Contrary to previous descriptions, the visual system displays a serial layout with only one first-order visual neuropil connected to a bilayered arcuate body by catecholaminergic interneurons. Fluorescent dye tracing reveals a previously reported second visual neuropil as the target of axons from the lateral sense organ instead of the eyes.
Conclusions
Ground pattern reconstruction reveals remarkable neuroanatomical stasis in the pycnogonid visual system since the Ordovician or even earlier. Its conserved layout exhibits similarities to the median eye pathway in euchelicerates, especially in xiphosurans, with which pycnogonids share two median eye pairs that differentiate consecutively during development and target one visual neuropil upstream of the arcuate body. Given multiple losses of median and/or lateral eyes in chelicerates, and the tightly linked reduction of visual processing centers, interconnections between median and lateral visual neuropils in xiphosurans and arachnopulmonates are critically discussed, representing a plausible ancestral condition of taxa that have retained both eye types.
Background
Asymmetries are a widespread phenomenon in otherwise bilaterally symmetric organisms, and investigation of asymmetric structures can help us gather insights into fundamental evolutionary processes such as the selection for morphological novelties caused by behavioural changes. In insects, asymmetric genitalia have evolved in almost every order, and usually it’s the sclerotized parts and most conspicuous male phallic organs that are known to exhibit asymmetries. While external copulatory organs in insects have often been subject to investigations concerning asymmetries and the evolution thereof, internal reproductive structures have received far less attention. Here we describe the internal and external male genitalia in three species of Austrophasmatidae, Mantophasmatodea, using μ-CT imaging and light microscopy. Mantophasmatodea is the most recently discovered insect order, and with 21 species described to date, it is among the smallest insect orders currently known.
Results
We confirm that male heelwalkers exhibit asymmetries in the external genitalia and associated structures, represented by asymmetric phallic lobes and cerci. Moreover, we found an extreme asymmetry within the internal male genitalia: in all adult males investigated (N = 5), the seminal vesicle, a dilatation of the vas deferens, was only developed on the right side of the male while missing on the left side.
Conclusion
The false-male-above mating position exhibited by Mantophasmatodea and especially the long copulation duration of ca. 3 days might select for this unusual absence asymmetry of the left seminal vesicle. If this holds true for all heelwalker species, this absence asymmetry constitutes another autapomorphy for Austrophasmatidae or even the insect order Mantophasmatodea.
The aquatic gastropod Theodoxus fluviatilis occurs in Europe and adjacent areas of Asia. The snail species has formed two genetically closely related subgroups, the freshwater ecotype (FW) and the brackish water ecotype (BW). Other than individuals of the FW ecotype, those of the BW ecotype survive in salinities of up to 28‰. Coastal aquatic ecosystems may be affected by climate change due to salinization. Thus, we investigated how the two Theodoxus ecotypes adjust to changes in environmental salinity, focusing on the question whether Na+/K+-ATPase or V-ATPase are regulated on the transcriptional, the translational or at the activity level under changing external salinities. Animals were gradually adjusted to extreme salinities in containers under long-day conditions and constant temperature. Whole body RNA- or protein extracts were prepared. Semi-quantitative PCR- and western blot-analyses did not reveal major changes in transcript or protein abundances for the two transporters under low or high salinity conditions. No significant changes in ATPase activities in whole body extracts of animals adjusted to high or low salinity conditions were detected. We conclude that constitutive expression of ATPases is sufficient to support osmotic and ion regulation in this species under changing salinities given the high level of tolerance with respect to changes in body fluid volume.
Shallow aquatic environments are characterized by strong environmental variability. For ectotherms, temperature is the main driver of metabolic activity, thus also shaping performance. Ingestion rates in mysids are fast responses, influenced by metabolic and behavioral activity. We examined ingestion rates of the mysid Neomysis integer, collected in the Baltic Sea, after one-week exposure to different constant and fluctuating temperature regimes (5, 10, 15, 20°C and 9 ± 5, 14 ± 5°C, respectively). To investigate possible differences between sexes, thermal performance curves (TPCs) were established for female and male mysids based on ingestion rates measured at constant temperatures. TPCs of ingestion rates at constant temperatures differed between sexes, with female mysids showing a higher total ingestion rate as well as a higher thermal optimum compared to male mysids. Females showed reduced ingestion rates when exposed to fluctuating temperatures around their thermal optimum, whereas ingestion of male mysids was not reduced when exposed to fluctuating temperatures. The observed sex-specific differences might be related to potentially higher lipid and energy demands of the females. We suggest future studies should investigate males and females to improve our understanding about impacts of environmental variability on natural populations.
Foraging behavior, neuroanatomy and neuroplasticity in cursorial and stationary hunting spiders
(2023)
The central nervous system (CNS) is the integration center for the coordination and regulation of
all body activities of animals and the source of behavioral patterns, behavioral plasticity and
personality. Understanding the anatomy and the potential for plastic changes of the CNS not only
widens the knowledge on the biology of the respective species, but also enables a more
fundamental understanding of behavioral and ecological patterns. The CNS of species with
different sensory ecologies for example, will show specific differences in the wiring of their CNS,
related to their lifestyle. Spiders are a group of mesopredators that include stationary hunting
species that build webs for prey capture, and cursorial hunting species that do not build capture
webs. These distinct lifestyles are associated with major differences in their sensory equipment,
such as size of the different eyes.
In this thesis, I aimed to answer if a cursorial mesopredator would change its behavior due to
different levels of perceived predation risk, and if this behavior would be influenced by individual
differences (chapter 1); how the visual pathways in the brain of the cursorial hunting jumping
spider Marpissa muscosa differs from that of the nocturnal cursorial hunting wandering spider
Cupiennius salei (chapter 2); to what degree the visual systems of stationary and cursorial hunting
spiders differ and whether CNS areas that process vibratory information show similar differences
(chapter 3); and finally if the CNS in stationary and cursorial hunting spiders shows different
patterns of neuroplasticity in response to sensory input and deprivation during development
(chapter 4).
In chapter 1, I found that jumping spiders adjust their foraging behavior to the perceived level of
risk. By favoring a dark over a light substrate, they displayed a background-matching strategy.
Short pulses of acute risk, produced by simulated bird overflights, had only small effects on the
behavior. Instead, a large degree of variation in behavior was due to among-individual differences
in foraging intensity. These covaried with consistent among-individual differences in activity,
forming a behavioral syndrome. Our findings highlight the importance of consistent amongindividual
differences in the behavior of animals that forage under risk. Future studies should
address the mechanisms underlying these stable differences, as well as potential fitness
consequences that may influence food-web dynamics.
In chapter 2, I found that the visual pathways in the brain of the jumping spider M. muscosa differ
from that in the wandering spider C. salei. While the pathway of the principal eyes, which are
responsible for object discrimination, is the same in both species, considerable differences occur
in the pathway of the secondary eyes, which detect movement. Notably, M. muscosa possesses
an additional second-order visual neuropil, which is integrating information from two different
secondary eyes, and may enable faster movement decisions. I also showed that the tiny posterior
median eye is connected to a first-order visual neuropil which in turn connects to the arcuate body
(a higher-order neuropil), and is thus not vestigial as suggested before. Subsequent studies should
focus on exploring the function of the posterior median eyes in different jumping spider species,
Foraging behavior, neuroanatomy, and neuroplasticity in cursorial and stationary hunting spiders
as they show considerable inter-specific size differences that may be correlated with a differing
connectivity in the brain.
In chapter 3, I described all neuropils and major tracts in the CNS of two stationary (Argiope
bruennichi and Parasteatoda tepidariorum) and two cursorial hunting spiders (Pardosa amentata
and M. muscosa). I found major differences in the visual systems of the secondary eyes between
cursorial and stationary hunting spiders, but also within the groups. A. bruennichi has specialized
retinula cells in two of the secondary eyes, which connect to different higher-order neuropils. P.
tepidariorum has only a single visual neuropil connected to all secondary eyes, and lacks
recognizable mushroom bodies. The neuroanatomy of CNS areas that process mechanosensory
information on the other hand, is remarkably similar between cursorial and stationary hunting
species. This suggests that the same major circuits are used for the processing of mechanosensory
information in both cursorial and stationary hunting spiders. Future studies on functional aspects
of sensory processing in spiders can build on the findings of our study.
In chapter 4, I found that developmental neuroplasticity in response to sensory input differs
between a cursorial (M. muscosa) and a stationary hunting spider (P. tepidariorum). While
deprivation of sensory input leads to a volume increase in several visual and mechanosensory
neuropils M. muscosa, neither sensory deprivation nor sensory enrichment had an effect on the
volume of neuropils in P. tepidariorum. However, exposure to mechanical cues during
development had an effect on the allometric scaling slope of the leg neuropils in both M. muscosa
and P. tepidariorum. Future studies should focus on the genetic and cellular basis of
developmental neuroplasticity in response to sensory input in order to explain the observed
patterns.
Increasing environmental changes primarily due to anthropogenic impacts, are affecting organisms all over the planet. In general, scientists distinguish between three different ways in which organisms can respond to environmental changes in their habitat: extinction, dispersal and adaptation. An example of organisms which are highly adaptable and can easily cope with new and changing environments are invasive species which are able to colonize new habitats with only few individuals. To successfully survive in their new environment, invasive species adapt fast to novel abiotic and biotic parameters, such as different temperature regimes. Phenotypic plasticity which enables organisms to quickly modify their phenotype to new environmental conditions, explains the success in adaptation of invasive species.
While underlying mechanisms of phenotypic plasticity are not fully understood, one possible “motor” of phenotypic plasticity is epigenetics. Especially DNA methylation could explain the fast changes of the organism’s phenotype due to plasticity when experiencing changing environments, as invasive species do. DNA methylation could even contribute to the adaptation of invasive species via phenotypic plasticity, especially with clonally reproducing species. Methods such as common garden experiments with clonally reproducing species are a useful tool to differentiate between phenotypic plasticity and genetic adaptation because the confusing effects of genetic variation are lowered in clonally reproducing species.
Our overall goal was to evaluate the genetic adaptive potential of New Zealand mud snail (Potamopyrgus antipodarum) populations from Europe since they went through an extreme bottleneck after colonizing Europe only 180-360 generations ago. Seemingly, two different clonal lineages colonized Europe because two 16 s rRNA and cytochrome b haplotypes were found across different European countries, haplotypes t and z. The NZMS is a highly successful invasive species that is nowadays nearly globally distributed. The shells of the NZMS show a habitat-dependent high variability and are a fitness-relevant trait. The high variability in shell morphology is due to both genetic variation and phenotypic plasticity. To disentangle genetic from environmental effects on the shell morphology NZMS, we conducted a common garden experiment. We kept asexually reproducing females from eleven European populations in climate cabinets with three different temperatures to produce offspring. We compared shell size and shape across three generations using the geometric morphometrics approach. Furthermore, we estimated reaction norms, maternal effects, broad-sense heritability, the coefficient of genetic variation (CVA) and evolvability (IA) in shell size and shape across different temperature conditions. Additionally, we investigated the reproductive rate of the parental generation.
Results showed that the shell morphology of the parental generation differed across populations. In contrast, the shell morphology of offspring generations became more similar. The reaction norms of the F1 generation were rather variable across the three temperatures. However, we were able to observe a haplotype-dependent pattern across the reaction norms suggesting a restricted genetic differentiation among NZMS in Europe. We detected high heritability values in size indicating a high genetic influence. Heritability values for shape were lower than in size. Generally, heritability varied slightly depending on temperature. Size seemed to have a higher evolvability than shape. However, the values of all our calculations were very low which indicates that the European NZMS populations are genetically diminished. The reproductive rate of the parental generation was rather haplotype than temperature dependent. In summary, we were able to display that the NZMS is capable to plastically adapt its shell morphology to different temperatures showing significant differences between the two haplotypes. Nevertheless, the low evolvability values indicate that little genetic variation has formed since the arrival of the NZMS in Europe and therefore, European NZMS seem to have a reduced ability to react to selection.
These results implied that phenotypic plasticity is important for the adaptation to different environmental conditions in the NZMS and maybe other molluscan species. Since classical experimental approaches can only describe the resulting phenotypes, we also intended to shed more light on the mechanistic side of environmentally induced phenotypic modifications using DNA methylation analysis. Although molluscs represent one of the most diverse taxa within the metazoan and are found in many different habitats, our knowledge of the DNA methylation in molluscs is scarce. Therefore, we aimed at deepening and summarizing our understanding about DNA methylation in molluscs. Publicly available molluscan genomic and transcriptomic data of all eight mollusc classes was downloaded to search for DNA methyltransferases (DNMTs 1-3) responsible for DNA methylation. Additionally, we estimated the normalized CpG dinucleotide content (CpG o/e) indicating the presence/absence and the frequency of DNA methylation in the genome. The CpG o/e ratio refers to the level of DNA methylation in the genome. Based on the sensitivity of methylated cytosines to mutate into thymine residues, species having a high germline methylation in genomic regions over evolutionary time, also have a lower CpG content, which is called CpG depletion. In contrary, species with a limited germline methylation in genomic regions over evolutionary time, show a higher CpG content and lack CpG depletion. The presence or absence of CpG depletion can be calculated with the CpG o/e ratio. Ultimately, the goal of our analyses was to gain insight into the evolution of methylation in molluscs.
We detected DNMTs in all eight mollusc classes and in most of the species. It is therefore plausible that the last common ancestor of molluscs has already had the enzymatic machinery which is needed for DNA methylation. However, various species did not possess the complete DNMT toolkit indicating evolutionary modification in DNA methylation. In general, we found a wide distribution of the bimodal CpG o/e pattern in six mollusc classes, resulting from CpG depletion. The genes in these groups seem to be divided into genes with a high degree of methylation and genes with a lower degree of methylation. This implies that DNA methylation seems to be rather common in molluscs. Species of Solenogastres and Monoplacophora were not or only sparsely methylated. It seems that those mollusc groups have undergone a reduction in DNA methylation. We hope that our investigations will demonstrate the lacking knowledge in epigenetics of molluscs and encourage scientist to execute and continue genetic studies on molluscs.
Emerging infectious diseases are among the greatest threats to human, animal and plant health as well as to global biodiversity. They often arise following the human-mediated transport of a pathogen beyond its natural geographic range, where host species are typically not well adapted due to a lack of co-evolutionary host-pathogen dynamics. One such pathogen is the fungus Pseudogymnoascus destructans (Pd), which causes White-Nose disease in hibernating bats. While Pd was first observed in North America where it has led to mass-mortalities in some bat species, the pathogen originates from Eurasia where infection is not associated with mortality. Most of the Pd research has focused on the invasive North American range, which likely underestimated the genetic structure of the pathogen and the role it might play in the disease dynamics.
In my work, I therefore evaluated the genetic structure of Pd in its native range with the aim of uncovering cryptic diversity and further use population genetic data to address some key ecological aspects of the disease dynamics. With an extensive reference collection of more than 5,000 isolates from 27 countries I first demonstrated strong differentiation between two monophyletic clades across several genetic measures (multi-locus genotypes, full genome long-read sequencing and Illumina NovaSeq on isolate pools). These findings are consistent with the presence of two cryptic species which are both causative agents of bat White-Nose disease (‘Pd-1’, which corresponds to P. destructans sensu stricto, and ‘Pd-2’). Both species exist in the same geographic range and co-occur in the same hibernacula (i.e., in sympatry), though with specialised host preferences. I further described the fine-scale population structure in Eurasia which revealed that most genotypes are unique to single hibernacula (more than 95% of genotypes). The associated differences in microsatellite allele frequencies among hibernacula allowed the use of assignment methods to assign the North American isolates (exclusively Pd-1) to regions in Eurasia. Hence, a region in Ukraine (Podilia) is the most likely origin of the North American introduction.
To gain further insights into the spatial and temporal dynamics of White-Nose disease on a localised scale, several hibernacula were sampled with high intensity (artificial hibernaculum in Germany and natural karst caves in Bulgaria). Low rates of Pd gene flow were observed even among closely situated hibernacula. This indicates that Pd does not remain viable on bats over summer or it would be frequently exchanged among bats (and hence hibernacula) resulting in a homogenous distribution of genotypes. Instead, bats need to become re-infected each hibernation season to explain the yearly re-occurrence of White-Nose disease. Given the distribution and richness of Pd genotypes on hibrnacula walls and infected bats of the same hibernacula, bats become infected from the hibernacula walls when they return after summer. This means that environmental reservoirs exist within hibernacula (i.e., the walls) on which Pd spores persist during bat absence and which drive the yearly re-occurrence of White-Nose disease. In an experimental setup, I confirmed the long-term viability of Pd spores on abiotic substrate for at least two years and furthermore discovered temporal variations in Pd spores’ ability to germinate. In fact, these variations followed a seasonal pattern consistent with the timing of bats absence (reduced germination) and presence (increased germination) and could indicate adaptations of Pd to the bats’ life-cycle. The infection of bats from environmental reservoirs hence seems to be a central aspect of White-Nose disease dynamics and Pd biology.
Pds ability to remain viable for extended periods outside the host increases its risk of being anthropogenically transported and might have played a role in the emergence of White-Nose disease in North America. The existence of a second species (Pd-2) poses a great additional danger to North American bats considering that its introduction there could lead to deaths and associated population declines in so-far unaffected species given what is known about differing host species preferences in Eurasian bats. Even within the native range of Pd, the movement of Pd between differentiated fungal populations could facilitate genetic exchanges (e.g., through sexual reproduction) between genetically distant genotypes. Such genetic exchanges could lead to phenotypic jumps in pathogenicity or host-species preferences and should hence be prevented.
The native range of a pathogen holds great potential to better understand the genetic and ecological basis of a (wildlife) disease. My work informs about the dangers associated with the accidental transport of Pd (and other pathogens) and highlights the need for ‘prezootic’ biosecurity-oriented strategies to prevent disease outbreaks globally. Once a pathogen has arrived in a new geographic range, and particularly if it has environmentally durable spores (as demonstrated for Pd), it will be difficult/impossible to eradicate. Furthermore, a pathogen’s ability to remain viable outside the host and infect them from environmental reservoirs has been associated with an increased risk of species extinctions and needs to be considered when designing management strategies to mitigate disease impact.
Amid the current global biodiversity crisis, being able to accurately monitor the changing state of biodiversity is essential for successful conservation actions and policy. Despite the pressing need for reliable and cost-effective monitoring methods, collecting such data remains extremely difficult for elusive species, such as temperate zone bats. Although bats are important indicators of environmental changes, monitoring bat populations is challenging because they are nocturnal, volant, small, and highly sensitive to human activities and disturbance. Thus far, population trends of temperate zone bats have been mainly based on visual surveys, including winter hibernation counts at underground sites. However, as bats may not always be roosting in visible locations within the hibernacula, it is currently unknown how these estimates relate to actual population sizes.
Infrared light barriers combined with camera traps are a novel method to monitor bats at underground sites. When installed at the entrance of hibernacula, infrared light barriers have the potential to estimate site-level population sizes more accurately than visual surveys, by counting all bats flying in and out of the site. Moreover, camera traps, consisting of a digital camera and white flash, can be used for species-level identification. However, for this new method to be applicable as a large-scale bat monitoring technique, it is important to characterize it with regard to three main criteria: is the method minimally invasive, is it accurate, and is it scalable in terms of spatial and temporal resolution? Therefore, the purpose of this thesis was to investigate the invasiveness and accuracy of this novel bat monitoring method, and to develop standardized and automated data analysis pipelines, both for the light barrier and camera trap data, to support the deployment of this method at scale.
In Publication I, we used light barrier data, infrared video recordings and acoustic data from an experimental field study to investigate whether the white flash of the camera trap has any measurable short- or long-term effect on bat activity and behavior. The flash of the camera trap was turned on and off every week at each site, which allowed us to compare the activity and behavior of bats between flash-on and flash-off nights. We found that despite the high sensitivity of bats to disturbance, they did not change their nightly activity patterns, flight direction, echolocation behavior, or long-term site use in response to the white flash of the camera trap. Based on these results, we concluded that camera traps using a white flash are a minimally invasive method for monitoring bat populations at hibernacula, providing high quality images that allows species-level identification.
In Publication II, we used infrared video surveillance to quantify the accuracy of infrared light barriers, and we described a standardized methodology to estimate population sizes and trends of hibernating bat assemblages using light barrier data. We showed that light barrier accuracy varies based on the model and location of the installation relative to the entrance, with the best combination achieving nearly perfect accuracy over the spring emergence phase. When compared to light barrier-based estimates, we found that visual counts markedly underestimated population sizes, recovering less than 10% of the bats at the most complex hibernacula. Moreover, light barrier-based population trends showed regional patterns of growth and decline that were not detectable using the visual count data. Overall, we established that the light barrier data can be used to estimate the population size and trends of hibernating bat assemblages with unprecedented accuracy and in a standardized way.
In Publication III, we described a deep learning-based tool, BatNet, that can accurately and efficiently identify bat species from camera trap images. The baseline model was trained to identify 13 European bat species or species complexes using camera trap images collected at 32 hibernation sites (i.e., trained sites). We showed that the baseline model performance was very high across all 13 bat species on trained sites, as well as on untrained sites when the camera angle and distance from the entrance were comparable to the training images. At untrained sites with more atypical camera placements, we demonstrated the ability to retrain the baseline model and achieve an accuracy comparable to the trained sites. Additionally, we showed that the model can learn to identify a new species, while maintaining high classification accuracy for all original species. Finally, we established that BatNet can be used to accurately describe ecological metrics from camera trap images (i.e., species diversity, relative abundance, and species-specific phenology) that are relevant for bat conservation.
We conclude that infrared light barriers and camera traps offer a minimally invasive and accurate method to monitor site-level bat population trends and species-specific phenological estimates at underground sites. Such remote data collection approaches are particularly relevant for monitoring large, complex hibernation sites, where traditional visual surveys are not feasible or account only for a small fraction of the actual population. Combining this automated monitoring method with a deep learning-based species identification tool, BatNet, allows us quickly and accurately analyze millions of camera trap images resulting from large-scale, long-term camera trap studies. As a result, we can gain unprecedented insights into the behavior and population dynamics of these enigmatic species, drastically improving our ability to support data-driven bat conservation.
The need for the diversification of utilised species has emerged in the present aquaculture
production environment. Shifts in consumer interest, climate change-induced temperature
increases, and major fish disease outbreaks have put a strain on this industry. In this context,
the pikeperch (Sander lucioperca) has become a new target species for aquaculture in Central
Europe. This new aquaculture focus species exhibits high numbers of offspring, fast growth,
and high consumer acceptance. It can also effectively deal with higher temperatures and turbid
water. However, the rate of successful rearing is still low, as various developmental
transformations and environmental effects commonly lead to high mortality rates during the
early ontogenetic stages. The aim of this doctoral project was thus to obtain insight into
embryonic to larval developmental changes during pikeperch ontogeny. Specifically, the times
of change that influence survival were of focus. Based on the available literature, particular
attention was paid to general growth patterns and the connected developmental changes, the
determination of myogenesis gene marker expression changes, and the support of animal
welfare efforts for pikeperch rearing procedures. To achieve the aims of the study, a methodical
setup consisting of morphometric and developmental observations was combined with
transcriptome gene marker analysis for the different ontogenetic stages.
Three developmental phases were differentiated during the embryo-larval transition. Each of
these possessed distinct growth patterns with different growth rates. The intermediate
threshold phase showed internal organ development that focused on digestive, neuronal, and
heart tissues. Three activity phases of myogenesis were determined: during early embryonic
development, before hatching, and after hatching during the larval stages. Therefore, muscle
development seemed to be regulated to balance energy expenditures. Additionally, two
coinciding skeletogenic phases were found. Furthermore, a cell line from whole embryos was
developed to support the replacement of animals in future experimental setups. A software
system for video analyses was developed to support rearing procedures in aquaculture
facilities. This prototype can be used to automate the counting of specimens and thus allows
for faster responses to increasing mortalities. Based on the results of this thesis project, further
insights into the early development of pikeperches were obtained. This will facilitate the design
and adaptation of raising and husbandry protocols, which can help to further establish
pikeperch as an aquaculture species and support its application in modern recirculatory
systems.