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Abstract
Non‐native invasive species are threatening ecosystems and biodiversity worldwide. High genetic variation is thought to be a critical factor for invasion success. Accordingly, the global invasion of a few clonal lineages of the gastropod Potamopyrgus antipodarum is thus both puzzling and has the potential to help illuminate why some invasions succeed while others fail. Here, we used SNP markers and a geographically broad sampling scheme (N = 1617) including native New Zealand populations and invasive North American and European populations to provide the first widescale population genetic assessment of the relationships between and among native and invasive P. antipodarum. We used a combination of traditional and Bayesian molecular analyses to demonstrate that New Zealand populations harbour very high diversity relative to the invasive populations and are the source of the two main European genetic lineages. One of these two European lineages was in turn the source of at least one of the two main North American genetic clusters of invasive P. antipodarum, located in Lake Ontario. The other widespread North American group had a more complex origin that included the other European lineage and two New Zealand clusters. Altogether, our analyses suggest that just a small handful of clonal lineages of P. antipodarum were responsible for invasion across continents. Our findings provide critical information for prevention of additional invasions and control of existing invasive populations and are of broader relevance towards understanding the establishment and evolution of asexual populations and the forces driving biological invasion.
Abstract
Two decades after the discovery of adult‐born neurons in the brains of decapod crustaceans, the deutocerebral proliferative system (DPS) producing these neural lineages has become a model of adult neurogenesis in invertebrates. Studies on crayfish have provided substantial insights into the anatomy, cellular dynamics, and regulation of the DPS. Contrary to traditional thinking, recent evidence suggests that the neurogenic niche in the crayfish DPS lacks self‐renewing stem cells, its cell pool being instead sustained via integration of hemocytes generated by the innate immune system. Here, we investigated the origin, division and migration patterns of the adult‐born neural progenitor (NP) lineages in detail. We show that the niche cell pool is not only replenished by hemocyte integration but also by limited numbers of symmetric cell divisions with some characteristics reminiscent of interkinetic nuclear migration. Once specified in the niche, first generation NPs act as transit‐amplifying intermediate NPs that eventually exit and produce multicellular clones as they move along migratory streams toward target brain areas. Different clones may migrate simultaneously in the streams but occupy separate tracks and show spatio‐temporally flexible division patterns. Based on this, we propose an extended DPS model that emphasizes structural similarities to pseudostratified neuroepithelia in other arthropods and vertebrates. This model includes hemocyte integration and intrinsic cell proliferation to synergistically counteract niche cell pool depletion during the animal's lifespan. Further, we discuss parallels to recent findings on mammalian adult neurogenesis, as both systems seem to exhibit a similar decoupling of proliferative replenishment divisions and consuming neurogenic divisions.
In agricultural grasslands, management practice highly determines reproductive success for ground-nesting bird species. The most effective conservation measure is the delay of first mowing dates until broods fledge or bird friendly mowing. Late mowing often implies economical losses for farmers and may increase land use abandonment, which will, in turn, cause habitat deterioration. Thus, grassland bird conservation involves the challenge to protect broods against land use and to promote an appropriate management to sustain habitat quality at the same time. Because of their late and extended breeding season Corncrakes Crex crex are in particular vulnerable to frequent mowing which increases nest destruction, chick mortality and habitat loss.
This thesis aims to gain knowledge on favourable habitat characteristics and brood protection in relation with grassland management to derive implications for the conservation of Corncrake breeding sites in floodplain meadows. Study area is the Lower Oder Valley National Park in northeastern Germany that holds a Corncrake population of 50 to 250 calling males. The study covered two study periods, before (1998-2000) and after (2012-2015) the implementation of new Corncrake conservation measures allowing inferences on the effects of different timing and intensity of mowing for brood protection and habitat conservation.
Breeding was only confirmed on meadows with high forb cover, low sedge cover, low litter heights and a close location to ditches. Radio-tracked females preferred areas with high cover of forbs (> 30%) and a distinct relief heterogeneity, which was associated with increased vegetation diversity. Vegetation characteristics on sites with day calling activity of males showed more similarity with breeding sites than with sites only used for nocturnal calling, supporting the assumption that diurnal calling indicates the occurrence of females. Favoured vegetation structure was best provided by mowing in the preceding year. Low-intensity grazing was less effective in reducing litter and sedge cover, especially when conducted late in the season. In the absence of management, meadows rapidly overgrow and dense litter accumulates from dead plant material in eutrophic floodplains, which increases walking resistance for Corncrakes and may impede prey accessibility. Plant species richness and forb cover declined after land use cessation. Male Corncrakes abandoned calling sites on meadows unmanaged for longer periods.
Besides the availability of suitable nesting sites, food supply and nest predation risk are also related to vegetation structure and may indirectly influence the habitat quality. Faecal samples of Corncrakes consisted mainly of beetles and their larvae, followed by snails, spiders and earthworms. Invertebrate biomass, sampled with pitfall-traps, was twice as high, the numbers of large ground beetles even five times higher on previously unmanaged than on managed meadows. Invertebrate abundance was highest in the first and second years after land use abandonment, but strongly decreased afterwards to a similar level like under annual management. Therefore, unmown refuge strips for Corncrake protection and alternating mowing also enhance invertebrate prey resources in floodplain meadows.
Mammals caused the majority of all observed artificial ground nest predations. Nest predation risk was higher on previously unmanaged than on managed sites. Unmanaged meadows probably attract mammalian predators, because they provide a more favourable vegetation structure for foraging and harbour high numbers of small rodents, increasing also the risk of incidental nest predations. These findings suggest that an annual removal of vegetation, if conducted late in the season to protect grassland birds may reduce predation risk of ground nests in the subsequent year.
Whereas during 1998-2000 half of the study area was managed by the end of July, land use was delayed on meadows occupied by Corncrakes until at least 15 July or 15 August during 2012-2015. On meadows mown between 15 July and 15 August refuge strips were applied. The majority of Corncrake broods were started in the second half of May and mowing postponement until 15 August allows 80% of chicks to fledge without disturbance in the study area. In 65% of broods chicks reach independence (> 14 days old) until 15 July and can be protected by Corncrake friendly mowing because then they are large enough to successfully escape during mowing. Both adults and chicks survived in 10 m wide refuge strips. Because most birds tried to leave the unmown block for the first time when it was up to 30 m wide and only 15 to 30 m wide strips served as temporary habitat for unfledged chicks from mowing to departure, 10 m should be considered as the absolute minimum width for refuge strips.
The strong reduction of land use especially during July should have allowed more chicks to survive until fledging in 2012-2015 than 1998-2000. Besides the protection of nests and higher chick survival, the decline of mowing intensity increased the extent of habitat available for second breeding attempts. In 2012-2015, broods were initiated until late July in the study area. Male Corncrakes showed continuous arrival and departure during the breeding season. Similar departure rates were estimated by a multi-state occupancy model and for radio-tracked males in the same study area and periods, which both left their home ranges spontaneous and due to the impact of mowing. Compared to 1998-2000, total departure of males during June and July was reduced by 50% in 2012-2015, when more calling sites were protected from mowing. Although male Corncrakes show high intra-seasonal dispersal due to their sequential polygamous breeding system, postponed land use should have increased mating opportunities and re-nesting at first breeding sites.
Therefore, future directions of Corncrake conservation in eutrophic floodplains should address the increase of annual late mowing to protect broods and maintain favourable habitat conditions by creating a more flexible mowing regime adjusted to actual occurrence of Corncrakes. This requires expert advice to farmers based on an intense monitoring of calling Corncrakes. Repeated nocturnal surveys during May and June are highly recommended because low detection probability in combination with constant departure substantially underestimated the number of males present. Additionally, diurnal calling activity could improve the identification of breeding sites and timing could be used to estimate chick age in July to select sites for Corncrake friendly mowing. Because currently late mowing dates are unattractive for farmers conservation actions should along with financial compensations for mowing after 15 August promote the utilization of late-cut grass with poor nutrient quality for combustion. Energy production could provide an alternative income for farmers operating in conservation areas with delayed land use dates and will increase their acceptance of Corncrake protection measures.
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.
Bats spend half of their life at roosting sites. Hence, exploring for potential roosts is an essential task for their survival, especially for those species which switch roosts regularly, such as several temperate bat species. However, localizing new roosts is a difficult task due to bats’ sensory limitations (e.g., vision, echolocation range). To compensate such constrains, it has been hypothesized that bats rely on cognitive processes like associative learning, spatial memory, social information use and memory retention for an efficient roost localization. However, no previous study has assessed these cognitive skills under natural conditions.
The aim of my thesis was to assess how individually RFID-marked, free-ranging bats use different cognitive processes when localizing suitable day roosts. For this purpose, I used a pairwise roost-quality (suitable vs. unsuitable) choice experiment with automatic monitoring and assessed bats’ cognitive processes according to different cues available. Cues were echo-reflective (spectral signature of boxes), spatial (position of the box within the experimental pair) and social (presence of conspecific at roosts), each one linked to a different cognitive process.
I found that Bechstein’s bats (Myotis bechsteinii) used associative learning to discriminate between suitable and unsuitable newly placed boxes according to their echo-reflective cues. However, when individuals returned to known suitable roosts, they relied more on spatial memory to localize them. This was evidenced by the higher proportion of visits to the unsuitable boxes after swapping box positions within the same experimental pairs. When social cues were available, bats discovered a higher number of suitable roosts and re-localized previously occupied roosts more accurately. Taken together, Bechstein’s bats used multiple cognitive processes and prioritized one process over another depending on the relevance of the cues and search context.
Memory retention of the learned association was analyzed one year later, after the bats had returned to their breeding sites from their hibernacula. I found no evidence that individuals remembered the association between roosts’ suitability and their respective echo-reflective cue. The lack of memory retention could be attributed to hibernation or the duration of the period that the bats spent away from their summer habitat without the opportunity to reinforce the association contingencies. Nevertheless, bats quickly relearned the same association in a short period of time. This emphasizes the high behavioral flexibility of the bats.
Given the ability of Bechstein’s bats to quickly learn to discriminate roosts based on their external echo-reflective cue via associative learning, I investigated whether the use of echo-reflective cues improves box detectability and further occupancy. This was also assessed in free-ranging Natterer’s (Myotis nattereri) bats and the brown long-eared bats (Plecotus auritus). I found that the use of echo-reflective cues did not improve the detectability and occupancy of newly placed boxes despite the previous experience of the colonies with such cues. There were differences among species in the number of discovered boxes, visits and roosting days. These differences could be related to the species-specific explorative behavior and roost-switching behavior. Box supplementations programs aimed to conserve or relocate bat colonies should consider these behaviors to increase their likelihood of success even when bat colonies are used to roosting in artificial shelters.
My research underlined the importance of evaluating multiple cues under natural conditions to understand how natural selection has shaped the cognitive process used for localizing resources. Cognitive field studies are logistically challenging given the number of factors to control. However, automatic monitoring techniques like the one used in this study give the possibility to deepen the understanding of the cognitive ecology of animals. I finally discuss two venues of further research to understand the spread of information within colony members about novel roosts and the recruitment dynamic to novel roosts.
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.
Abstract
Understanding how organisms adapt to complex environments is a central goal of evolutionary biology and ecology. This issue is of special interest in the current era of rapidly changing climatic conditions. Here, we investigate clinal variation and plastic responses in life history, morphology and physiology in the butterfly Pieris napi along a pan‐European gradient by exposing butterflies raised in captivity to different temperatures. We found clinal variation in body size, growth rates and concomitant development time, wing aspect ratio, wing melanization and heat tolerance. Individuals from warmer environments were more heat‐tolerant and had less melanised wings and a shorter development, but still they were larger than individuals from cooler environments. These findings suggest selection for rapid growth in the warmth and for wing melanization in the cold, and thus fine‐tuned genetic adaptation to local climates. Irrespective of the origin of butterflies, the effects of higher developmental temperature were largely as expected, speeding up development; reducing body size, potential metabolic activity and wing melanization; while increasing heat tolerance. At least in part, these patterns likely reflect adaptive phenotypic plasticity. In summary, our study revealed pronounced plastic and genetic responses, which may indicate high adaptive capacities in our study organism. Whether this may help such species, though, to deal with current climate change needs further investigation, as clinal patterns have typically evolved over long periods.
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.
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.
Global climate change is omnipresent all over the world and is affecting and challenging organisms in various ways. Species either have to adapt to the changing environmental conditions or move to new habitats in order to avoid extinction.
Possible ways for an organism to react can be dispersal, phenotypic plasticity, genetic adaptation or a combination of these factors. Among the various consequences of climate change, especially changes in temperature affect plenty of species. In ectotherms, the body temperature and associated mechanisms are strongly dependent on environmental conditions.
The aim of this work was to investigate the mechanisms underlying adaptation to thermal variation and heat stress in the widespread butterfly species <i>Pieris napi<i>.
Focusing on indicators of individual condition, including morphology, physiology and life history traits, the purpose was to specify whether the species’ responses to temperature variation have a plastic or genetic basis. In the first experiment, phenotypic variation along a latitudinal and altitudinal cline was investigated. Yellow reflectance of wings was negatively correlated with wing melanisation, providing evidence for a trade-off between a sexually selected trait (yellow color) and thermoregulation (black color). Body size decreased with increasing latitude and led to the assumption that warmer conditions are more beneficial for <i>P. napi<i> than cooler ones. An increased flight performance at higher altitudes but not latitudes may
indicate stronger challenges for flight activity in high-altitude environments.
The second experiment focused on clinal variation and plasticity in morphology, physiology and life history in F1-generation individuals reared in captivity at different temperatures. It could be shown that individuals from cooler environments were less heat-tolerant, had a longer development but were nevertheless smaller, and had more melanised wings. These differences were genetically-based. Furthermore, it could be shown that a higher developmental temperature speeded up development, reduced body size, potential metabolic activity, and wing melanisation but increased heat tolerance, documenting plastic responses.
In a third experiment, we examined physiological responses to heat stress. A transcriptome analysis revealed an upregulation in molecular chaperones under hot conditions, whereas antioxidant responses and oxidative damage remained unaffected. The antioxidant glutathione (GSH) though was reduced under both cold and hot conditions. Interestingly, Swedish individuals were characterized by higher levels of GSH, lower early fecundity, and lower larval growth rates compared with German or Italian populations, suggesting a ‘pace-of-life’ syndrome. Thus, the individuals from warmer regions show the opposite pattern with a lower investment into maintenance but a faster lifestyle.
In summary, we found clinal variation in body size, growth rates and concomitant development time, wing aspect ratio, wing melanisation and heat tolerance. The effects of high developmental temperature very likely reflect adaptive phenotypic plasticity. When speeding up development; heat tolerance is increasing while body size, potential metabolic activity and wing melanisation are decreasing. Overall, body size of <i>P. napi<i> individuals decreased from south to north while the melanisation of the wings increased. Furthermore, we found a connection between increased wing melanisation and decreased yellow reflectance, most likely caused by a trade-off between the two. We could confirm that <i>P. napi<i> individuals from warmer environments were more heat-tolerant and larger than individuals from colder environments. Due to increasing temperatures and heat waves becoming more frequent in the future, being able to cope with such conditions will be advantageous. As warmer conditions had positive effects on individual development, <i>P. napi<i> may benefit from global warming, but its association with moist habitats suggests negative consequences of climate change. We could also reveal pronounced plastic and genetic responses in <i>P. napi<i>, which may indicate high adaptive capacities. Thus, increasing temperature may not be too problematic for the species, as it seems to be rather well equipped to deal with such challenges. However, as climate change entails changes in precipitation / humidity along with temperature changes, such issues need further investigation.