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Urbanization is a major contributor to the loss of biodiversity. Its rapid progress is mostly at the expense of natural ecosystems and the species inhabiting them. While some species can adjust quickly and thrive in cities, many others cannot. To support biodiversity conservation and guide management decisions in urban areas, it is important to find robust methods to estimate the urban affinity of species (i.e. their tendency to live in urban areas) and understand how it is associated with their traits. Since previous studies mainly relied on discrete classifications of species' urban affinity, often involving inconsistent assessments or variable parameters, their results were difficult to compare. To address this issue, we developed and evaluated a set of continuous indices that quantify species' urban affinity based on publicly available occurrence data. We investigated the extent to which a species' position along the urban affinity gradient depends on the chosen index and how this choice affects inferences about the relationship between urban affinity and a set of morphological, sensory and functional traits. While these indices are applicable to a wide range of taxonomic groups, we examined their performance using a global set of 356 bat species. As bats vary in sensitivity to anthropogenic disturbances, they provide an interesting case study. We found that different types of indices resulted in different rankings of species on the urban affinity spectrum, but this had little effect on the association of traits with urban affinity. Our results suggest that bat species predisposed to urban life are characterized by low echolocation call frequencies, relatively long call durations, small body size and flexibility in the selection of the roost type. We conclude that simple indices are appropriate and practical, and propose to apply them to more taxa to improve our understanding of how urbanization favours or filters species with particular traits.
Abstract
The neritid snail Theodoxus fluviatilis has formed regional subgroups in northern Europe, where it appears in both freshwater (FW) and brackish water (BW) in coastal areas of the Baltic Sea. These ecotypes show clear differences in osmotolerance and in the modes of accumulating organic osmolytes under hyperosmotic stress. We reasoned that the expression patterns of soluble proteins in the two ecotypes may differ as well. BW snails have to deal with a higher salinity (up to 20‰) than FW snails (0.5‰) and also cope with frequent fluctuations in environmental salinity that occur after heavy rains or evaporation caused by extended periods of intense sunshine. Therefore, the protein expression patterns of specimens collected at five different FW and BW sites were analyzed using 2D SDS‐PAGE, mass spectrometry, and sequence comparisons based on a transcriptome database for Theodoxus fluviatilis. We identified 89 differentially expressed proteins. The differences in the expression between FW and BW snails may be due to phenotypic plasticity, but may also be determined by local genetic adaptations. Among the differentially expressed proteins, 19 proteins seem to be of special interest as they may be involved in mediating the higher tolerance of BW animals towards environmental change compared with FW animals.
Comparative neuroanatomy of the central nervous system in web-building and cursorial hunting spiders
(2023)
Spiders (Araneae) include cursorial species that stalk their prey and more stationary species that use webs for prey capture. While many cursorial hunting spiders rely on visual cues, web-building spiders use vibratory cues (mechanosensation) for prey capture. We predicted that the differences in primary sensory input between the species are mirrored by differences in the morphology/architecture of the central nervous system (CNS). Here, we investigated the CNS anatomy of four spider species, two cursorial hunters Pardosa amentata (Lycosidae) and Marpissa muscosa (Salticidae), and two web-building hunters Argiope bruennichi (Araneidae) and Parasteatoda tepidariorum (Theridiidae). Their CNS was analyzed using Bodian silver impregnations, immunohistochemistry, and microCT analysis. We found that there are major differences between species in the secondary eye pathway of the brain that pertain to first-order, second-order, and higher order brain centers (mushroom bodies [MB]). While P. amentata and M. muscosa have prominent visual neuropils and MB, these are much reduced in the two web-building species. Argiope bruennichi lacks second-order visual neuropils but has specialized photoreceptors that project into two distinct visual neuropils, and P. tepidariorum lacks MB, suggesting that motion vision might be absent in this species. Interestingly, the differences in the ventral nerve cord are much less pronounced, but the web-building spiders have proportionally larger leg neuropils than the cursorial spiders. Our findings suggest that the importance of visual information is much reduced in web-building spiders, compared to cursorial spiders, while processing of mechanosensory information requires the same major circuits in both web-building and cursorial hunting spiders.
Human habitat disturbance affects both species diversity and intraspecific genetic diversity, leading to correlations between these two components of biodiversity (termed species–genetic diversity correlation, SGDC). However, whether SGDC predictions extend to host‐associated communities, such as the intestinal parasite and gut microbial diversity, remains largely unexplored. Additionally, the role of dominant generalist species is often neglected despite their importance in shaping the environment experienced by other members of the ecological community, and their role as source, reservoir and vector of zoonotic diseases. New analytical approaches (e.g. structural equation modelling, SEM) can be used to assess SGDC relationships and distinguish among direct and indirect effects of habitat characteristics and disturbance on the various components of biodiversity.
With six concrete and biologically sound models in mind, we collected habitat characteristics of 22 study sites from four distinct landscapes located in central Panama. Each landscape differed in the degree of human disturbance and fragmentation measured by several quantitative variables, such as canopy cover, canopy height and understorey density. In terms of biodiversity, we estimated on the one hand, (a) small mammal species diversity, and, on the other hand, (b) genome‐wide diversity, (c) intestinal parasite diversity and (d) gut microbial heterogeneity of the most dominant generalist species (Tome's spiny rat, Proechimys semispinosus). We used SEMs to assess the links between habitat characteristics and biological diversity measures.
The best supported SEM suggested that habitat characteristics directly and positively affect the richness of small mammals, the genetic diversity of P. semispinosus and its gut microbial heterogeneity. Habitat characteristics did not, however, directly impact intestinal parasite diversity. We also detected indirect, positive effects of habitat characteristics on both host‐associated assemblages via small mammal richness. For microbes, this is likely linked to cross species transmission, particularly in shared and/or anthropogenically altered habitats, whereas host diversity mitigates parasite infections. The SEM revealed an additional indirect but negative effect on intestinal parasite diversity via host genetic diversity.
Our study showcases that habitat alterations not only affect species diversity and host genetic diversity in parallel, but also species diversity of host‐associated assemblages. The impacts from human disturbance are therefore expected to ripple through entire ecosystems with far reaching effects felt even by generalist species.
Abstract
Social organisation in species with fluctuating population sizes can change with density. Therefore, information on (future) density obtained during early life stages may be associated with social behaviour. Olfactory cues may carry important social information. We investigated whether early life experience of different experimental densities was subsequently associated with differences in attraction to adult conspecific odours. We used common voles (Microtus arvalis), a rodent species undergoing extreme density fluctuations. We found that individuals originating from high experimental density populations kept in large outdoor enclosures invested more time in inspecting conspecific olfactory cues than individuals from low‐density populations. Generally, voles from both treatments spent more time with the olfactory cues than expected by chance and did not differ in their latency to approach the odour samples. Our findings indicate either that early experience affects odour sensitivity or that animals evaluate the social information contained in conspecific odours differently, depending on their early life experience of conspecific density.
Abstract
Surface waters are warming due to climate change, potentially pushing aquatic organisms closer to their thermal tolerance limits. However, cyanobacterial blooms are expected to occur more often with rising temperature, increasing the likelihood of poor‐quality food available for herbivorous zooplankton. Zooplankton can adapt locally by genetic differentiation or via adaptive phenotypic plasticity to increasing temperatures, but there is limited knowledge on how these processes may be affected by food quality limitation imposed by cyanobacteria.
To test the effects of cyanobacteria‐mediated food quality on local temperature adaptation, we measured juvenile somatic growth and reproduction of five Daphnia magna clones from different latitudinal origin grown on three food qualities at 20, 24, and 28°C. Additionally we estimated short‐term heat tolerance, measured as knockout time (time to immobility) at lethally high temperature, of two clones acclimated to the three temperatures and two food quality levels to test for the effects of food quality on adaptive plastic responses.
As expected, clones from lower latitudes showed on average better somatic growth and reproduction than clones from higher latitudes at higher temperatures. However, the difference in somatic growth diminished with increasing cyanobacteria abundance in the diet, suggesting constraints on local genetic adaptation under predicted decreases in food quality. As expected, short‐term heat tolerance of the clones generally increased with increasing acclimation temperature. However, heat tolerance of animals acclimated to the highest temperature was larger when grown at medium than at good food quality, whereas the opposite response was observed for animals acclimated to the lowest temperature. This suggests a better adaptive phenotypic response of animals to elevated temperatures under higher cyanobacteria abundance, and thus shows an opposite pattern to the results for somatic growth.
Overall, we demonstrate that food quality limitation can mediate responses of D. magna life history traits and heat tolerance to increasing temperatures, and that the effects differ depending on the time scale studied, that is, mid‐term (somatic growth) versus short‐term (tolerance to acute heat stress). These aspects will need further attention to accurately predict of how organisms will cope with future global warming by local adaptation and adaptive phenotypic plasticity.
Hibernation is a widespread adaptation in animals to seasonally changing environmental conditions. In the face of global anthropogenic change, information about plastic adjustments to environmental conditions and associated mortality costs are urgently needed to assess population persistence of hibernating species. Here, we used a five-year data set of 1047 RFID-tagged individuals from two bat species, Myotis nattereri and Myotis daubentonii that were automatically recorded each time they entered or left a hibernaculum. Because the two species differ in foraging strategy and activity pattern during winter, we expected species–specific responses in the timing of hibernation relative to environmental conditions, as well as different mortality costs of early departure from the hibernaculum in spring. Applying mixed-effects modelling, we disentangled population-level and individual-level plasticity in the timing of departure. To estimate mortality costs of early departure, we used both a capture mark recapture analysis and a novel approach that takes into account individual exposure times to mortality outside the hibernaculum. We found that the timing of departure varied between species as well as among and within individuals, and was plastically adjusted to large-scale weather conditions as measured by the NAO (North Atlantic Oscillation) index. Individuals of M. nattereri, which can exploit milder temperatures for foraging during winter, tuned departure more closely to the NAO index than individuals of M. daubentonii, which do not hunt during winter. Both analytical approaches used to estimate mortality costs showed that early departing individuals were less likely to survive until the subsequent hibernation period than individuals that departed later. Overall, our study demonstrates that individuals of long-lived hibernating bat species have the potential to plastically adjust to changing climatic conditions, although the potential for adjustment differs between species.
Primary producer communities are often growth-limited by essential nutrients such as nitrogen (N) and phosphorus (P). The magnitude of limitation and whether N, P or both elements are limiting autotroph growth depends on the supply and ratios of these essential nutrients. Previous studies identified single, serial or co-limitation as predominant limitation outcomes in autotroph communities by factorial nutrient additions. Little is known about potential consequences of such scenarios for herbivores and whether their growth is primarily affected by changes in autotroph quantity or nutritional quality. We grew a community of phytoplankton species differing in various food quality aspects in experimental microcosms at varying N and P concentrations resulting in three different N:P ratios. At carrying capacity, N, P, both nutrients or none were added to reveal which nutrients were limiting. The nutrient-supplied communities were fed to the generalist herbivorous rotifer Brachionus calyciflorus to investigate how changing phytoplankton biomass and community composition affect herbivore abundance. We found phytoplankton being growth-limited either by N alone (single limitation) or serially, i.e. primarily by N and secondarily by P, altering available food quantity for rotifers. Rotifer growth showed a different response pattern compared to phytoplankton, suggesting that apart from food quantity food quality aspects played a substantial role in the transfer from primary to secondary production. The combined addition of N and P to phytoplankton had generally a positive effect on herbivore growth, whereas adding non-limiting nutrients had a rather detrimental effect probably due to stoichiometrically imbalanced food in terms of nutrient excess. Our experiment shows that adding various nutrients to primary producer communities will not always lead to increased autotroph and herbivore growth, and that differences between autotroph and herbivore responses under co-limiting conditions can be partly well explained by concepts of ecological stoichiometry theory.
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.
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.