Sex segregation in the Bryophyta

Ohne Zusammenfassung     

Stage of pregnancy dictates heterothermy in temperate forest-dwelling bats

Bats face high energetic requirements, as powered flight is costly and they have a disadvantageous surface-to-volume-ratio. To deal with those requirements energy saving mechanisms, such as heterothermy (torpor), have evolved. Torpor during pregnancy, however, reduces rates of foetal development and consequently prolongs pregnancy. Therefore, heterothermy has a great effect on reproduction, as an unhindered parturition can only be assured by high body temperatures. Regardless of these adverse affects of torpor the energetic requirements of bats during reproduction urge for energy savings and bats are known to enter torpor during pregnancy. The species in the current study differ in their torpor patterns and thus their heterothermic strategy. However, we hypothesized, that species-specific heterothermic behaviour should be revoked at the end of pregnancy. We analyzed skin temperatures of Myotis bechsteinii, Myotis nattereri and Plecotus auritus during pregnancy and found no differences in torpor depth between species during the last phase of pregnancy. Furthermore, we could show that individuals entered torpor frequently during pregnancy and only minimized torpor during the last stage of pregnancy. This suggests that close to the end of pregnancy, heterothermy is restricted but not species-specific and the required energy is allocated otherwise.     

Thermoregulation in male temperate bats depends on habitat characteristics

Several energy-saving strategies have evolved in animals, one example being the short-term reduction of metabolism and body temperature (torpor) in endotherms. For bats, pronounced torpor behaviour has been described. The aim of this study was to assess individual variation in torpor expression of male Myotis daubentonii, and to analyse whether this variation is related to habitat characteristics. For that we measured skin temperatures of bats from different habitats using radio transmitters and also recorded ambient temperature. Skin temperature was corrected for ambient temperature and individual body mass. Cluster analysis of residuals revealed two different thermoregulatory strategies. Males in cluster 1 were more often encountered torpid and reached lower minimum skin temperatures than males in cluster 2. The differences in behaviour were related to environmental variables (water surface area near the roost, roost altitude, precipitation, ambient temperature in the warmest quarter of the year). Males from cluster 1 occupied less favourable habitats (less water surface, higher altitudes, wetter and colder climate) than males from cluster 2. Our data suggest a linkage between torpor behaviour and habitat characteristics. These characteristics could be used to identify favourable and marginal habitats for M. daubentonii.     

Sex segregation ratio and gender expression in the genus Actinidia

The sex segregation ratio was checked in bi-parental families of Actinidia deliciosa (2n=6x=174) obtained by crossing four females (A12, Mo3, Br4, Hw1) with two males (T2, M1) and one fruiting male (M3h, subandroecious) according to a factorial mating design. The M3h fruiting male was also selfed. The sex ratio was checked in maternal families of A. kolomikta (2n=2x) and A. chinensis (2n=2x) as well as in A. deliciosa. Seedlings of both diploid species took 3–4 years to progress beyond juvenility, whereas a noticeable number of seedlings from biparental crosses of A. deliciosa involving A12 and Hw1 as seed parents were still non-flowering after seven growing seasons. Open-pollinated families of both diploid and hexaploid species as well as most families from biparental crosses showed a sex segregation ratio approaching 11. Subandroecious lines with different degrees of ovary and pistil development appeared in proportions of 0–4.2%, depending on the cross, but only 6 of the 2567 male vines checked were capable of setting fruit. No case of self-fertility or apomixis was detected among 1866 bagged female vines. Selfed M3h progenies gave only female and male phenotypes in a ratio of 1 female to 3 males. No off-type vines were found among these progenies. The same disomic sex segregation ratio seems to be operating at different ploidy levels in the genus Actinidia. Since selfed fruiting males produced both female and male individuals, the male sex appears to be the heterogametic one. Such evidence indicates that a monofactorial system based on one or more linked genes or on an X/Y chromosome set must be controlling sex expression. How a monofactorial sex-determining mechanism could operate in polyploids to give a 11 female: male ratio is discussed. Minor modifying gene(s) seem to be responsible for the feminization of males, and their expression appears enhanced by environmental conditions. Masculinizing gene(s) seem to be lacking in female genotypes.     

Sexual segregation occurs in bats within fragmented remnant woodlands in an agricultural landscape

Species‐specific responses to landscape configuration and landscape composition have been studied extensively. However, little work has been done to compare intraspecific differences in habitat preferences. Bats have potential as good bioindicator taxa in woodland habitats. Therefore, studying sex differences in responses to woodland and the wider landscape can allow us to gain insight into the relative importance of these habitats for both bats and other taxa. In this study, we aimed to test the predictions that (i) habitat type and connectivity will influence the probability of recording female bats in woodlands and (ii) sex differences in response to habitat type and connectivity will be species‐specific. Bat capture data was collected in 206 woodlands over 3 years in England. The probability of detecting females relative to males was modeled in response to a range of woodland characteristics and landscape metrics for six bat species. We recorded sex differences in responses to landscape features in three species. We found a higher probability of capturing female Myotis nattereri in woodlands that were surrounded by a higher proportion of improved grasslands, whereas female Myotis mystacinus were less likely to be recorded in woodlands surrounded by semi‐natural vegetation. Female Plecotus auritus were more likely to be recorded in isolated woodlands with less connectivity to other woodlands and where agriculture dominated the surrounding landscape. Our findings indicate that sexual segregation occurs across several UK bat species in response to landscape connectivity and composition. Sexual segregation in response to landscape characteristics in bats should therefore be an important consideration in the management of fragmented agricultural landscapes.     

Comparative analyses suggest that information transfer promoted sociality in male bats in the temperate zone

The evolution of sociality is a central theme in evolutionary biology. The vast majority of bats are social, which has been explained in terms of the benefits of communal breeding. However, the causes for segregated male groups remain unknown. In a comparative study, we tested whether diet and morphological adaptations to specific foraging styles, two factors known to influence the occurrence of information transfer, can predict male sociality. Our results suggest that the species most likely to benefit from information transfer--namely, those preying on ephemeral insects and with morphological adaptations to feeding in open habitat--are more likely to form male groups. Our findings also indicate that solitary life was the ancestral state of males and sociality evolved in several lineages. Beyond their significance for explaining the existence of male groups in bats, our findings highlight the importance of information transfer in the evolution of animal sociality.     

Spatiotemporal pattern of local sexual segregation in a tree-dwelling temperate bat Myotis daubentonii

Sexual segregation is a common phenomenon in temperate bats, but little is known about driving forces or spatiotemporal patterns. Sexual segregation of the tree-dwelling Daubenton’s bat (Myotis daubentonii) was analyzed. Day roosts and foraging areas of radio-tracked animals were recorded during late spring, early summer, and late summer. Home ranges were calculated for each sex based on identified locations. Distance analysis between sex-specific roosts and foraging areas was conducted for each period. Mixed colonies were confirmed by trapping at roosts. Home range of males was larger (47.3 km²) than of females (9.7 km²). During late spring, distances between male and female roosts were larger (median = 715 m) than during early (median = 474 m) and late summer (median = 489 m). Distances between sex-specific foraging areas were larger during early summer (median = 2,134 m) than during both late spring (median = 1,116 m) and late summer (median = 628 m). The proportion of males in mixed groups increased from late spring (0.2 ± 0.1) to late summer (0.5 ± 0.2). These results show that sexual segregation is not static, but depends on energetic demand of individuals and mating willingness. A high energetic demand in females and low mating willingness in both sexes leads to distinct sexual segregation during late spring. When mating willingness increases, despite an increasing energy demand in males, sexes aggregate to mate.     

Growth of horseshoe bats (Chiroptera: Rhinolophidae) in temperate continental conditions and the influence of climate

Growth characteristics of three species of horseshoe bats (Rhinolophus ferrumequinum, R. euryale and R. mehelyi) were studied in northern Bulgaria, and measurements of cohorts born there in different years were compared interannually. Bulgarian horseshoe bats are usually born in the first 3 weeks of June and start to leave the roost at an age of about 3 weeks. Young horseshoe bats of all three species had attained more than 95% of the adult dimensions at the time when they started to regularly leave the cave to forage on their own in mid of July. Individually marked juvenile R. ferrumequinum reached adult dimensions in most external wing measurements in the first half of August. Accordingly the pooled measurements of all juveniles did not differ anymore from those of adult bats in the second half of August. The same pattern was found in R. mehelyi and R. euryale.We found a clear relationship between the climatic conditions prevailing in each year and the final size of individuals born respectively in those years. Whereas previous studies have addressed climatic effects only on several bat species along their northern limits of distribution, these data provide the first evidence for an influence of climate on the growth of individuals in the centre of the species’ distributions.     

Separating the effects of water quality and urbanization on temperate insectivorous bats at the landscape scale

Many local scale studies have shown that bats respond to water quality degradation or urbanization in a species‐specific manner. However, few have separated the effects of urbanization versus water quality degradation on bats, in single city or single watershed case studies. Across North Carolina, USA, we used the standardized North American Bat Monitoring Program mobile transect protocol to survey bat activity in 2015 and 2016 at 41 sites. We collected statewide water quality and urban land cover data to disentangle the effects of urbanization and water quality degradation on bats at the landscape scale. We found that statewide, water quality degradation and urbanization were not correlated. We found that bats responded to water quality degradation and urbanization independently at the landscape scale. Eptesicus fuscus and Lasiurus cinereus negatively responded to water quality degradation. Lasiurus borealis and Perimyotis subflavus positively responded to water quality degradation. Lasionycteris noctivagans did not respond to water quality degradation but was more active in more urbanized areas. Tadarida brasiliensis positively responded to urbanization and was less active in areas with degraded water quality. We show that bat–water quality relationships found at the local scale are evident at a landscape scale. We confirm that bats are useful bioindicators for both urbanization and water quality degradation. We suggest that water quality can be used to predict the presence of bat species of conservation concern, such as P. subflavus, in areas where it has not been studied locally.     

Sex and the selfish herd: sexual segregation within nonmating whirligig groups

The fitness costs and benefits at different positions in fishshoals, bird flocks, and insect swarms can be asymmetric; agroup's edge may provide more feeding opportunities, but alsogreater predator risk. Animals make trade-offs between theseselection pressures based on individual differences in traitsincluding satiation level, ability to avoid predators, and sex.Previous studies did not evaluate the impact of sex on grouppositioning in these types of nonhierarchical, nonmating groupscalled congregations. A controlled laboratory experiment wasconducted, using marked whirligig beetles (Coleoptera: Gyrinidae),to test for sexual segregation and why different sexes mightchoose different positions. Soon after a disturbance, malesoften were found at the periphery and females at the centerof groups. There was also an overlying influence of feedingon position; satiated individuals moved toward the center andhungry individuals toward the periphery. Several minutes aftera disturbance, sexual segregation disappeared, but segregationdue to hunger persisted. Sexual segregation in this study wasbest explained by the predator avoidance hypothesis, not theenergy needs hypothesis. Females weighed less than males; thismay make them more at risk to predation because of reduced swimmingspeed or less mechanical protection from their exoskeleton.No difference between the sexes was found in the volume of theirdefensive chemicals. This is one of the first studies to showthat sex influences position of individuals within simple nonmatinggroups (congregations) and suggests that more attention shouldbe given to positional sex differences within shoals, flocks,herds, and swarms.     

Sex promotes spatial and dietary segregation in a migratory shorebird during the non-breeding season

Several expressions of sexual segregation have been described in animals, especially in those exhibiting conspicuous dimorphism. Outside the breeding season, segregation has been mostly attributed to size or age-mediated dominance or to trophic niche divergence. Regardless of the recognized implications for population dynamics, the ecological causes and consequences of sexual segregation are still poorly understood. We investigate the foraging habits of a shorebird showing reversed sexual dimorphism, the black-tailed godwit Limosa limosa, during the winter season, and found extensive segregation between sexes in spatial distribution, microhabitat use and dietary composition. Males and females exhibited high site-fidelity but differed in their distributions at estuary-scale. Male godwits (shorter-billed) foraged more frequently in exposed mudflats than in patches with higher water levels, and consumed more bivalves and gastropods and fewer polychaetes than females. Females tended to be more frequently involved and to win more aggressive interactions than males. However, the number of aggressions recorded was low, suggesting that sexual dominance plays a lesser role in segregation, although its importance cannot be ruled out. Dimorphism in the feeding apparatus has been used to explain sex differences in foraging ecology and behaviour of many avian species, but few studies confirmed that morphologic characteristics drive individual differences within each sex. We found a relationship between resource use and bill size when pooling data from males and females. However, this relationship did not hold for either sex separately, suggesting that differences in foraging habits of godwits are primarily a function of sex, rather than bill size. Hence, the exact mechanisms through which this segregation operates are still unknown. The recorded differences in spatial distribution and resource use might expose male and female to distinct threats, thus affecting population dynamics through differential mortality. Therefore, population models and effective conservation strategies should increasingly take sex-specific requirements into consideration.     

Sex chromosome loss and non-disjunction in women: Analysis of chromosomal segregation in binucleated lymphocytes

Chromosomal lagging and non-disjunction are the main mechanisms of chromosomal malsegregation at mitosis. To date, the relative importance of these two events in the genesis of spontaneous or induced aneuploidy has not been fully elucidated. A methodology based on in situ hybridization with centromeric probes in binucleated lymphocytes was previously developed to provide some insight into this matter. With this method, both chromosomal loss and non-disjunction can be simultaneously detected by following the distribution of specific chromosomes in the nuclei and micronuclei of binucleated cells. In this study, this approach was used for studying the role of chromosomal loss and non-disjunction in the age-related malsegregation of sex chromosomes in females. For this purpose, cultures of cytokinesis-blocked lymphocytes were established from 12 healthy women ranging in age from 25 to 56. The occurrence of malsegregation of X chromosomes in vitro was estimated in binucleated cells that contained four signals, which orginates from the division of normal disomic cells. In this cell population, the frequencies of X chromosome loss and non-disjunction ranged from 0% to 1.69% (mean 0.75%), and from 0.20% to 1.33% (mean 0.57%), respectively. This indicates that both events contribute to malsegregation of X chromosomes in vitro. Moreover, a small but not negligible fraction of binucleated cells with two or six copies of the X chromosome was noticed in all donors. These cells, which are thought to arise from parental monosomic and trisomic types, may indicate the malsegregation of X chromosomes in vivo. The frequency of X chromosome aneuploidy both in vivo and in vitro significantly correlated with the age of donors. Analysis of chromosomal distribution in unbalanced cells demonstrated that both X homologues were frequently involved. The frequency of such multiple events (0.17%) was far greater than that expected by mere chance, indicating a tendency to multiple malsegregation events in the cell population investigated. Finally, parallel analysis of the segregation of chromosomex X and 1 in five of the donors confirmed the greater (about tenfold) susceptibility of X chromosomes to malsegregate compared with autosomes.     

No evidence of spatial root system segregation and elevated fine root biomass in multi-species temperate broad-leaved forests

Differences in spatial rooting patterns among coexisting species have been recognized as an important mechanism for generating biodiversity effects on ecosystem functioning. However, it is not yet clear whether complementarity in root space exploration is a universal characteristic of multi-species woody communities. In a temperate broad-leaved forest with a mosaic of species-poor and species-rich stands, we tested two hypotheses related to putative below-ground ‘overyielding’ in more diverse forests, (1) that species mixture results in a partial spatial segregation of the fine root systems of different species, and (2) that stand fine root biomass increases with tree species diversity. We investigated 12 stands either with one, three, or five dominant tree species (4 replicate stands each) under similar soil and climate conditions for stand fine root biomass and spatial root segregation in vertical and horizontal direction in the soil. Fine roots of different tree species were identified using a morphological key based on differences in colour, periderm surface structure, and branching patterns. In species-poor and species-rich stands, and in all tree species present, fine root density (biomass per soil volume) decreased exponentially with soil depth at very similar rates. Stand fine root biomass in the densely rooted upper soil (0–40 cm depth) was not significantly different between stands with 1, 3 or 5 dominant tree species. We conclude that ‘below-ground overyielding’ in terms of higher fine root biomasses in species-rich stands as compared to monospecific ones does not occur in these broad-leaved forests which most likely results from a missing complementarity in vertical rooting patterns of the present tree species.     

Top-down control of herbivory by birds and bats in the canopy of temperate broad-leaved oaks (Quercus robur)

The intensive foraging of insectivorous birds and bats is well known to reduce the density of arboreal herbivorous arthropods but quantification of collateral leaf damage remains limited for temperate forest canopies. We conducted exclusion experiments with nets in the crowns of young and mature oaks, Quercus robur, in south and central Germany to investigate the extent to which aerial vertebrates reduce herbivory through predation. We repeatedly estimated leaf damage throughout the vegetation period. Exclusion of birds and bats led to a distinct increase in arthropod herbivory, emphasizing the prominent role of vertebrate predators in controlling arthropods. Leaf damage (e.g., number of holes) differed strongly between sites and was 59% higher in south Germany, where species richness of vertebrate predators and relative oak density were lower compared with our other study site in central Germany. The effects of bird and bat exclusion on herbivory were 19% greater on young than on mature trees in south Germany. Our results support previous studies that have demonstrated clear effects of insectivorous vertebrates on leaf damage through the control of herbivorous arthropods. Moreover, our comparative approach on quantification of leaf damage highlights the importance of local attributes such as tree age, forest composition and species richness of vertebrate predators for control of arthropod herbivory.     

Competition and habitat suitability: small-scale segregation underpins large-scale coexistence of key species on temperate rocky shores

Identifying the mechanisms that underpin species richness is one of the central issues of community ecology. On rocky shores in north-western Europe, two key limpet species coexist on the mid- and low shore but are segregated at small scales with respect to habitat. Short-term and long-term experiments were done to test whether habitat suitability or habitat-specific competition drives the small-scale segregation of these species and therefore underpins their coexistence at larger spatial scales. In a controlled short-term experiment, Patella vulgata was transplanted onto open rock and into pools that either contained Patella ulyssiponensis and/or their mucus or from which P. ulyssiponensis and/or their mucus had been removed. After 2 days, P. vulgata remained in all experimental plots in similar numbers irrespective of treatment indicating that there was no negative response to P. ulyssiponensis, mucus or the pool habitat. In a long-term experiment, cage enclosures containing both species were set up in pools and on open rock over a 6-month period. P. vulgata grew equally well on both open rock and in pools but suffered higher mortality in pools. P. ulyssiponensis showed lower growth rate and higher mortality on open rock than in pools. P. ulyssiponensis exhibited increased growth in higher intraspecific densities on open rock and reduced growth in higher intraspecific densities in pools, indicating some degree of intraspecific facilitation on open rock and intraspecific competition in pools. There was no evidence of interspecific competition either in the short term or in the long term. Results revealed that habitat suitability was the mechanism causing segregation of these species at smaller spatial scales enabling them to coexist at larger spatial scales. Conflicting results in the short-term and long-term experiments highlight the importance of considering the correct temporal extent for experimental tests of hypotheses.