Stable‐hydrogen isotope turnover in red blood cells of two migratory thrushes: application to studies of connectivity and carry‐over effects

ABSTRACT Understanding turnover rates of stable isotopes in metabolically active tissues is critical for making spatial connections for migratory birds because samples provide information about pre‐migratory location only until the tissue turns over to reflect local values. We calculated stable‐hydrogen isotope (δ²H) turnover rate in the red blood cells of two long‐distance migratory songbirds, Bicknell's Thrushes (Catharus bicknelli) and Swainson's Thrushes (Catharus ustulatus), using samples collected at a breeding site in New Brunswick, Canada. Blood from both species captured early in the breeding site was more positive in δ²H than blood sampled later in the summer, but did not match blood values for wintering Bicknell's Thrushes. An asymptotic exponential model was used to estimate turnover of red blood cell δ²H and yielded a half‐life estimate of 21 days and 14 days for Bicknell's and Swainson's thrushes, respectively. Red blood cells of both species approached the local breeding site value one month after the first individuals were detected at the site. For Bicknell's Thrushes, estimated δ²H in blood at arrival (?72‰) was closer to blood collected at wintering sites (mean ?61‰) than to expected breeding site δ²H (?120‰). Discrimination values calculated for red blood cells collected at the breeding site for both species were greater than expected based on studies using keratin. Turnover during migration currently limits the use of blood sampled early in the breeding season for connectivity/carry‐over effect studies. However, direct tracking technology such as geolocators can provide information about migration duration, timing, and stopovers that can be used to improve isotopic turnover equations for metabolically active tissues.     

Role of breeding and natal movements in lifetime dispersal of a forest‐dwelling rodent

The lifetime movements of an individual determine the gene flow and invasion potential of the species. However, sex dependence of dispersal and selective pressures driving dispersal have gained much more attention than dispersal at different life and age stages. Natal dispersal is more common than dispersal between breeding attempts, but breeding dispersal may be promoted by resource availability and competition. Here, we utilize mark–recapture data on the nest‐box population of Siberian flying squirrels to analyze lifetime dispersal patterns. Natal dispersal means the distance between the natal nest and the nest used the following year, whereas breeding movements refer to the nest site changes between breeding attempts. The movement distances observed here were comparable to distances reported earlier from radio‐telemetry studies. Breeding movements did not contribute to lifetime dispersal distance and were not related to variation in food abundance or habitat patch size. Breeding movements of males were negatively, albeit not strongly, related to male population size. In females, breeding movement activity was low and was not related to previous breeding success or to competition between females for territories. Natal philopatry was linked to apparent death of a mother; that is, we did not find evidence for mothers bequeathing territories for offspring, like observed in some other rodent species. Our results give an example of a species in which breeding movements are not driven by environmental variability or nest site quality. Different evolutionary forces often operate in natal and breeding movements, and our study supports the view that juveniles are responsible for redistributing individuals within and between populations. This emphasizes the importance of knowledge on natal dispersal, if we want to understand consequences of movement ecology of the species at the population level.     

Effects of rearing conditions on natal dispersal processes in a long‐lived predator bird

Natal or prebreeding dispersal is a key driver of the functioning, dynamics, and evolution of populations. Conditions experienced by individuals during development, that is, rearing conditions, may have serious consequences for the multiple components that shape natal dispersal processes. Rearing conditions vary as a result of differences in parental and environmental quality, and it has been shown that favorable rearing conditions are beneficial for individuals throughout their lives. However, the long‐term consequences of rearing conditions on natal dispersal are still not fully understood in long‐lived birds. In this study, we aim to test the following hypotheses to address the relationship between rearing conditions and certain components of the natal dispersal process in Bonelli’s eagle (Aquila fasciata): (1) The body condition of nestlings depends on the quality of the territory and/or breeders; and (2) the survival until recruitment, (3) the age of recruitment, and (4) the natal dispersal distance (NDD) all depend on rearing conditions. As expected, nestlings reared in territories with high past productivity of chicks had better body condition, which indicates that both body condition and past productivity reflect the rearing conditions under which chicks are raised. In addition, chicks raised in territories with high past productivity and with good body condition had greater chances of surviving until recruitment. Furthermore, birds that have better condition recruit earlier, and males recruit at a younger age than females. At last, although females in good body condition exhibited higher NDD when they recruited at younger ages, this pattern was not observed in either older females or males. Overall, this study provides evidence that rearing conditions have important long‐term consequences in long‐lived birds. On the basis of our results, we advocate that conservation managers work actively in the promotion of actions aimed at improving the rearing conditions under which individuals develop in threatened populations.     

The short‐ and long‐term fitness consequences of natal dispersal in a wild bird population

Dispersal is a key process in population and evolutionary ecology. Individual decisions are affected by fitness consequences of dispersal, but these are difficult to measure in wild populations. A long‐term dataset on a geographically closed bird population, the Mauritius kestrel, offers a rare opportunity to explore fitness consequences. Females dispersed further when the availability of local breeding sites was limited, whereas male dispersal correlated with phenotypic traits. Female but not male fitness was lower when they dispersed longer distances compared to settling close to home. These results suggest a cost of dispersal in females. We found evidence of both short‐ and long‐term fitness consequences of natal dispersal in females, including reduced fecundity in early life and more rapid aging in later life. Taken together, our results indicate that dispersal in early life might shape life history strategies in wild populations.     

Sex‐specific estimates of dispersal show female philopatry and male dispersal in a promiscuous amphibian,the alpine salamander (Salamandra atra)

Amphibians display wide variations in life‐history traits and life cycles that should prove useful to explore the evolution of sex‐biased dispersal, but quantitative data on sex‐specific dispersal patterns are scarce. Here, we focused on Salamandra atra, an endemic alpine species showing peculiar life‐history traits. Strictly terrestrial and viviparous, the species has a promiscuous mating system, and females reproduce only every 3 to 4 years. In the present study, we provide quantitative estimates of asymmetries in male vs. female dispersal using both field‐based (mark–recapture) and genetic approaches (detection of sex‐biased dispersal and estimates of migration rates based on the contrast in genetic structure across sexes and age classes). Our results revealed a high level of gene flow among populations, which stems exclusively from male dispersal. We hypothesize that philopatric females benefit from being familiar with their natal area for the acquisition and defence of an appropriate shelter, while male dispersal has been secondarily favoured by inbreeding avoidance. Together with other studies on amphibians, our results indicate that a species' mating system alone is a poor predictor of sex‐linked differences in dispersal, in particular for promiscuous species. Further studies should focus more directly on the proximate forces that favour or limit dispersal to refine our understanding of the evolution of sex‐biased dispersal in animals.     

Extinction,reintroduction, and restoration of a lizard meta‐population equilibrium in the missouri ozarks

In this issue of Molecular Ecology, Neuwald & Templeton (2013) report on a 22‐year study of natural populations of Collared Lizards (Crotaphytus collaris) that evolved on isolated on rock outcrops (‘glades’) in the Ozark Mountains in eastern Missouri. This ecosystem was originally maintained by frequent fires that kept the forest understory open, but fire‐suppression was adopted as official policy in about 1945, which led to a loss of native biodiversity, including local extinctions of some lizard populations. Policies aimed at restoring biodiversity included controlled burns and re‐introductions of lizards to some glades, which began in 1984. Populations were monitored from 1984–2006, and demographic and genetic data collected from 1 679 lizards were used to documents shifts in meta‐population dynamics over four distinct phases of lizard recovery: 1–an initial translocation of lizards drawn from the same source populations onto three glades that were likely part of one meta‐population; 2–a period of isolation and genetic drift associated with the absence of fires; 3–a period of rapid colonization and population increase following restoration of fire; and 4–stabilization of the meta‐population under regular prescribed burning. This study system thus provides a rare opportunity to characterize the dynamics of a landscape‐scale management strategy on the restoration of the meta‐population of a reintroduced species; long‐term case studies of the extinction, founding, increase, and stabilization of a well‐defined meta‐population, based on both demographic and population genetic data, are rare in the conservation, ecological, and evolutionary literature.     

Dispersal patterns in a medium‐density Irish badger population: Implications for understanding the dynamics of tuberculosis transmission

European badgers (Meles meles) are group‐living mustelids implicated in the spread of bovine tuberculosis (TB) to cattle and act as a wildlife reservoir for the disease. In badgers, only a minority of individuals disperse from their natal social group. However, dispersal may be extremely important for the spread of TB, as dispersers could act as hubs for disease transmission. We monitored a population of 139 wild badgers over 7 years in a medium‐density population (1.8 individuals/km²). GPS tracking collars were applied to 80 different individuals. Of these, we identified 25 dispersers, 14 of which were wearing collars as they dispersed. This allowed us to record the process of dispersal in much greater detail than ever before. We show that dispersal is an extremely complex process, and measurements of straight‐line distance between old and new social groups can severely underestimate how far dispersers travel. Assumptions of straight‐line travel can also underestimate direct and indirect interactions and the potential for disease transmission. For example, one female disperser which eventually settled 1.5 km from her natal territory traveled 308 km and passed through 22 different territories during dispersal. Knowledge of badgers' ranging behavior during dispersal is crucial to understanding the dynamics of TB transmission, and for designing appropriate interventions, such as vaccination.     

The interacting effects of food,spring temperature,and global climate cycles on population dynamics of a migratory songbird

Although long‐distance migratory songbirds are widely believed to be at risk from warming temperature trends, species capable of attempting more than one brood in a breeding season could benefit from extended breeding seasons in warmer springs. To evaluate local and global factors affecting population dynamics of the black‐throated blue warbler (Setophaga caerulescens), a double‐brooded long‐distance migrant, we used Pradel models to analyze 25 years of mark–recapture data collected in New Hampshire, USA. We assessed the effects of spring temperature (local weather) and the El Niño Southern Oscillation index (a global climate cycle), as well as predator abundance, insect biomass, and local conspecific density on population growth in the subsequent year. Local and global climatic conditions affected warbler populations in different ways. We found that warbler population growth was lower following El Niño years (which have been linked to poor survival in the wintering grounds and low fledging weights in the breeding grounds) than La Niña years. At a local scale, populations increased following years with warm springs and abundant late‐season food, but were unaffected by spring temperature following years when food was scarce. These results indicate that the warming temperature trends might have a positive effect on recruitment and population growth of black‐throated blue warblers if food abundance is sustained in breeding areas. In contrast, potential intensification of future El Niño events could negatively impact vital rates and populations of this species.     

Fine‐scale spatiotemporal patterns of genetic variation reflect budding dispersal coupled with strong natal philopatry in a cooperatively breeding mammal

The relatedness structure of animal populations is thought to be a critically important factor underlying the evolution of mating systems and social behaviours. While previous work has shown that population structure is shaped by many biological processes, few studies have investigated how these factors vary over time. Consequently, we explored the fine‐scale spatiotemporal genetic structure of an intensively studied population of cooperatively breeding banded mongooses (Mungos mungo) over a 10‐year period. Overall population structure was strong (average F_ST = 0.129) but groups with spatially overlapping territories were not more genetically similar to one another than noncontiguous groups. Instead, genetic differentiation was associated with historical group‐fission (budding) events, with new groups diverging from their parent groups over time. Within groups, relatedness was high within but not between the sexes, although the latter increased over time since group formation due to group founders being replaced by philopatric young. This trend was not mirrored by a decrease in average offspring heterozygosity over time, suggesting that close inbreeding may often be avoided, even when immigration into established groups is virtually absent and opportunities for extra‐group matings are rare. Fine‐scale spatiotemporal population structure could have important implications in social species, where relatedness between interacting individuals is a vital component in the evolution of patterns of inbreeding avoidance, reproductive skew and kin‐selected helping and harming.     

Temperature‐driven color lightness and body size variation scale to local assemblages of European Odonata but are modified by propensity for dispersal

1. Previous macrophysiological studies suggested that temperature‐driven color lightness and body size variations strongly influence biogeographical patterns in ectotherms. However, these trait–environment relationships scale to local assemblages and the extent to which they can be modified by dispersal remains largely unexplored. We test whether the predictions of the thermal melanism hypothesis and the Bergmann's rule hold for local assemblages. We also assess whether these trait–environment relationships are more important for species adapted to less stable (lentic) habitats, due to their greater dispersal propensity compared to those adapted to stable (lotic) habitats.
2. We quantified the color lightness and body volume of 99 European dragon‐ and damselflies (Odonata) and combined these trait information with survey data for 518 local assemblages across Europe. Based on this continent‐wide yet spatially explicit dataset, we tested for effects temperature and precipitation on the color lightness and body volume of local assemblages and assessed differences in their relative importance and strength between lentic and lotic assemblages, while accounting for spatial and phylogenetic autocorrelation.
3. The color lightness of assemblages of odonates increased, and body size decreased with increasing temperature. Trait–environment relationships in the average and phylogenetic predicted component were equally important for assemblages of both habitat types but were stronger in lentic assemblages when accounting for phylogenetic autocorrelation.
4. Our results show that the mechanism underlying color lightness and body size variations scale to local assemblages, indicating their general importance. These mechanisms were of equal evolutionary significance for lentic and lotic species, but higher dispersal ability seems to enable lentic species to cope better with historical climatic changes. The documented differences between lentic and lotic assemblages also highlight the importance of integrating interactions of thermal adaptations with proxies of the dispersal ability of species into trait‐based models, for improving our understanding of climate‐driven biological responses.

     

Genomic analysis of a migratory divide reveals candidate genes for migration and implicates selective sweeps in generating islands of differentiation

Differential gene flow, reductions in diversity following linked selection and/or features of the genome can structure patterns of genomic differentiation during the process of speciation. Possible sources of reproductive isolation are well studied between coastal and inland subspecies groups of Swainson's thrushes, with differences in seasonal migratory behaviour likely playing a key role in reducing hybrid fitness. We assembled and annotated a draft reference genome for this species and generated whole‐genome shotgun sequence data for populations adjacent to the hybrid zone between these groups. We documented substantial genomewide heterogeneity in relative estimates of genetic differentiation between the groups. Within population diversity was lower in areas of high relative differentiation, supporting a role for selective sweeps in generating this pattern. Absolute genetic differentiation was reduced in these areas, further suggesting that recurrent selective sweeps in the ancestral population and/or between divergent populations following secondary contact likely occurred. Relative genetic differentiation was also higher near centromeres and on the Z chromosome, suggesting that features of the genome also contribute to genomewide heterogeneity. Genes linked to migratory traits were concentrated in islands of differentiation, supporting previous suggestions that seasonal migration is under divergent selection between Swainson's thrushes. Differences in migratory behaviour likely play a central role in the speciation of many taxa; we developed the infrastructure here to permit future investigations into the role several candidate genes play in reducing gene flow between not only Swainson's thrushes but other species as well.     

Disentangling the effects of environmental conditions on wintering and breeding grounds on age‐specific survival rates in a trans‐Saharan migratory raptor

Migratory species are subject to environmental variability occurring on breeding and wintering grounds. Estimating the relative contribution of environmental factors experienced sequentially during breeding and wintering, and their potential interaction, to the variation of survival is crucial to predict population viability of migratory species. Here we investigated this issue for the Montagu's harrier Circus pygargus, a trans‐Saharan migrant. We analysed capture–recapture data from a 29‐year long monitoring of wing‐tagged offspring and adults at two study sites in France (Rochefort‐RO and Maine‐et‐Loire‐ML). The study period covers a climatic shift occurring in the Sahel with increasing rainfall following a period of droughts (Sahel greening). We found that harriers’ adult survival in RO (between 1988 and 2005) varied over time and was sensitive to the interaction between the amount of rainfall in the Sahel and the annual mean breeding success, two proxies of prey availability. The occurrence of adverse conditions on breeding and wintering grounds in the same year decreased survival from 0.70–0.77 to 0.48 ± 0.05. Juvenile survival in RO was slightly more sensitive to conditions in Europe than in the Sahel. Unexpectedly, lower survival rates were found in years with higher mean breeding success, suggesting compensatory density feedbacks may operate. By contrast, adult survival in ML, monitored between 1999 and 2017, was higher compared to RO (0.76 ± 0.03 versus 0.66 ± 0.02), remained constant and unaffected by any proxy of prey availability. This difference seems consistent with the fact that harriers in ML experienced better and especially less variable environmental conditions during breeding and wintering seasons compared to RO. Overall, we showed that survival of a migratory bird is sensitive to the level of variability in environmental conditions and that adverse conditions on wintering grounds can amplify the negative effects of conditions during the previous breeding season on birds’ survival.     

Global macroecology of bird assemblages in urbanized and semi‐natural ecosystems

Aim Despite the increasing pace of urbanization, little is known about how this process affects biodiversity globally. We investigate macroecological patterns of bird assemblages in urbanized areas relative to semi‐natural ecosystems. Location World‐wide. Methods We use a database of quantitative bird surveys to compare key assemblage structure parameters for plots in urbanized and semi‐natural ecosystems controlling for spatial autocorrelation and survey methodology. We use the term ‘urbanized’ instead of ‘urban’ ecosystems as many of the plots were not located in the centre of towns but in remnant habitat patches within conurbations. Results Some macroecological relationships were conserved in urbanized landscapes. Species–area, species–abundance and species–biomass relationships did not differ significantly between urbanized and non‐urbanized environments. However, there were differences in the relationships between productivity and assemblage structure. In forests, species richness increased with productivity; in both forests and open habitats, the evenness of species abundances declined as productivity increased. Among urbanized plots, instead, both species richness and the evenness of species abundances were independent of variation in productivity. Main conclusions Remnant habitats within urbanized areas are subject to many ecological alterations, yet key macroecological patterns differ remarkably little in urbanized versus non‐urbanized plots. Our results support the need for increased conservation activities in urbanized landscapes, particularly given the additional benefits of local experiences of biodiversity for the human population. With increasing urbanization world‐wide, broad‐scale efforts are needed to understand and manage the effects of this driver of change on biodiversity.     

Effects of parents and Brown‐headed Cowbirds (Molothrus ater) on nest predation risk for a songbird

Nest predation limits avian fitness, so ornithologists study nest predation, but they often only document patterns of predation rates without substantively investigating underlying mechanisms. Parental behavior and predator ecology are two fundamental drivers of predation rates and patterns, but the role of parents is less certain, particularly for songbirds. Previous work reproduced microhabitat‐predation patterns experienced by Yellow Warblers (Setophaga petechia) in the Mono Lake basin at experimental nests without parents, suggesting that these patterns were driven by predator ecology rather than predator interactions with parents. In this study, we further explored effects of post‐initiation parental behavior (nest defense and attendance) on predation risk by comparing natural versus experimental patterns related to territory density, seasonal timing of nest initiation, and nest age. Rates of parasitism by Brown‐headed Cowbirds (Molothrus ater) were high in this system (49% nests parasitized), so we also examined parasitism‐predation relationships. Natural nest predation rates (NPR) correlated negatively with breeding territory density and nonlinearly (U‐shaped relationship) with nest‐initiation timing, but experimental nests recorded no such patterns. After adjusting natural‐nest data to control for these differences from experimental nests other than the presence of parents (e.g., defining nest failure similarly and excluding nestling‐period data), we obtained similar results. Thus, parents were necessary to produce observed patterns. Lower natural NPR compared with experimental NPR suggested that parents reduced predation rates via nest defense, so this parental behavior or its consequences were likely correlated with density or seasonal timing. In contrast, daily predation rates decreased with nest age for both nest types, indicating this pattern did not involve parents. Parasitized nests suffered higher rates of partial predation but lower rates of complete predation, suggesting direct predation by cowbirds. Explicit behavioral research on parents, predators (including cowbirds), and their interactions would further illuminate mechanisms underlying the density, seasonal, and nest age patterns we observed.