Adjustment of the annual cycle to climatic change in a long-lived migratory bird species

Climate change has advanced the phenology of many organisms. Migratory animals face particular problems because climate change in the breeding and the wintering range may be asynchronous, preventing rapid response to changing conditions. Advancement in timing of spring migration may have carry-over effects to other parts of the annual cycle, simply because advancement of one event in the annual cycle also advances subsequent events, gradually causing a general shift in the timing of the entire annual cycle. Such a phenotypic shift could generate accumulating effects over the years for individuals, but also across generations. Here we test this novel hypothesis of phenotypic response to climate change by using long-term data on the Arctic tern Sterna paradisaea. Mean breeding date advanced by almost three weeks during the last 70 years. Annual arrival date at the breeding grounds during a period of 47 years was predicted by environmental conditions in the winter quarters in the Southern Ocean near the Antarctic and by mean breeding date the previous year. Annual mean breeding date was only marginally determined by timing of arrival the current year, but to a larger extent by arrival date and breeding date the previous year. Learning affected arrival date as shown by a positive correlation between arrival date in year (i+1) relative to breeding date in year (i) and the selective advantage of early breeding in year (i). This provides a mechanism for changes in arrival date being adjusted to changing environmental conditions. This study suggests that adaptation to changing climatic conditions can be achieved through learning from year to year[Current Zoology 55(2):92-101,2009].     

Cavity use throughout the annual cycle of a migratory woodpecker revealed by geolocators

The importance of cavities as roost sites in migratory species is often unknown because it is challenging to monitor cavity use during the non‐breeding period. We documented cavity use throughout the annual cycle of a woodpecker using light‐level geolocators. Northern Flickers Colaptes auratus spent 63–90% of nights roosting in a cavity throughout the year, including during migration. The high frequency of year‐round cavity use by Flickers suggests that cavities provide benefits beyond nest‐sites. Our work highlights the potential use of geolocators to examine cavity use.     

Population identification of western hemisphere shorebirds throughout the annual cycle

Identification of relationships among geographically distinct populations of migratory species can provide an understanding of breeding and natal philopatry, migration pathways, and population mixing during winter. We used random amplified polymorphic DNA (RAPD) analyses to search for markers specific to difficult-to-differentiate shorebird species (e.g. long-billed dowitcher Limnodromus scolopaceus and short-billed dowitcher L. griseus ) as well as geographically distinct breeding populations of Hudsonian godwits Limosa haemastica , red-necked phalaropes Phalaropus lobatus , semipalmated plovers Charadrius semipalmatus , dunlin Calidris alpina , pectoral sandpipers C. melanotos , semipalmated sandpipers C. pusilla and western sandpipers C. mauri . Markers clearly differentiated all shorebird species. Estimates of population differentiation varied greatly among species ( F _ST= 0.095–0.685) and correlated with interspecific variation in philopatry and geographical separation of breeding populations. We assigned individuals to putative breeding locales with greater certainty in well-differentiated species than in poorly differentiated species. Our findings indicate specific phylogeographical structure varies among species, which has strong implications for conservation of habitats within migratory corridors. We suggest that RAPDs are useful in identifying geographical populations of migratory species and that molecular markers should be considered for tracking migratory birds throughout the annual cycle.     

Hatching date influences winter habitat occupancy: Examining seasonal interactions across the full annual cycle in a migratory songbird

Birds experience a sequence of critical events during their life cycle, and past events can subsequently determine future performance via carry‐over effects. Events during the non‐breeding season may influence breeding season phenology or productivity. Less is understood about how events during the breeding season affect individuals subsequently in their life cycle. Using stable carbon isotopes, we examined carry‐over effects throughout the annual cycle of prairie warblers (Setophaga discolor), a declining Nearctic–Neotropical migratory passerine bird. In drier winters, juvenile males that hatched earlier at our study site in Massachusetts, USA, occupied wetter, better‐quality winter habitat in the Caribbean, as indicated by depleted carbon isotope signatures. For juveniles that were sampled again as adults, repeatability in isotope signatures indicated similar winter habitat occupancy across years. Thus, hatching date of juvenile males appears to influence lifetime winter habitat occupancy. For adult males, reproductive success did not carry over to influence winter habitat occupancy. We did not find temporally consecutive “domino” effects across the annual cycle (breeding to wintering to breeding) or interseasonal, intergenerational effects. Our finding that a male''s hatching date can have a lasting effect on winter habitat occupancy represents an important contribution to our understanding of seasonal interactions in migratory birds.     

Connecting the dots: Stopover strategies of an intercontinental migratory songbird in the context of the annual cycle

The phases of the annual cycle for migratory species are inextricably linked. Yet, less than five percent of ecological studies examine seasonal interactions. In this study, we utilized stable hydrogen isotopes to geographically link individual black‐and‐white warblers (Mniotilta varia) captured during spring migration with breeding destinations to understand a migrant's stopover strategy in the context of other phases of the annual cycle. We found that stopover strategy is not only a function of a bird's current energetic state, but also the distance remaining to breeding destination and a bird's time‐schedule, which has previously been linked to habitat conditions experienced in the preceding phase of the annual cycle. Birds in close proximity to their breeding destination accumulate additional energy reserves prior to arrival on the breeding grounds, as reflected by higher migratory condition upon arrival, higher refueling rates measured via blood plasma metabolites, and longer stopover durations compared to birds migrating to breeding destinations farther from the stopover site. However, late birds near their breeding destination were more likely to depart on the day of arrival (i.e., transients), and among birds that stopped over at the site, the average duration of stopover was almost half the time of early conspecifics, suggesting late birds are trying to catch‐up with the overall time‐schedule of migration for optimal arrival time on the breeding grounds. In contrast, birds with long distances remaining to breeding destinations were more likely to depart on the day of arrival and primarily used stopover to rest before quickly resuming migration, adopting similar strategies regardless of a bird's time‐schedule. Our study demonstrates that migrants adjust their en route strategies in relation to their time‐schedule and distance remaining to their breeding destination, highlighting that strategies of migration should be examined in the context of other phases of the annual cycle.     

Climate and density influence annual survival and movement in a migratory songbird

Assessing the drivers of survival across the annual cycle is important for understanding when and how population limitation occurs in migratory animals. Density‐dependent population regulation can occur during breeding and nonbreeding periods, and large‐scale climate cycles can also affect survival throughout the annual cycle via their effects on local weather and vegetation productivity. Most studies of survival use mark–recapture techniques to estimate apparent survival, but true survival rates remain obscured due to unknown rates of permanent emigration. This is especially problematic when assessing annual survival of migratory birds, whose movement between breeding attempts, or breeding dispersal, can be substantial. We used a multistate approach to examine drivers of annual survival and one component of breeding dispersal (habitat‐specific movements) in a population of American redstarts (Setophaga ruticilla) over 11 years in two adjacent habitat types. Annual survival displayed a curvilinear relation to the Southern Oscillation Index, with lower survival during La Niña and El Niño conditions. Although redstart density had no impact on survival, habitat‐specific density influenced local movements between habitat types, with redstarts being less likely to disperse from their previous year's breeding habitat as density within that habitat increased. This finding was strongest in males and may be explained by conspecific attraction influencing settlement decisions. Survival was lowest in young males, but movement was highest in this group, indicating that apparent survival rates were likely biased low due to permanent emigration. Our findings demonstrate the utility of examining breeding dispersal in mark–recapture studies and complement recent work using spatially explicit models of dispersal probability to obtain greater accuracy in survival estimates.     

Population assignment reveals low migratory connectivity in a weakly structured songbird

Understanding migratory connectivity is essential for determining the drivers behind population dynamics and for implementing effective conservation strategies for migratory species. Genetic markers provide a means to describe migratory connectivity; however, they can be uninformative for species with weak population genetic structure, which has limited their application. Here, we demonstrated a genomic approach to describing migratory connectivity in the prothonotary warbler, Protonotaria citrea, a Neotropical songbird of conservation concern. Using 26,189 single nucleotide polymorphisms (SNPs), we revealed regional genetic structure between the Mississippi River Valley and the Atlantic Seaboard with overall weak genetic differentiation among populations (F_ST = 0.0055; 95% CI: 0.0051–0.0059). Genetic variation had a stronger association with geographic rather than environmental factors, with each explaining 14.5% and 8.2% of genetic variation, respectively. By varying the numbers of genomic markers used in population assignment models with individuals of known provenance, we identified a maximum assignment accuracy (89.7% to site, 94.3% to region) using a subset of 600 highly differentiated SNPs. We then assigned samples from nonbreeding sites to breeding region and found low migratory connectivity. Our results highlight the importance of filtering markers for informative loci in models of population assignment. Quantifying migratory connectivity for weakly structured species will be useful for expanding studies to a wider range of migratory species across taxonomic groups and may contribute to a deeper understanding of the evolution of migratory strategies.     

Behavioural response of a migratory songbird to geographic variation in song and morphology

Introduction

Sexually selected traits contribute substantially to evolutionary diversification, for example by promoting assortative mating. The contributing traits and their relevance for reproductive isolation differ between species. In birds, sexually selected acoustic and visual signals often undergo geographic divergence. Clines in these phenotypes may be used by both sexes in the context of sexual selection and territoriality. The ways conspecifics respond to geographic variation in phenotypes can give insights to possible behavioural barriers, but these may depend on migratory behaviour. We studied a migratory songbird, the Stonechat, and tested its responsiveness to geographic variation in male song and morphology. The traits are acquired differently, with possible implications for population divergence. Song can evolve quickly through cultural transmission, and thus may contribute more to the establishment of geographic variation than inherited morphological traits. We first quantified the diversity of song traits from different populations. We then tested the responses of free-living Stonechats of both sexes to male phenotype with playbacks and decoys, representing local and foreign stimuli derived from a range of distances from the local population.

Results

Both sexes discriminated consistently between stimuli from different populations, responding more strongly to acoustic and morphological traits of local than foreign stimuli. Time to approach increased, and time spent close to the stimuli and number of tail flips decreased consistently with geographic distance of the stimulus from the local population. Discriminatory response behaviour was more consistent for acoustic than for morphological traits. Song traits of the local population differed significantly from those of other populations.

Conclusions

Evaluating an individual’s perception of geographic variation in sexually selected traits is a crucial first step for understanding reproductive isolation mechanisms. We have demonstrated that in both sexes of Stonechats the responsiveness to acoustic and visual signals decreased with increasing geographic distance of stimulus origin. These findings confirm consistent, fine discrimination for both learned song and inherited morphological traits in these migratory birds. Maintenance or further divergence in phenotypic traits could lead to assortative mating, reproductive isolation, and potentially speciation.

     

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.     

Conditions on the Mexican moulting grounds influence feather colour and carotenoids in Bullock's orioles (Icterus bullockii)

Carotenoid‐based plumage coloration plays a critical role for both inter‐ and intrasexual communication. Habitat and diet during molt can have important consequences for the development of the ornamental signals used in these contexts. When molt occurs away from the breeding grounds (e.g., pre‐alternate molt on the wintering grounds, or stopover molt), discerning the influence of habitat and diet can be particularly important, as these effects may result in important carryover effects that influence territory acquisition or mate choice in subsequent seasons. Several species of songbirds in western North America, including the Bullock's oriole (Icterus bullockii), migrate from the breeding grounds to undergo a complete prebasic (post‐breeding) molt at a stopover site in the region affected by the Mexican monsoon climate pattern. This strategy appears to have evolved several times independently in response to the harsh, food‐limited late‐summer conditions in the arid West, which contrast strongly with the high productivity driven by heavy rains that is characteristic of the Mexican monsoon region. Within this region, individuals may be able to optimize plumage coloration by molting in favourable areas characterized by high resource abundance. We used stable isotope analysis (δ¹³C, δ¹⁵N) to ask whether the diet and molt habitat/location of Bullock's orioles influenced their expression of carotenoid‐based plumage coloration as well as plumage carotenoid content and composition. Bullock's orioles with lower feather δ¹⁵N values acquired more colorful plumage (orange‐shifted hue) but had feathers with lower total carotenoid concentration, lower zeaxanthin concentration, and marginally lower canthaxanthin and lutein concentration. Examining factors occurring throughout the annual cycle are critical for understanding evolutionary and ecological processes. Here, we demonstrate that conditions experienced during a stopover molt, occurring hundreds to thousands of kilometers from the breeding grounds, influence the production of ornamental plumage coloration, which may carryover to influence inter‐ and intrasexual signaling in subsequent seasons.     

Climate change leads to differential shifts in the timing of annual cycle stages in a migratory bird

Shifts in reproductive phenology due to climate change have been well documented in many species but how, within the same species, other annual cycle stages (e.g. moult, migration) shift relative to the timing of breeding has rarely been studied. When stages shift at different rates, the interval between stages may change resulting in overlaps, and as each stage is energetically demanding, these overlaps may have negative fitness consequences. We used long‐term data of a population of European pied flycatchers (Ficedula hypoleuca) to investigate phenological shifts in three annual cycle stages: spring migration (arrival dates), breeding (egg‐laying and hatching dates) and the onset of postbreeding moult. We found different advancements in the timing of breeding compared with moult (moult advances faster) and no advancement in arrival dates. To understand these differential shifts, we explored which temperatures best explain the year‐to‐year variation in the timing of these stages, and show that they respond differently to temperature increases in the Netherlands, causing the intervals between arrival and breeding and between breeding and moult to decrease. Next, we tested the fitness consequences of these shortened intervals. We found no effect on clutch size, but the probability of a fledged chick to recruit increased with a shorter arrival‐breeding interval (earlier breeding). Finally, mark–recapture analyses did not detect an effect of shortened intervals on adult survival. Our results suggest that the advancement of breeding allows more time for fledgling development, increasing their probability to recruit. This may incur costs to other parts of the annual cycle, but, despite the shorter intervals, there was no effect on adult survival. Our results show that to fully understand the consequences of climate change, it is necessary to look carefully at different annual cycle stages, especially for organisms with complex cycles, such as migratory birds.     

Nitrogen accumulation and mobilization in Citrus leaves throughout the annual cycle

The changes of protein and amino acid contents of young and old leaves from field citrus trees [ Citrus sinensis (L.) Osbeck cv. Washington Navel] were studied throughout the year. the total protein content of old leaves decreased during the spring and summer growths, whereas in young developing leaves it increased rapidly. The end of the spring and summer flushes was followed by a quick recovery of the initial protein content due to a process of reversible senescence. The evolution of SDS-PAGE proteinograms indicated that most of the foliar proteins contributed to the nitrogen mobilization during the spring and summer growth periods. A protein band of molecular weight ca 55,000, probably containing the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase, decreased relatively more than the others. The amino acid content of the leaves increased during winter time due to the accumulation of proline, which was mobilized during the spring flush. The possible nitrogen storage function of proline is discussed.     

Contrast influences female attraction to performance-based sexual signals in a songbird

Animals do not make decisions in a bubble but often refer to previous experience when discriminating between options. Contrast effects occur when the value of a stimulus affects the response to another value of the stimulus, and the changes in value and response are in the same direction. Although contrast effects appear irrational, they could benefit decision makers when there is spatial or temporal variation and autocorrelation in the value of stimuli that elicit decisions. Here, we examined whether contrasts influence female evaluation of male performance-based sexual signals. We exposed female Lincoln''s sparrows (Melospiza lincolnii) to one week of songs that we had experimentally reduced or elevated in performance, followed by a novel song of intermediate performance. We found that high-performance songs were more attractive to females than low-performance songs. Moreover, the intermediate songs were more attractive following exposure to low- than to high-performance songs. These results indicate that contrast can influence evaluation of performance-based sexual stimuli. By examining contrast effects in the ecologically relevant context of mate choice for performance, we can better understand both the adaptive value of comparative evaluation as well as the mechanisms that underlie variation in mate choice and sexual selection.     

Migratory shorebird adheres to Bergmann's Rule by responding to environmental conditions through the annual lifecycle

The inverse relationship between body size and environmental temperature is a widespread ecogeographic pattern. However, the underlying forces that produce this pattern are unclear in many taxa. Expectations are particularly unclear for migratory species, as individuals may escape environmental extremes and reorient themselves along the environmental gradient. In addition, some aspects of body size are largely fixed while others are environmentally flexible and may vary seasonally. Here, we used a long‐term dataset that tracked multiple populations of the migratory piping plover Charadrius melodus across their breeding and non‐breeding ranges to investigate ecogeographic patterns of phenotypically flexible (body mass) and fixed (wing length) size traits in relation to latitude (Bergmann's Rule), environmental temperature (heat conservation hypothesis), and migratory distance. We found that body mass was correlated with both latitude and temperature across the breeding and non‐breeding ranges, which is consistent with predictions of Bergmann's Rule and heat conservation. However, wing length was correlated with latitude and temperature only on the breeding range. This discrepancy resulted from low migratory connectivity across seasons and the tendency for individuals with longer wings to migrate farther than those with shorter wings. Ultimately, these results suggest that wing length may be driven more by conditions experienced during the breeding season or tradeoffs related to migration, whereas body mass is modified by environmental conditions experienced throughout the annual lifecycle.     

Multiple selection pressures generate adherence to Bergmann's rule in a Neotropical migratory songbird

Aim Bergmann's rule, the tendency for body size to be positively correlated with latitude, is widely accepted but the mechanisms behind the patterns are still debated. Bergmann's originally conceived mechanism was based on heat conservation; other proposed mechanisms invoke phylogeny, migration distance and resource seasonality. With the goal of examining these mechanisms, we quantified morphological variation across the breeding range of a Neotropical migratory songbird, the cerulean warbler (Dendroica cerulea). Location Deciduous forests of eastern North America. Methods We sampled nine cerulean warbler populations, spanning the species’ breeding range. We captured 156 males using targeted playback and model presentation, and included 127 adult males in our analyses of morphological variation. We used an information‐theoretical approach to identify climatic variables associated with geographical variation in body size. Results Cerulean warbler body size adheres to Bergmann's rule: individuals in northern populations are larger than those in southern populations. Variation in body size is best explained by variation in dry and wet‐bulb temperature and actual evapotranspiration. Main conclusions Adherence to Bergmann's rule by the cerulean warbler appears to be linked to thermodynamics (heat conservation in the north, evaporative cooling in the south) and resource seasonality. Multiple selection pressures can interact to generate a single axis of morphological geographical variation, and even subtle fluctuations in climatic variables can exert significant selection pressures. We suggest that the influence of selection pressures on migrants might be enhanced by migratory connectivity, providing further support for the important role played by this phenomenon in the ecology, evolution and population dynamics of migratory songbirds.     

Demographic responses to climate‐driven variation in habitat quality across the annual cycle of a migratory bird species

The demography and dynamics of migratory bird populations depend on patterns of movement and habitat quality across the annual cycle. We leveraged archival GPS‐tagging data, climate data, remote‐sensed vegetation data, and bird‐banding data to better understand the dynamics of black‐headed grosbeak (Pheucticus melanocephalus) populations in two breeding regions, the coast and Central Valley of California (Coastal California) and the Sierra Nevada mountain range (Sierra Nevada), over 28 years (1992–2019). Drought conditions across the annual cycle and rainfall timing on the molting grounds influenced seasonal habitat characteristics, including vegetation greenness and phenology (maturity dates). We developed a novel integrated population model with population state informed by adult capture data, recruitment rates informed by age‐specific capture data and climate covariates, and survival rates informed by adult capture–mark–recapture data and climate covariates. Population size was relatively variable among years for Coastal California, where numbers of recruits and survivors were positively correlated, and years of population increase were largely driven by recruitment. In the Sierra Nevada, population size was more consistent and showed stronger evidence of population regulation (numbers of recruits and survivors negatively correlated). Neither region showed evidence of long‐term population trend. We found only weak support for most climate–demographic rate relationships. However, recruitment rates for the Coastal California region were higher when rainfall was relatively early on the molting grounds and when wintering grounds were relatively cool and wet. We suggest that our approach of integrating movement, climate, and demographic data within a novel modeling framework can provide a useful method for better understanding the dynamics of broadly distributed migratory species.