Breeding timed to maximize reproductive success for a migratory songbird: the importance of phenological asynchrony

Phenological advances and trophic mismatches are frequently reported ecological consequences of climate warming. Trophic mismatches occur when phenological responses to environmental conditions differ among trophic levels such that the timing of resource demand by consumers becomes decoupled from supply. We used 25 years of demographic measurements of a migratory songbird (the black‐throated blue warbler Setophaga caerulescens) to compare its breeding phenology to the phenology of both its caterpillar prey and the foliage on which caterpillars feed. Caterpillar biomass in this forest did not show a predictable seasonal pulse. Nest initiation by warblers in this northern hardwood forest was therefore not timed to coincide with a peak in food availability for nestlings. Nonetheless, timing of first clutches was strongly associated with spring leaf expansion (slope ± SE = 0.56 ± 0.08 days per day of change in leaf phenology, R² = 0.66). Warblers adjusted the timing of breeding to early springs mainly by shortening the interval between arrival and clutch initiation, but this likely has limits because recent early springs are approaching the relatively inflexible dates when birds arrive on the breeding grounds. Although the timing of first nests did not match 1:1 with leaf‐out phenology, the adjustments in breeding time maximized mean annual reproductive success. Nest predation had the greatest effect on annual reproductive success, but the ability of nesting warblers to appropriately track leaf phenology accounted for effects on annual reproductive success comparable to the influence of variation in caterpillar abundance and conspecific density. Nesting phenology in black‐throated blue warblers was generally well matched to the timing of leaf‐out, even though the match was not 1:1. Without measurements of reproductive success, these unequal phenological shifts might otherwise have been interpreted as having negative ecological consequences.     

Ecological conditions in wintering and passage areas as determinants of timing of spring migration in trans-Saharan migratory birds

1.?Climate change has been associated with shifts in the timing of biological events, including the spring arrival of migratory birds. Early arrival at breeding sites is an important life-history trait, usually associated with higher breeding success and therefore, susceptible to selection and evolution in response to changing climatic conditions. 2.?Here, we examine the effect of changes in the environmental conditions of wintering and passage areas on the mean passage time of 13 trans-Saharan passerines during their spring migration through the western Mediterranean over the 15 years from 1993 to 2007. 3.?We found that most of the species studied have been advancing the timing of their passage in recent years. However, annual variation in the mean date of passage was positively correlated with vegetation growth (measured as the normalized difference vegetation index [NDVI]) both in the Sahel (the region of departure) and in northern Africa (the passage area). Thus, migration dates were delayed in years with high primary productivity in passage and wintering zones. All species seem to respond similarly to NDVI in the Sahel; however, late migrants were less affected by ecological conditions in northern Africa than those migrating earlier, suggesting differences based on species ecology. 4.?Mean timing of passage was not related to the North Atlantic Oscillation (NAO), El Ni?o-Southern Oscillation (ENSO), temperature or NDVI in the species-specific wintering areas (the overwintering region) when analysed in combination with the other covariates. 5.?Our findings show that ecological conditions in the winter quarters (specifically the Sahel) and en route are relevant factors influencing trends in the passage dates of trans-Saharan migratory birds on the southern fringe of Europe. Possible long-term consequences for late arriving spring migrants are discussed.     

Variable reproductive effort for two ptarmigan species in response to spring weather in a northern alpine ecosystem

Predicting how animal populations respond to climate change requires knowledge of how species traits influence the response of individuals to variation in anuual weather. Over a four‐year study with two warm and two cold years, we examined how sympatric rock ptarmigan Lagopus muta and white‐tailed ptarmigan L. leucura in the southern Yukon Territory respond to spring weather in terms of breeding phenology and the allocation of reproductive effort. The onset of breeding was approximately synchronous; for each one‐degree rise in spring temperature, mean breeding dates of rock and white‐tailed ptarmigan advanced by about 2.7 and 4 days respectively. Although onset of breeding was similar, the two species differed in their reproductive effort. As breeding was delayed, average first clutch sizes of rock ptarmigan declined from 9.4 to 5.8 eggs over the breeding period, while those of white‐tailed ptarmigan only declined from an average of 7.8 to 6.8. Rock ptarmigan were also less likely to re‐nest if their first clutch was lost to predators and as a consequence they had shorter breeding seasons. White‐tailed ptarmigan produced about 25% more offspring annually than rock ptarmigan and contributed more young through re‐nesting. While white‐tailed ptarmigan had higher annual reproductive output, adult rock ptarmigan had a 20–25% higher annual survival rate, which may indicate a reproduction–survival trade‐off for the two species. These results show that even within the same location, closely related species can differ in how they allocate effort as environmental conditions fluctuate.     

Comparing the seasonal survival of resident and migratory oystercatchers: carry‐over effects of habitat quality and weather conditions

Events happening in one season can affect life‐history traits at (the) subsequent season(s) by carry‐over effects. Wintering conditions are known to affect breeding success, but few studies have investigated carry‐over effects on survival. The Eurasian oystercatcher Haematopus ostralegus is a coastal wader with sedentary populations at temperate sites and migratory populations in northern breeding grounds of Europe. We pooled continental European ringing‐recovery datasets from 1975 to 2000 to estimate winter and summer survival rates of migrant and resident populations and to investigate long‐term effects of winter habitat changes. During mild climatic periods, adults of both migratory and resident populations exhibited survival rates 2% lower in summer than in winter. Severe winters reduced survival rates (down to 25% reduction) and were often followed by a decline in survival during the following summer, via short‐term carry‐over effects. Habitat changes in the Dutch wintering grounds caused a reduction in food stocks, leading to reduced survival rates, particularly in young birds. Therefore, wintering habitat changes resulted in long‐term (>10 years) 8.7 and 9.4% decrease in adult annual survival of migrant and resident populations respectively. Studying the impact of carry‐over effects is crucial for understanding the life history of migratory birds and the development of conservation measures.     

Photoperiodic response may facilitate adaptation to climatic change in long-distance migratory birds

Recent climatic change is causing spring events in northern temperate regions to occur earlier in the year. As a result, migratory birds returning from tropical wintering sites may arrive too late to take full advantage of the food resources on their breeding grounds. Under these conditions, selection will favour earlier spring arrival that could be achieved by overwintering closer to the breeding grounds. However, it is unknown how daylength conditions at higher latitudes will affect the timing of life cycle stages. Here, we show in three species of Palaearctic-African migratory songbirds that a shortening of migration distance induces an advancement of springtime activities. Birds exposed to daylengths simulating migration to and wintering in southern Europe considerably advanced their spring migratory activity and testicular development. This response to the novel photoperiodic environment will enable birds wintering further north to advance spring arrival and to start breeding earlier. Thus, phenotypic flexibility in response to the photoperiod may reinforce selection for shorter migration distance if spring temperatures continue to rise.     

Quantifying full phenological event distributions reveals simultaneous advances,temporal stability and delays in spring and autumn migration timing in long‐distance migratory birds

Phenological changes in key seasonally expressed life‐history traits occurring across periods of climatic and environmental change can cause temporal mismatches between interacting species, and thereby impact population and community dynamics. However, studies quantifying long‐term phenological changes have commonly only measured variation occurring in spring, measured as the first or mean dates on which focal traits or events were observed. Few studies have considered seasonally paired events spanning spring and autumn or tested the key assumption that single convenient metrics accurately capture entire event distributions. We used 60 years (1955–2014) of daily bird migration census data from Fair Isle, Scotland, to comprehensively quantify the degree to which the full distributions of spring and autumn migration timing of 13 species of long‐distance migratory bird changed across a period of substantial climatic and environmental change. In most species, mean spring and autumn migration dates changed little. However, the early migration phase (≤10th percentile date) commonly got earlier, while the late migration phase (≥90th percentile date) commonly got later. Consequently, species' total migration durations typically lengthened across years. Spring and autumn migration phenologies were not consistently correlated within or between years within species and hence were not tightly coupled. Furthermore, different metrics quantifying different aspects of migration phenology within seasons were not strongly cross‐correlated, meaning that no single metric adequately described the full pattern of phenological change. These analyses therefore reveal complex patterns of simultaneous advancement, temporal stability and delay in spring and autumn migration phenologies, altering species' life‐history structures. Additionally, they demonstrate that this complexity is only revealed if multiple metrics encompassing entire seasonal event distributions, rather than single metrics, are used to quantify phenological change. Existing evidence of long‐term phenological changes detected using only one or two metrics should consequently be interpreted cautiously because divergent changes occurring simultaneously could potentially have remained undetected.     

Phenology of two interdependent traits in migratory birds in response to climate change

In migratory birds, arrival date and hatching date are two key phenological markers that have responded to global warming. A body of knowledge exists relating these traits to evolutionary pressures. In this study, we formalize this knowledge into general mathematical assumptions, and use them in an ecoevolutionary model. In contrast to previous models, this study novelty accounts for both traits—arrival date and hatching date—and the interdependence between them, revealing when one, the other or both will respond to climate. For all models sharing the assumptions, the following phenological responses will occur. First, if the nestling-prey peak is late enough, hatching is synchronous with, and arrival date evolves independently of, prey phenology. Second, when resource availability constrains the length of the pre-laying period, hatching is adaptively asynchronous with prey phenology. Predictions for both traits compare well with empirical observations. In response to advancing prey phenology, arrival date may advance, remain unchanged, or even become delayed; the latter occurring when egg-laying resources are only available relatively late in the season. The model shows that asynchronous hatching and unresponsive arrival date are not sufficient evidence that phenological adaptation is constrained. The work provides a framework for exploring microevolution of interdependent phenological traits.     

Diffuse migratory connectivity in two species of shrubland birds: evidence from stable isotopes

Connecting seasonal ranges of migratory birds is important for understanding the annual template of stressors that influence their populations. Brewer’s sparrows (Spizella breweri) and sagebrush sparrows (Artemisiospiza nevadensis) share similar sagebrush (Artemisia spp.) habitats for breeding but have different population trends that might be related to winter location. To link breeding and winter ranges, we created isoscapes of deuterium [stable isotope ratio (δ) of deuterium; δ ²H] and nitrogen (δ ¹⁵N) for each species modeled from isotope ratios measured in feathers of 264 Brewer’s and 82 sagebrush sparrows and environmental characteristics at capture locations across their breeding range. We then used feather $\delta^{2} {\text{H}}_{\text{f}}$ and $\delta^{15} {\text{N}}_{\text{f}}$ measured in 1,029 Brewer’s and 527 sagebrush sparrows captured on winter locations in southwestern United States to assign probable breeding ranges. Intraspecies population mixing from across the breeding range was strong for both Brewer’s and sagebrush sparrows on winter ranges. Brewer’s sparrows but not sagebrush sparrows were linked to more northerly breeding locations in the eastern part of their winter range. Winter location was not related to breeding population trends estimated from US Geological Survey Breeding Bird Survey routes for either Brewer’s or sagebrush sparrows. Primary drivers of population dynamics are likely independent for each species; Brewer’s and sagebrush sparrows captured at the same winter location did not share predicted breeding locations or population trends. The diffuse migratory connectivity displayed by Brewer’s and sagebrush sparrows measured at the coarse spatial resolution in our analysis also suggests that local environments rather than broad regional characteristics are primary drivers of annual population trends.     

Regulation of protein breakdown and adrenocortical response to stress in birds during migratory flight

During long-term fasting at rest, protein utilization is maintained at low levels until it increases at a threshold adiposity. This study examines 1) whether such a shift in energy substrate use also occurs during endurance exercise while fasting, 2) the role of corticosterone, and 3) the adrenocortical response to an acute stressor. Ten species of migrating birds caught after an endurance flight over at least 500 km were examined. Plasma uric acid and corticosterone levels were low in birds with fat stores >5% of body mass and high in birds with smaller fat stores. Corticosterone levels were very high in birds with no visible fat stores and emaciated breast muscles. Corticosterone levels increased with handling time only in birds with large fat stores. These findings suggest that 1) migrating birds with appreciable fat stores are not stressed by endurance flight, 2) a metabolic shift (increased protein breakdown), regulated by an endocrine shift (medium corticosterone levels), occurs at a threshold adiposity, as observed in birds at rest, 3) adrenocortical response to an acute stressor is inhibited after this shift, and 4) an adrenocortical response typical for an emergency situation (high corticosterone levels) is only reached when muscle protein is dangerously low.     

Nonrandom filtering effect on birds: species and guilds response to urbanization

Using bird survey data taken in three cities in Southern Chile, we evaluated the hypothesis that changes in community composition from periurban to urban areas are not random. Furthermore, the consistency of species and guild loss was assessed across cities. A consistent pattern of difference in community and guild structure between urban and periurban habitats was found. In addition, a nonrandom loss of species was found in urban areas compared to periurban areas, and non‐native species dominated urban communities in all cities. The average abundance of omnivores, granivores, and habitat generalists was higher in urban areas, while insectivores and open habitat species were more abundant in periurban areas. These results strongly suggest that urban habitats act as filters offering suitable conditions for only a fraction of the bird species present in a given area, and the lack of suitable conditions may be facilitating local biotic homogenization in the three studied cities. The results of this study not only fill a biogeographical knowledge gap, but the work presented here also aids the general understanding of factors that affect community structure in habitats with varied levels of local and global urbanization.     

Where the wild birds go: explaining the differences in migratory destinations across terrestrial bird species

Given their large movement capacities, migratory birds have in principle a wide range of possible geographical locations for their breeding and non‐breeding destinations, yet each species migrates between consistent breeding and non‐breeding ranges. In this study, we use a macroecological approach to search for the general factors explaining the location of the seasonal ranges of migratory bird species across the globe. We develop a null model to test the hypotheses that access to resources, geographical distance, tracking of temperature, and habitat conditions (separately as well as considered together) have a major influence in the location of species’ migratory destinations, once each species’ geographical constraints are taken into account. Our results provide evidence for a trade‐off between costs associated with distance travelled and gains in terms of better access to resources. We also provide strong support to the hypotheses that all factors tested, with the exception of habitat, have a strong and additive effect on the global geography of bird migration. Indeed, our results indicate that species’ contemporary migratory destinations (i.e. the combination of their breeding and non‐breeding ranges) are such that they allow species to track a temperature regime throughout the year, to escape local competition and reach areas with better access to resources, and to minimise the spatial distance travelled, within the limitations imposed by the geographical location of each species. Our study thus sheds light on the mechanisms underpinning bird migration and provides a strong basis for predicting how migratory species will respond to future change.     

Trait hierarchies are stronger than trait dissimilarities in structuring spatial co‐occurrence patterns of common tree species in a subtropical forest

1. The dissimilarity and hierarchy of trait values that characterize niche and fitness differences, respectively, have been increasingly applied to infer mechanisms driving community assembly and to explain species co‐occurrence patterns. Here, we predict that limiting similarity should result in the spatial segregation of functionally similar species, while functionally similar species will be more likely to co‐occur either due to environmental filtering or due to competitive exclusion of inferior competitors (hereafter hierarchical competition).
2. We used a fully mapped 50‐ha subtropical forest plot in southern China to explore how pairwise spatial associations between saplings and between adult trees were influenced by trait dissimilarity and hierarchy in order to gain insight into assembly mechanisms. We assessed pairwise spatial associations using two summary statistics of spatial point patterns at different spatial scales and compared the effects of trait dissimilarity and trait hierarchy of different functional traits on the interspecific spatial associations. These comparisons allow us to disentangle the effects of limiting similarity, environmental filtering, and hierarchical competition on species co‐occurrence.
3. We found that trait dissimilarity was generally negatively related to interspecific spatial associations for both saplings and adult trees across spatial scales, meaning that species with similar trait values were more likely to co‐occur and thus supporting environmental filtering or hierarchical competition. We further found that trait hierarchy outweighed trait dissimilarity in structuring pairwise spatial associations, suggesting that hierarchical competition played a more important role in structuring our forest community than environmental filtering across life stages.
4. This study employed a novel method, by offering the integration of pairwise spatial association and trait dissimilarity as well as trait hierarchy, to disentangle the relative importance of multiple assembly mechanisms in structuring co‐occurrence patterns, especially the mechanisms of environmental filtering and hierarchical competition, which lead to indistinguishable co‐occurrence patterns. This study also reinforced the importance of trait hierarchy rather than trait dissimilarity in driving neighborhood competition.

     

Can long‐distance migratory birds adjust to the advancement of spring by shortening migration distance? The response of the pied flycatcher to latitudinal photoperiodic variation

Many organisms use day length as a cue for synchronizing their life cycles with seasonal changes in environmental productivity. Under rapid climate change, however, responses to day length may become maladaptive, and photo‐responsive organisms may only be able to evade increasingly unsuitable habitats if they can accommodate to a wide range of photoperiodic conditions. A previous experiment showed that the pied flycatcher, Ficedula hypoleuca, a Palaearctic‐Afrotropical migratory bird, would strongly advance the timing of spring migration and reproductive maturation if it shifted its wintering area from sub‐Saharan Africa to the Mediterranean region. However, it is unknown whether this marked response to latitudinal variation in photoperiodic conditions is continuous over the entire range of potential wintering areas, and if a shortening of migration distance would be an effective mechanism to adjust the timing of migration to rapidly changing climatic conditions. Here, we experimentally show that a moderate northward displacement of the pied flycatcher's current wintering grounds by 10° would result in a clear advancement of the termination of prenuptial moult and the initiation of spring migratory activity and gonadal growth. However, we found no further advancement under conditions simulating higher wintering latitudes, suggesting the existence of a critical photoperiodic threshold or a steep gradual response within a narrow geographical range between 10° and 20° northern latitude. Because habitat conditions in this area are deteriorating rapidly, the potential for pied flycatchers to adjust their life cycle to changing climatic conditions by shortening the migration distance may be limited in the future.     

Geographic origin and past climatic experience influence the response to late spring frost in four common grass species in central Europe

Late spring frost events can affect vegetation. The response of grassland species, however, is generally unknown. We explore the late‐frost sensitivity of four common European grass species and investigate whether these species exhibit local adaptations to late frost on a continental scale and whether past climatic experience influences late frost sensitivity. Ecotypes of Arrhenatherum elatius, Alopecurus pratensis, Festuca pratensis, and Holcus lanatus from Spain, Italy, Bulgaria, Hungary, Sweden and Germany were exposed to late frost after drought and warming manipulations in the preceding growing season in a common garden experiment. Late frost reduced the productivity of the grasses on average by 20%. Ecotypes differed in their late‐frost sensitivity in three of the four species and local adaptations to late frost were identified. Previous exposure to drought and warming caused differences in late‐frost sensitivity in some cases. The impact of late frost events may increase in a warmer world due to an earlier onset of growing and no change in timing of late frost events. The history of climatic exposure can alter the performance of plants, possibly through epigenetic mechanisms. Based on the complex response pattern observed, a maximization of genetic diversity is proposed as a promising adaptation strategy against climate change.     

Using citizen science monitoring data in species distribution models to inform isotopic assignment of migratory connectivity in wetland birds

Stable isotopes have been used to estimate migratory connectivity in many species. Estimates are often greatly improved when coupled with species distribution models (SDMs), which temper estimates in relation to occurrence. SDMs can be constructed using point locality data from a variety of sources including extensive monitoring data typically collected by citizen scientists. However, one potential issue with SDM is that these data often have sampling bias. To avoid this potential bias, we created SDMs based on marsh bird monitoring program data collected by citizen scientists and other participants following protocols specifically designed to maximize detections of species of interest at locations representative of larger areas of inference. We then used the SDMs to refine isotopic assignments of breeding areas of autumn‐migrating and wintering sora Porzana carolina, Virginia rail Rallus limicola, and yellow rail Coturnicops noveboracensis based on feathers collected from individuals caught at various locations in the United States from Minnesota south to Louisiana and South Carolina. Sora were assigned to an area that included much of the western U.S. and prairie Canada, covering parts of the Pacific, Central, and Mississippi waterfowl Flyways. Yellow rails were assigned to a broad area along Hudson and James Bay in northern Manitoba and Ontario, as well as smaller parts of Québec, Minnesota, Wisconsin, and Michigan, including parts of the Mississippi and Atlantic Flyways. Virginia rails were from several discrete areas, including parts of Colorado, New Mexico, the central valley of California, and southern Saskatchewan and Manitoba in the Pacific and Central Flyways. Our study demonstrates extensive data from organized citizen science monitoring programs are especially useful for improving isotopic assignments of migratory connectivity in birds, which can ultimately lead to better informed management decisions and conservation actions.     

Floodplain ants show a stronger response to an extensive flood than to variations in fallen‐timber load

Understanding how species respond to differences in resource availability is critical to managing biodiversity under the increasing pressures associated with climate change and growing human populations. Over the last century, the floodplain forests of Australia's largest river system, the Murray‐Darling Basin, have been much affected by intensive harvesting of timber and firewood, and increasingly stressed by river regulation and, recently, an extended drought. Fallen timber – logs and shed branches – is known to play a key role in the ecology of several important species on these floodplains. Here, we monitored the response of the ant assemblages of a floodplain forest along the Murray River to a large‐scale (34 ha) experimental manipulation of fallen‐timber load (0 to 80 t ha^?1) over 4 years. The forest was subjected to an incidental, extensive flood that enabled us to examine how two important stressors (timber removal and river regulation) affect ant assemblages. Ants showed little response to the proximity of fallen timber within plots, prior to the flood, or to different loads among plots, unlike other floodplain biota. After the flood, both ant abundance and species richness increased and species composition changed. However, this increase in species richness after flooding was less pronounced in plots with higher amounts of fallen timber. Managing river red gum forest using a mosaic of flood regimes, more representative of historical conditions, is likely to be the most effective way to maintain and enhance the diversity of ants and other biota on these important floodplains.