Individual repeatability of avian migration phenology: A systematic review and meta-analysis.

Changes in phenology and distribution are being widely reported for many migratory species in response to shifting environmental conditions. Understanding these changes and the situations in which they occur can be aided by understanding consistent individual differences in phenology and distribution and the situations in which consistency varies in strength or detectability. Studies tracking the same individuals over consecutive years are increasingly reporting migratory timings to be a repeatable trait, suggesting that flexible individual responses to environmental conditions may contribute little to population-level changes in phenology and distribution. However, how this varies across species and sexes, across the annual cycle and in relation to study (tracking method, study design) and/or ecosystem characteristics is not yet clear. Here, we take advantage of the growing number of publications in movement ecology to perform a phylogenetic multilevel meta-analysis of repeatability estimates for avian migratory timings to investigate these questions. Of 2,433 reviewed studies, 54 contained suitable information for meta-analysis, resulting in 177 effect sizes from 47 species. Individual repeatability of avian migratory timings averaged 0.414 (95% confidence interval: 0.3-0.5) across landbirds, waterbirds and seabirds, suggesting consistent individual differences in migratory timings is a common feature of migratory systems. Timing of departure from the non-breeding grounds was more repeatable than timings of arrival at or departure from breeding grounds, suggesting that conditions encountered on migratory journeys and outcome of breeding attempts can influence individual variation. Population-level shifts in phenology could arise through individual timings changing with environmental conditions and/or through shifts in the numbers of individuals with different timings. Our findings suggest that, in addition to identifying the conditions associated with individual variation in phenology, exploring the causes of between-individual variation will be key in predicting future rates and directions of changes in migratory timings. We therefore encourage researchers to report the within- and between- individual variance components underpinning the reported repeatability estimates to aid interpretation of migration behaviour. In addition, the lack of studies in the tropics means that levels of repeatability in less strongly seasonal environments are not yet clear.

Isolation and characterization of 50 microsatellite loci for two shearwater species, Ardenna pacifica and Puffinus bailloni.

BACKGROUND: Shearwaters (order Procellariiformes) are an excellent study system to investigate the genetic consequences of the co-called "seabird paradox", as they are able to disperse long distances but many species exhibit natal and breeding philopatry. However, few microsatellite markers are currently available for these taxa, hampering genetic inferences. METHODS AND RESULTS: In this study, 25 novel microsatellite loci were isolated and characterized for each of two distantly related shearwater species: the wedge-tailed shearwater (Ardenna pacifica) and the tropical shearwater (Puffinus bailloni). Polymorphism tests were performed for a total of 91 A. pacifica individuals sampled at Reunion and Round Island, and 48 P. bailloni individuals from Reunion and Europa Island, in the western Indian Ocean. The analyses revealed 23 polymorphic loci for A. pacifica, with the number of alleles per locus (Na) ranging from 2 to 8 (mean = 3.957 ± 0.364). Nineteen polymorphic loci were found for P. bailloni, with Na varying from two to five (mean = 3.053 ± 0.247). The observed heterozygosity (Ho) was relatively low for the two species, with Ho ranging from 0.022 to 0.725 (mean = 0.326 ± 0.044) for A. pacifica and from 0.021 to 0.688 (mean = 0.271 ± 0.051) for P. bailloni, but comparable to the estimates available for other Puffinus species. CONCLUSIONS: The new microsatellite loci provide a valuable tool for further population genetic studies, and will allow for design of effective conservation and management plans for A. pacifica, P. bailloni and other closely-related species.

Widespread gene flow between oceans in a pelagic seabird species complex.

Global-scale gene flow is an important concern in conservation biology as it has the potential to either increase or decrease genetic diversity in species and populations. Although many studies focus on the gene flow between different populations of a single species, the potential for gene flow and introgression between species is understudied, particularly in seabirds. The only well-studied example of a mixed-species, hybridizing population of petrels exists on Round Island, in the Indian Ocean. Previous research assumed that Round Island represents a point of secondary contact between Atlantic (Pterodroma arminjoniana) and Pacific species (Pterodroma neglecta and Pterodroma heraldica). This study uses microsatellite genotyping and tracking data to address the possibility of between-species hybridization occurring outside the Indian Ocean. Dispersal and gene flow spanning three oceans were demonstrated between the species in this complex. Analysis of migration rates estimated using bayesass revealed unidirectional movement of petrels from the Atlantic and Pacific into the Indian Ocean. Conversely, structure analysis revealed gene flow between species of the Atlantic and Pacific oceans, with potential three-way hybrids occurring outside the Indian Ocean. Additionally, geolocation tracking of Round Island petrels revealed two individuals travelling to the Atlantic and Pacific. These results suggest that interspecific hybrids in Pterodroma petrels are more common than was previously assumed. This study is the first of its kind to investigate gene flow between populations of closely related Procellariiform species on a global scale, demonstrating the need for consideration of widespread migration and hybridization in the conservation of threatened seabirds.

Contrasting effects of tropical cyclones on the annual survival of a pelagic seabird in the Indian Ocean.

Tropical cyclones are renowned for their destructive nature and are an important feature of marine and coastal tropical ecosystems. Over the last 40 years, their intensity, frequency and tracks have changed, partly in response to ocean warming, and future predictions indicate that these trends are likely to continue with potential consequences for human populations and coastal ecosystems. However, our understanding of how tropical cyclones currently affect marine biodiversity, and pelagic species in particular, is limited. For seabirds, the impacts of cyclones are known to be detrimental at breeding colonies, but impacts on the annual survival of pelagic adults and juveniles remain largely unexplored and no study has simultaneously explored the direct impacts of cyclones on different life-history stages across the annual life cycle. We used a 20-year data set on tropical cyclones in the Indian Ocean, tracking data from 122 Round Island petrels and long-term capture-mark-recapture data to explore the impacts of tropical cyclones on the survival of adult and juvenile (first year) petrels during both the breeding and migration periods. The tracking data showed that juvenile and adult Round Island petrels utilize the three cyclone regions of the Indian Ocean and were potentially exposed to cyclones for a substantial part of their annual cycle. However, only juvenile petrel survival was affected by cyclone activity; negatively by a strong cyclone in the vicinity of the breeding colony and positively by increasing cyclone activity in the Northern Indian Ocean where they spend the majority of their first year at sea. These contrasting effects raise the intriguing prospect that the projected changes in cyclones under current climate change scenarios may have positive as well as the more commonly perceived negative impacts on marine biodiversity.

Past volcanic activity predisposes an endemic threatened seabird to negative anthropogenic impacts.

Humans are regularly cited as the main driver of current biodiversity extinction, but the impact of historic volcanic activity is often overlooked. Pre-human evidence of wildlife abundance and diversity are essential for disentangling anthropogenic impacts from natural events. Réunion Island, with its intense and well-documented volcanic activity, endemic biodiversity, long history of isolation and recent human colonization, provides an opportunity to disentangle these processes. We track past demographic changes of a critically endangered seabird, the Mascarene petrel Pseudobulweria aterrima, using genome-wide SNPs. Coalescent modeling suggested that a large ancestral population underwent a substantial population decline in two distinct phases, ca. 125,000 and 37,000 years ago, coinciding with periods of major eruptions of Piton des Neiges. Subsequently, the ancestral population was fragmented into the two known colonies, ca. 1500 years ago, following eruptions of Piton de la Fournaise. In the last century, both colonies declined significantly due to anthropogenic activities, and although the species was initially considered extinct, it was rediscovered in the 1970s. Our findings suggest that the current conservation status of wildlife on volcanic islands should be firstly assessed as a legacy of historic volcanic activity, and thereafter by the increasing anthropogenic impacts, which may ultimately drive species towards extinction.

How life history influences population dynamics in fluctuating environments.

A major question in ecology is how age-specific variation in demographic parameters influences population dynamics. Based on long-term studies of growing populations of birds and mammals, we analyze population dynamics by using fluctuations in the total reproductive value of the population. This enables us to account for random fluctuations in age distribution. The influence of demographic and environmental stochasticity on the population dynamics of a species decreased with generation time. Variation in age-specific contributions to total reproductive value and to stochastic components of population dynamics was correlated with the position of the species along the slow-fast continuum of life-history variation. Younger age classes relative to the generation time accounted for larger contributions to the total reproductive value and to demographic stochasticity in "slow" than in "fast" species, in which many age classes contributed more equally. In contrast, fluctuations in population growth rate attributable to stochastic environmental variation involved a larger proportion of all age classes independent of life history. Thus, changes in population growth rates can be surprisingly well explained by basic species-specific life-history characteristics.

Tracking seabird migration in the tropical Indian Ocean reveals basin-scale conservation need.

Understanding marine predator distributions is an essential component of arresting their catastrophic declines.1,2,3,4 In temperate, polar, and upwelling seas, predictable oceanographic features can aggregate migratory predators, which benefit from site-based protection.5,6,7,8 In more oligotrophic tropical waters, however, it is unclear whether environmental conditions create similar multi-species hotspots. We track the non-breeding movements and habitat preferences of a tropical seabird assemblage (n = 348 individuals, 9 species, and 10 colonies in the western Indian Ocean), which supports globally important biodiversity.9,10,11,12 We mapped species richness from tracked populations and then predicted the same diversity measure for all known Indian Ocean colonies. Most species had large non-breeding ranges, low or variable residency patterns, and specific habitat preferences. This in turn revealed that maximum species richness covered >3.9 million km2, with no focused aggregations, in stark contrast to large-scale tracking studies in all other ocean basins.5,6,7,13,14 High species richness was captured by existing marine protected areas (MPAs) in the region; however, most occurred in the unprotected high seas beyond national jurisdictions. Seabirds experience cumulative anthropogenic impacts13 and high mortality15,16 during non-breeding. Therefore, our results suggest that seabird conservation in the tropical Indian Ocean requires an ocean-wide perspective, including high seas legislation.17 As restoration actions improve the outlook for tropical seabirds on land18,19,20,21,22 and environmental change reshapes the habitats that support them at sea,15,16 appropriate marine conservation will be crucial for their long-term recovery and whole ecosystem restoration.

Individual consistency in migration strategies of a tropical seabird, the Round Island petrel.

BACKGROUND: In migratory species, the extent of within- and between-individual variation in migratory strategies can influence potential rates and directions of responses to environmental changes. Quantifying this variation requires tracking of many individuals on repeated migratory journeys. At temperate and higher latitudes, low levels of within-individual variation in migratory behaviours are common and may reflect repeated use of predictable resources in these seasonally-structured environments. However, variation in migratory behaviours in the tropics, where seasonal predictability of food resources can be weaker, remains largely unknown. METHODS: Round Island petrels (Pterodroma sp.) are tropical, pelagic seabirds that breed all year round and perform long-distance migrations. Using multi-year geolocator tracking data from 62 individuals between 2009 and 2018, we quantify levels of within- and between-individual variation in non-breeding distributions and timings. RESULTS: We found striking levels of between-individual variation in at-sea movements and timings, with non-breeding migrations to different areas occurring across much of the Indian Ocean and throughout the whole year. Despite this, repeat-tracking of individual petrels revealed remarkably high levels of spatial and temporal consistency in within-individual migratory behaviour, particularly for petrels that departed at similar times in different years and for those departing in the austral summer. However, while the same areas were used by individuals in different years, they were not necessarily used at the same times during the non-breeding period. CONCLUSIONS: Even in tropical systems with huge ranges of migratory routes and timings, our results suggest benefits of consistency in individual migratory behaviours. Identifying the factors that drive and maintain between-individual variation in migratory behaviour, and the consequences for breeding success and survival, will be key to understanding the consequences of environmental change across migratory ranges.

Climate change and the risks associated with delayed breeding in a tropical wild bird population.

There is growing evidence of changes in the timing of important ecological events, such as flowering in plants and reproduction in animals, in response to climate change, with implications for population decline and biodiversity loss. Recent work has shown that the timing of breeding in wild birds is changing in response to climate change partly because individuals are remarkably flexible in their timing of breeding. Despite this work, our understanding of these processes in wild populations remains very limited and biased towards species from temperate regions. Here, we report the response to changing climate in a tropical wild bird population using a long-term dataset on a formerly critically endangered island endemic, the Mauritius kestrel. We show that the frequency of spring rainfall affects the timing of breeding, with birds breeding later in wetter springs. Delays in breeding have consequences in terms of reduced reproductive success as birds get exposed to risks associated with adverse climatic conditions later on in the breeding season, which reduce nesting success. These results, combined with the fact that frequency of spring rainfall has increased by about 60 per cent in our study area since 1962, imply that climate change is exposing birds to the stochastic risks of late reproduction by causing them to start breeding relatively late in the season.

Multiple environmental gradients affect spatial variation in the productivity of a tropical bird population.

1. Spatial variation in habitat quality and its demographic consequences have important implications for the regulation of animal populations. Theoretically, habitat quality is typically viewed as a single gradient from 'poor' to 'good', but in wild populations it is possible that there are multiple environmental gradients that determine spatial variation in demography. 2. Understanding environmental gradients is important to gain mechanistic insights into important population processes, but also to understand how populations might respond to environmental change. Here, we explore habitat and elevation gradients and their implications for population persistence using detailed long-term data on 600 individuals of the Mauritius kestrel. These data allow us to statistically separate spatial variation in demography from variation arising out of individual or environmental quality and explore its relationships with habitat and topography. 3. Birds that breed earlier in the season have higher reproductive success, and we found that the timing of breeding varies significantly between territories. This variation is primarily driven by elevation, with birds breeding progressively later as elevation increases. 4. Pre-fledging survival from the egg to fledgling stage (independently of timing), and recruitment, also varied significantly between territories. This variation is driven by the habitat surrounding breeding sites with increasing agricultural encroachment causing survival and recruitment to decline. 5. Taken together, our results suggest that there are likely to be multiple environmental gradients affecting spatial variation in productivity in wild populations, and hence multiple and different routes through which environmental change might have consequences for population dynamics by modifying spatial processes.

The impact of habitat quality inside protected areas on distribution of the Dominican Republic's last endemic non-volant land mammals.

The Hispaniolan solenodon, Solenodon paradoxus, and Hispaniolan hutia, Plagiodontia aedium, are the Dominican Republic's only surviving endemic non-volant land mammals, and are high priorities for conservation. The country has an extensive protected area (PA) network designed to maintain habitats and benefit biodiversity, but which faces significant anthropogenic threats likely to detrimentally impact both species. We examined how differences in habitats, forest structure, topography, and human activity influence presence of solenodons and hutias across the Dominican Republic. Systematic surveys of seven PAs were undertaken to record indirect signs, with presence-absence data analyzed using a multi-model inference approach incorporating ecological variables from both field and GIS data. Solenodons were detected relatively frequently, whereas detections of hutias were uncommon. Lower elevations, increased surrounding tree cover, canopy closure, and reduced levels of low vegetation are all associated with increased probability of detecting solenodons, whereas agriculture and mangrove represent poor-quality habitat. Increased canopy closure, tree basal area (indicating older-growth forest), and increased rock substrate (providing more den sites) are associated with increased probability of detecting hutias. Our findings indicated that human activities within PAs are likely to negatively affect both species, and conservation activities should focus on preventing encroachment and conversion of forest to agriculture to maintain high-quality forest habitats. El solenodonte de la Hispaniola, Solenodon paradoxus, y la hutia de la Hispaniola, Plagiodontia aedium, son los únicos mamíferos endémicos terrestres no voladores que sobreviven en la República Dominicana, su conservación es de alta prioridad. El país tiene una extensa red de áreas protegidas (AP) diseñada para mantener hábitats y beneficiar la biodiversidad, pero se enfrenta a amenazas antropogénicas. Sin embargo, no existen datos cuantitativos para evaluar las presiones antropogénicas que amenazan a los solenodontes y las hutias. Examinamos cómo las diferencias en los hábitats, la estructura del bosque, la topografía y la actividad humana influyen la presencia de solenodontes y hutias en toda la República Dominicana. Se realizaron encuestas sistemáticas de siete AP para registrar los signos indirectos de ambas especies, los datos de presencia/ausencia fueron analizados mediante inferencia multimodelo que incorpora variables ecológicas de los datos de campo y Sistema de Información Geográfica. Los Solenodontes se detectaron relativamente frecuentemente, mientras que las detecciones de hutias fueron menos comunes. Las elevaciones más bajas, el aumento de la cubierta arbórea circundante, el cierre del dosel y los niveles reducidos de vegetación baja se asocian con una mayor probabilidad de detectar solenodones. Mientras que la agricultura y los manglares representan un hábitat de mala calidad para el solenodonte. Aumento del cierre del dosel, área basal del árbol (que indica un bosque más antiguo) y un sustrato con mayor proporcion de roca (que proporciona más sitios para madrigueras) se asocian con una mayor probabilidad de detectar hutias. Nuestros hallazgos indican que las actividades humanas dentro de las AP pueden afectar negativamente a ambas especies. Las actividades de conservación deberían enfocarse en mantener hábitats forestales de alta calidad por medio de prevenir la invasión y la conversión de los bosques a agricultura.

Senescence rates are determined by ranking on the fast-slow life-history continuum.

Comparative analyses of survival senescence by using life tables have identified generalizations including the observation that mammals senesce faster than similar-sized birds. These generalizations have been challenged because of limitations of life-table approaches and the growing appreciation that senescence is more than an increasing probability of death. Without using life tables, we examine senescence rates in annual individual fitness using 20 individual-based data sets of terrestrial vertebrates with contrasting life histories and body size. We find that senescence is widespread in the wild and equally likely to occur in survival and reproduction. Additionally, mammals senesce faster than birds because they have a faster life history for a given body size. By allowing us to disentangle the effects of two major fitness components our methods allow an assessment of the robustness of the prevalent life-table approach. Focusing on one aspect of life history - survival or recruitment - can provide reliable information on overall senescence.

Restricted dispersal reduces the strength of spatial density dependence in a tropical bird population.

Spatial processes could play an important role in density-dependent population regulation because the disproportionate use of poor quality habitats as population size increases is widespread in animal populations-the so-called buffer effect. While the buffer effect patterns and their demographic consequences have been described in a number of wild populations, much less is known about how dispersal affects distribution patterns and ultimately density dependence. Here, we investigated the role of dispersal in spatial density dependence using an extraordinarily detailed dataset from a reintroduced Mauritius kestrel (Falco punctatus) population with a territorial (despotic) breeding system. We show that recruitment rates varied significantly between territories, and that territory occupancy was related to its recruitment rate, both of which are consistent with the buffer effect theory. However, we also show that restricted dispersal affects the patterns of territory occupancy with the territories close to release sites being occupied sooner and for longer as the population has grown than the territories further away. As a result of these dispersal patterns, the strength of spatial density dependence is significantly reduced. We conclude that restricted dispersal can modify spatial density dependence in the wild, which has implications for the way population dynamics are likely to be impacted by environmental change.

Inbreeding and loss of genetic variation in a reintroduced population of Mauritius Kestrel.

Many populations have recovered from severe bottlenecks either naturally or through intensive conservation management. In the past, however, few conservation programs have monitored the genetic health of recovering populations. We conducted a conservation genetic assessment of a small, reintroduced population of Mauritius Kestrel (Falco punctatus) to determine whether genetic deterioration has occurred since its reintroduction. We used pedigree analysis that partially accounted for individuals of unknown origin to document that (1) inbreeding occurred frequently (2.6% increase per generation; N(eI)= 18.9), (2) 25% of breeding pairs were composed of either closely or moderately related individuals, (3) genetic diversity has been lost from the population (1.6% loss per generation; N(eV)= 32.1) less rapidly than the corresponding increase in inbreeding, and (4) ignoring the contribution of unknown individuals to a pedigree will bias the metrics derived from that pedigree, ultimately obscuring the prevailing genetic dynamics. The rates of inbreeding and loss of genetic variation in the subpopulation of Mauritius Kestrel we examined were extreme and among the highest yet documented in a wild vertebrate population. Thus, genetic deterioration may affect this population's long-term viability. Remedial conservation strategies are needed to reduce the impact of inbreeding and loss of genetic variation in this species. We suggest that schemes to monitor genetic variation after reintroduction should be an integral component of endangered species recovery programs.

Agriculture modifies the seasonal decline of breeding success in a tropical wild bird population.

Habitat conversion for agriculture is a major driver of biodiversity loss, but our understanding of the demographic processes involved remains poor. We typically investigate the impacts of agriculture in isolation even though populations are likely to experience multiple, concurrent changes in the environment (e.g. land and climate change). Drivers of environmental change may interact to affect demography, but the mechanisms have yet to be explored fully in wild populations.Here, we investigate the mechanisms linking agricultural land use with breeding success using long-term data for the formerly Critically Endangered Mauritius kestrel Falco punctatus, a tropical forest specialist that also occupies agricultural habitats. We specifically focused on the relationship between breeding success, agriculture and the timing of breeding because the latter is sensitive to changes in climatic conditions (spring rainfall) and enables us to explore the interactive effects of different (land and climate) drivers of environmental change.Breeding success, measured as egg survival to fledging, declines seasonally in this population, but we found that the rate of this decline became increasingly rapid as the area of agriculture around a nest site increased. If the relationship between breeding success and agriculture was used in isolation to estimate the demographic impact of agriculture, it would significantly under-estimate breeding success in dry (early) springs and over-estimate breeding success in wet (late) springs.Analysis of prey delivered to nests suggests that the relationship between breeding success and agriculture might be due, in part, to spatial variation in the availability of native, arboreal geckos.Synthesis and applications. Agriculture modifies the seasonal decline in breeding success in this population. As springs are becoming wetter in our study area and since the kestrels breed later in wetter springs, the impact of agriculture on breeding success will become worse over time. Our results suggest that forest restoration designed to reduce the detrimental impacts of agriculture on breeding may also help reduce the detrimental effects of breeding late due to wetter springs. Our results therefore highlight the importance of considering the interactive effects of environmental change when managing wild populations.

Anthropogenic natal environmental effects on life histories in a wild bird population.

Recent work suggests that the environment experienced in early life can alter life histories in wild populations, but our understanding of the processes involved remains limited. Since anthropogenic environmental change is currently having a major impact on wild populations, this raises the possibility that life histories may be influenced by human activities that alter environmental conditions in early life. Whether this is the case and the processes involved remain unexplored in wild populations. Using 23 years of longitudinal data on the Mauritius kestrel (Falco punctatus), a tropical forest specialist, we found that females born in territories affected by anthropogenic habitat change shifted investment in reproduction to earlier in life at the expense of late life performance. They also had lower survival rates as young adults. This shift in life history strategy appears to be adaptive, because fitness was comparable to that of other females experiencing less anthropogenic modification in their natal environment. Our results suggest that human activities can leave a legacy on wild birds through natal environmental effects. Whether these legacies have a detrimental effect on populations will depend on life history responses and the extent to which these reduce individual fitness.