Annual Schedule Adjustment by a Long-Distance Migratory Bird.

AbstractMatching the timing of annual cycle events with the required resources can have crucial consequences for individual fitness. But as the annual cycle is composed of sequential events, a delay at any point may be carried over to the subsequent stage (or more, in a domino effect) and negatively influence individual performance. To investigate how migratory animals navigate their annual schedule and where and when it may be adjusted, we used full annual cycle data on 38 Icelandic whimbrels (Numenius phaeopus islandicus) tracked over 7 years-a subspecies that typically performs long-distance migrations to West Africa. We found that individuals apparently used the wintering sites to compensate for delays that mostly arose as a result of previous successful breeding, and a domino effect was observed from spring departure to laying date, with the potential to affect breeding output. However, the total time saved during all stationary periods is apparently enough to avoid interannual effects between breeding seasons. These findings highlight the importance of preserving good-quality nonbreeding sites in which individuals may adjust annual schedules and avoid potentially adverse effects of arriving late at the breeding grounds.

Effects of pair migratory behavior on breeding phenology and success in a partially migratory shorebird population.

In migratory systems, variation in individual phenology can arise through differences in individual migratory behaviors, and this may be particularly apparent in partial migrant systems, where migrant and resident individuals are present within the same population. Links between breeding phenology and migratory behavior or success are generally investigated at the individual level. However, for breeding phenology in particular, the migratory behaviors of each member of the pair may need to be considered simultaneously, as breeding phenology will likely be constrained by timing of the pair member that arrives last, and carryover effects on breeding success may vary depending on whether pair members share the same migratory behavior or not. We used tracking of marked individuals and monitoring of breeding success from a partially migrant population of Eurasian oystercatchers (Haematopus ostralegus) breeding in Iceland to test whether (a) breeding phenology varied with pair migratory behavior; (b) within-pair consistency in timing of laying differed among pair migratory behaviors; and (c) reproductive performance varied with pair migratory behavior, timing of laying, and year. We found that annual variation in timing of laying differed among pair migratory behaviors, with resident pairs being more consistent than migrant and mixed pairs, and migrant/mixed pairs breeding earlier than residents in most years but later in one (unusually cold) year. Pairs that laid early were more likely to replace their clutch after nest loss, had higher productivity and higher fledging success, independent of pair migratory behavior. Our study suggests that the links between individual migratory behavior and reproductive success can vary over time and, to a much lesser extent, with mate migratory behavior and can be mediated by differences in laying dates. Understanding these cascading effects of pair phenology on breeding success is likely to be key to predicting the impact of changing environmental conditions on migratory species.

Why do earlier-arriving migratory birds have better breeding success?

In migratory birds, early arrival on breeding sites is typically associated with greater breeding success, but the mechanisms driving these benefits are rarely known. One mechanism through which greater breeding success among early arrivers can potentially be achieved is the increased time available for replacement clutches following nest loss. However, the contribution of replacement clutches to breeding success will depend on seasonal variation in nest survival rates, and the consequences for juvenile recruitment of hatching at different times in the season. In particular, lower recruitment rates of late-hatched chicks could offset the benefits to early arrivers of being able to lay replacement clutches, which would reduce the likelihood of replacement clutch opportunities influencing selection on migratory timings. Using a simulation model of time-constrained capacity for replacement clutches, paramaterized with empirically-derived estimates from avian migratory systems, we show that greater reproductive success among early-arriving individuals can arise solely through the greater time capacity for replacement clutches among early arrivers, even when later renesting attempts contribute fewer recruits to the population. However, these relationships vary depending on the seasonal pattern of nest survival. The benefits of early arrival are greatest when nest survival rates are constant or decline seasonally, and early arrival is least beneficial when nest success rates increase over the breeding season, although replacement clutches can mitigate this effect. The time benefits of early arrival facilitating replacement clutches following nest loss may therefore be an important but overlooked source of selection on migratory timings. Empirical measures of seasonal variation in nest survival, renesting, and juvenile recruitment rates are therefore needed in order to identify the costs and benefits associated with individual migration phenology, the selection pressures influencing migratory timings, and the implications for ongoing shifts in migration and breeding phenology.

Mechanisms driving phenological and range change in migratory species.

Many migratory systems are changing rapidly in space and time, and these changes present challenges for conservation. Changes in local abundance and site occupancy across species' ranges have raised concerns over the efficacy of the existing protected area networks, while changes in phenology can potentially create mismatches in the timing of annual events with the availability of key resources. These changes could arise either through individuals shifting in space and time or through generational shifts in the frequency of individuals using different locations or on differing migratory schedules. Using a long-term study of a migratory shorebird in which individuals have been tracked through a period of range expansion and phenological change, we show that these changes occur through generational shifts in spatial and phenological distributions, and that individuals are highly consistent in space and time. Predictions of future rates of changes in range size and phenology, and their implications for species conservation, will require an understanding of the processes that can drive generational shifts. We therefore explore the developmental, demographic and environmental processes that could influence generational shifts in phenology and distribution, and the studies that will be needed to distinguish among these mechanisms of change. This article is part of the theme issue 'Linking behaviour to dynamics of populations and communities: application of novel approaches in behavioural ecology to conservation'.

Linking warming effects on phenology, demography, and range expansion in a migratory bird population.

Phenological changes in response to climate change have been recorded in many taxa, but the population-level consequences of these changes are largely unknown. If phenological change influences demography, it may underpin the changes in range size and distribution that have been associated with climate change in many species. Over the last century, Icelandic black-tailed godwits (Limosa limosa islandica) have increased 10-fold in numbers, and their breeding range has expanded throughout lowland Iceland, but the environmental and demographic drivers of this expansion remain unknown. Here, we explore the potential for climate-driven shifts in phenology to influence demography and range expansion. In warmer springs, Icelandic black-tailed godwits lay their clutches earlier, resulting in advances in hatching dates in those years. Early hatching is beneficial as population-wide tracking of marked individuals shows that chick recruitment to the adult population is greater for early hatched individuals. Throughout the last century, this population has expanded into progressively colder breeding areas in which hatch dates are later, but temperatures have increased throughout Iceland since the 1960s. Using these established relationships between temperature, hatching dates and recruitment, we show that these warming trends have the potential to have fueled substantial increases in recruitment throughout Iceland, and thus to have contributed to local population growth and expansion across the breeding range. The demographic consequences of temperature-mediated phenological changes, such as the advances in lay dates and increased recruitment associated with early hatching reported here, may therefore be key processes in driving population size and range changes in response to climate change.

Very rapid long-distance sea crossing by a migratory bird.

Landbirds undertaking within-continent migrations have the possibility to stop en route, but most long-distance migrants must also undertake large non-stop sea crossings, the length of which can vary greatly. For shorebirds migrating from Iceland to West Africa, the shortest route would involve one of the longest continuous sea crossings while alternative, mostly overland, routes are available. Using geolocators to track the migration of Icelandic whimbrels (Numenius phaeopus), we show that they can complete a round-trip of 11,000 km making two non-stop sea crossings and flying at speeds of up to 24 m s(−1); one of the fastest recorded for shorebirds flying over the ocean. Although wind support could reduce flight energetic costs, whimbrels faced headwinds up to twice their ground speed, indicating that unfavourable and potentially fatal weather conditions are not uncommon. Such apparently high risk migrations might be more common than previously thought, with potential fitness gains outweighing the costs.

The Effects of Habitat Type and Volcanic Eruptions on the Breeding Demography of Icelandic Whimbrels Numenius phaeopus.

Distinct preference of species for habitats is most often driven by long term differences in demographic rates between habitats. Estimating variation in those rates is key for developing successful conservation strategies. Stochastic events can interact with underlying variation in habitat quality in regulating demography but the opportunities to explore such interactions are rare. Whimbrels in Iceland show a strong preference for sparsely vegetated riverplains. Such habitats in Iceland face various threats, e.g., climate change, river regulation and spread of alien plant species. In this study we compared demographic parameters of breeding Whimbrels between riverplains and other habitats before, during and after volcanic eruption events to estimate the importance of the habitats for the species and the effect of ash deposit on breeding success. We found that an estimated minimum of 23% of the Icelandic population of Whimbrels and c. 10% of the world population of the species breed in riverplain habitats in Iceland. Whimbrels bred consistently at much higher densities in riverplain habitats than in other habitats and riverplains also had higher densities of pairs with fledglings although the proportion of successful breeders was similar between habitats. Predation by livestock may have had a considerable negative effect on breeding success on our study sites. Breeding was negatively affected by the volcanic activity, probably through the effects of ash on the invertebrate food supply, with breeding success being gradually worse closer to the eruption. Breeding success was equally affected by volcanism across habitats which differed in underlying habitat quality. This study gives an example of how populations can be regulated by factors which operate at different spatial scales, such as local variation in habitat quality and stochastic events which impact larger areas.

Why is timing of bird migration advancing when individuals are not?

Recent advances in spring arrival dates have been reported in many migratory species but the mechanism driving these advances is unknown. As population declines are most widely reported in species that are not advancing migration, there is an urgent need to identify the mechanisms facilitating and constraining these advances. Individual plasticity in timing of migration in response to changing climatic conditions is commonly proposed to drive these advances but plasticity in individual migratory timings is rarely observed. For a shorebird population that has significantly advanced migration in recent decades, we show that individual arrival dates are highly consistent between years, but that the arrival dates of new recruits to the population are significantly earlier now than in previous years. Several mechanisms could drive advances in recruit arrival, none of which require individual plasticity or rapid evolution of migration timings. In particular, advances in nest-laying dates could result in advanced recruit arrival, if benefits of early hatching facilitate early subsequent spring migration. This mechanism could also explain why arrival dates of short-distance migrants, which generally return to breeding sites earlier and have greater scope for advance laying, are advancing more rapidly than long-distance migrants.

Costs, benefits, and fitness consequences of different migratory strategies.

The relative fitness of individuals across a population can shape distributions and drive population growth rates. Migratory species often winter over large geographic ranges, and individuals in different locations experience very different environmental conditions, including different migration costs, which can potentially create fitness inequalities. Here we used energetics models to quantify the trade-offs experienced by a migratory shorebird species at locations throughout the nonbreeding range, and the associated consequences for migratory performance, survival, and breeding habitat quality. Individuals experiencing more favorable winter conditions had higher survival rates, arrived on the breeding grounds earlier, and occupied better quality breeding areas, even when migration costs are substantially higher, than individuals from locations where the energy balance on the wintering grounds was less favorable. The energy costs and benefits of occupying different winter locations can therefore create fitness inequalities which can shape the distribution and population-wide demography of migratory species.

Sex-biases in distribution and resource use at different spatial scales in a migratory shorebird.

In migratory species, sexual size dimorphism can mean differing energetic requirements for males and females. Differences in the costs of migration and in the environmental conditions occurring throughout the range may therefore result in sex-biases in distribution and resource use at different spatial scales. In order to identify the scale at which sexual segregation operates, and thus the scale at which environmental changes may have sex-biased impacts, we use range-wide tracking of individually color-ringed Icelandic black-tailed godwits (Limosa limosa islandica) to quantify sexual segregation at scales ranging from the occupation of sites throughout the non-breeding range to within-site differences in distribution and resource use. Throughout the range of this migratory shorebird, there is no evidence of large-scale sex differences in distribution during the non-breeding season. However, the sexes differ in their selection of prey types and sizes, which results in small-scale sexual segregation within estuaries. The scale of sexual segregation therefore depends on the scale of variation in resource distribution, which, in this system, is primarily within estuaries. Sexual segregation in within-site distribution and resource use means that local-scale anthropogenic impacts on estuarine benthic prey communities may disproportionately affect the sexes in these migratory shorebirds.

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

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

When density dependence is not instantaneous: theoretical developments and management implications.

Most organisms live in changing environments or do not use the same resources at different stages of their lives or in different seasons. As a result, density dependence will affect populations differently at different times. Such sequential density dependence generates markedly different population responses compared to the unrealistic assumption that all events occur simultaneously. Various field studies have also shown that the conditions that individuals experience during one period can influence success and per capita vital rates during the following period. These carry-over effects further complicate any general principles and increase the diversity of possible population dynamics. In this review, we describe how studies of sequential density dependence have diverged in directions that are both taxon-specific and have non-overlapping terminology, despite very similar underlying problems. By exploring and highlighting these similarities, we aim to improve communication between fields, clarify common misunderstandings, and provide a framework for improving conservation and management practices, including sustainable harvesting theory.

Why do female migratory birds arrive later than males?

1. In migratory birds males tend to arrive first on breeding grounds, except in sex-role reversed species. The two most common explanations are the rank advantage hypothesis, in which male-male competition for breeding sites drives stronger selection for early arrival in males than females, and the mate opportunity hypothesis, which relies on sexual selection, as early arrival improves prospects of mate acquisition more for males than for females. 2. To date, theoretical work has focused on selection for early arrival within a single sex, usually male. However, if fitness depends on territory quality, selection for early arrival should operate on both sexes. Here we use two independent modelling approaches to explore the evolution of protandry (male-first arrival) and protogyny (female-first arrival) under the rank advantage and mate opportunity hypotheses. 3. The rank advantage hypothesis, when operating alone, fails to produce consistent patterns of protandry, despite our assumption that males must occupy territories before females. This is because an individual of either sex benefits if it out-competes same-sex competitors. Rather than promoting protandry, the rank advantage mechanism can sometimes result in protogyny. Female-female competition is stronger than male-male competition early in the season, if females compete for a resource (territories occupied by males) that is initially less common than the resource of interest to males (unoccupied territories). 4. Our results support the mate opportunity hypothesis as an explanation of why protandry is the norm in migratory systems. Male-biased adult sex ratios and high levels of sperm competition (modelled as extra-pair young: EPY) both produce protandry as a result of sexual selection. Protogyny is only observed in our models with female-biased sex ratios and low EPY production. 5. We also show that the effects of sex ratio biases are much stronger than those of EPY production, explore the evidence for sex ratio biases and extra-pair paternity in migratory species and suggest future research directions.

Population-scale drivers of individual arrival times in migratory birds.

1. In migratory species, early arrival on the breeding grounds can often enhance breeding success. Timing of spring migration is therefore a key process that is likely to be influenced both by factors specific to individuals, such as the quality of winter and breeding locations and the distance between them, and by annual variation in weather conditions before and during migration. 2. The Icelandic black-tailed godwit Limosa limosa islandica population is currently increasing and, throughout Iceland, is expanding into poorer quality breeding areas. Using a unique data set of arrival times in Iceland in different years for individuals of known breeding and wintering locations, we show that individuals breeding in lower quality, recently occupied and colder areas arrive later than those from traditionally occupied areas. The population is also expanding into new wintering areas, and males from traditionally occupied winter sites also arrive earlier than those occupying novel sites. 3. Annual variation in timing of migration of individuals is influenced by large-scale weather systems (the North Atlantic Oscillation), but between-individual variation is a stronger predictor of arrival time than the NAO. Distance between winter and breeding sites does not influence arrival times. 4. Annual variation in timing of migration is therefore influenced by climatic factors, but the pattern of individual arrival is primarily related to breeding and winter habitat quality. These habitat effects on arrival patterns are likely to operate through variation in individual condition and local-scale density-dependent processes. Timing of migration thus appears to be a key component of the intricate relationship between wintering and breeding grounds in this migratory system.