Why do some,but not all,tropical birds migrate? A comparative study of diet breadth and fruit preference

Annual migrations of birds profoundly influence terrestrial communities. However, few empirical studies examine why birds migrate, in part due to the difficulty of testing causal hypotheses in long-distance migration systems. Short-distance altitudinal migrations provide relatively tractable systems in which to test explanations for migration. Many past studies explain tropical altitudinal migration as a response to spatial and temporal variation in fruit availability. Yet this hypothesis fails to explain why some coexisting, closely-related frugivorous birds remain resident year-round. We take a mechanistic approach by proposing and evaluating two hypotheses (one based on competitive exclusion and the other based on differences in dietary specialization) to explain why some, but not all, tropical frugivores migrate. We tested predictions of these hypotheses by comparing diets, fruit preferences, and the relationships between diet and preference in closely-related pairs of migrant and resident species. Fecal samples and experimental choice trials revealed that sympatric migrants and residents differed in both their diets and fruit preferences. Migrants consumed a greater diversity of fruits and fewer arthropods than did their resident counterparts. Migrants also tended to have slightly stronger fruit preferences than residents. Most critically, diets of migrants more closely matched their preferences than did the diets of residents. These results suggest that migrants may be competitively superior foragers for fruit compared to residents (rather than vice versa), implying that current competitive interactions are unlikely to explain variation in migratory behavior among coexisting frugivores. We found some support for the dietary specialization hypothesis, propose refinements to the mechanism underlying this hypothesis, and discuss how dietary specialization might ultimately reflect past interspecific competition. We recommend that future studies quantify variation in nutritional content of tropical fruits, and determine whether frugivory is a consequence or a cause of migratory behaviour.     

Storms drive altitudinal migration in a tropical bird

Although migration is a widespread and taxonomically diverse behaviour, the ecological factors shaping migratory behaviour are poorly understood. Like other montane taxa, many birds migrate along elevational gradients in the tropics. Forty years ago, Alexander Skutch postulated that severe storms could drive birds to migrate downhill. Here, we articulate a novel mechanism that could link storms to mortality risks via reductions in foraging time and provide, to our knowledge, the first tests of this hypothesis in the White-ruffed Manakin (Corapipo altera), a small partially migratory frugivore breeding on the Atlantic slope of Costa Rica. As predicted, variation in rainfall was associated with plasma corticosterone levels, fat stores, plasma metabolites and haematocrit. By collecting data at high and low elevation sites simultaneously, we also found that high-elevation residents were more adversely affected by storms than low elevation migrants. These results, together with striking temporal capture patterns of altitudinal migrants relative to storms, provide, to our knowledge, the first evidence that weather-related risks incurred by species requiring high food intake rates can explain altitudinal migrations of tropical animals. These findings resolve conflicting evidence for and against food limitation being important in the evolution of this behaviour, and highlight how endogenous and exogenous processes influence life-history trade-offs made by individuals in the wild. Because seasonal storms are a defining characteristic of most tropical ecosystems and rainfall patterns will probably change in ensuing decades, these results have important implications for understanding the ecology, evolution and conservation of tropical animals.     

Altitudinal migration: ecological drivers,knowledge gaps,and conservation implications

Animal migration has been the subject of intensive research for more than a century, but most research has focused on long‐distance rather than short‐distance migration. Altitudinal migration is a form of short‐distance migration in which individuals perform seasonal elevational movements. Despite its geographic and taxonomic ubiquity, there is relatively little information about the intrinsic and extrinsic factors that influence altitudinal migratory behaviour. Without this information, it is difficult to predict how rapid environmental changes will affect population viability of altitudinal migrants. To synthesize current knowledge, we compiled literature on altitudinal migration for all studied taxa, and identified the leading hypotheses explaining this behaviour. Studies of animal altitudinal migration cover many taxonomic lineages, with birds being the most commonly studied group. Altitudinal migration occurs in all continents except for Antarctica, but about a third of the literature focused on altitudinal migration in North America. Most research suggests that food and weather are the primary extrinsic drivers of altitudinal migration. In addition, substantial individual‐level variation in migratory propensity exists. Individual characteristics that are associated with sex, dominance rank, and body size explain much of the variation in migratory propensity in partially migratory populations, but individual‐level correlates are poorly known for most taxa. More research is needed to quantify the effects of habitat loss, habitat fragmentation, and climate change on altitudinal migrants. Demographic studies of individually marked populations would be particularly valuable for advancing knowledge of the cascading effects of environmental change on migratory propensity, movement patterns, and population viability. We conclude our review with recommendations for study designs and modelling approaches that could be used to narrow existing knowledge gaps, which currently hinder effective conservation of altitudinal migratory species.     

Altitudinal migration by birds: a review of the literature and a comprehensive list of species

Altitudinal migration is the seasonal altitudinal movement of birds from breeding areas to non‐breeding or wintering areas at different elevations. Although this type of migration is widely reported, questions remain concerning the number of species that perform altitudinal migration, possible variation among different taxa and geographic locations in the extent of altitudinal migration, and the foraging guilds of altitudinal migrants. We conducted an extensive bibliographic survey and compiled a list of altitudinal migrant birds worldwide. We characterized species in terms of their foraging guilds because the spatial distribution of food resources along altitudinal gradients is often evoked as a driver of bird altitudinal migration. We identified 1238 species of altitudinal migrants, ~10% of the ~10,000 extant species of birds. We found a strong geographic bias in publications focusing on avian altitudinal migration toward the United States and Costa Rica, and a paucity of studies in megadiverse regions such as the Afrotropical and Indomalayan realms, and areas in the Neotropics other than Costa Rica. We also found that most species of altitudinal migrants were invertivores rather than frugivores or nectarivores. This general pattern held true for all zoogeographic realms except the Neotropics, where nectarivores and frugivores predominated among altitudinal migrants. The prevalence of invertivore birds among altitudinal migrants is not unexpected because this is the most common foraging guild among birds worldwide. Overall, we found no prevalence of any specific foraging guild among altitudinal migrants across zoogeographic regions. The results of studies to date suggest that altitudinal migration by birds may be driven by a number of factors, including access to increased food resources for breeding or molting, weather conditions, and mating and nesting opportunities. However, to better understand the mechanisms underlying altitudinal migration, broadening the geographic scope of studies is paramount, with additional study of altitudinal migration especially needed in the megadiverse tropical regions of sub‐Saharan Africa, Southeast Asia, and South America.     

Young and female‐biased irruptions in pygmy owls Glaucidium passerinum in southern Finland

Irruptive migrants often show biased sex and age ratio, and typically young females are the most abundant class participating in irruptions. Several hypotheses have been proposed to explain differential migration in birds. We examined these hypotheses in a sexually size‐dimorphic species (females being larger than males), the pygmy owl Glaucidium passerinum, whose migration behaviour has also been poorly documented. Migration data were collected at the Hanko Bird Observatory, SW Finland during 1979–2010. Pygmy owls showed large fluctuations in migration numbers between years. Most of the migrants were young birds and females migrated in larger numbers than males. Results support the ‘territory defence hypothesis’ since males showed weaker tendency to migrate despite the smaller body size, but the ‘dominance hypothesis’ was also supported (subordinate young outnumber dominant adults in migration numbers). Findings support the idea that in owl species, which are dependent on nesting cavities, males show lower migration behaviour than females, whereas the pattern is opposite in species which normally breed outside cavities. In addition, adults migrated later than young, likely because they need to moult remiges before departure. Early hatched young also migrated earlier than late hatched young, suggesting that more dominant young migrate first.     

Correlates of alternative migratory strategies in western bluebirds

Partial migration occurs when only some animals in a population migrate. While evidence suggests that migratory strategies are partially controlled by genes, individual and environmental conditions which alter the cost‐benefit trade‐off of migration among individuals are also likely to play a role. Three hypotheses have been advanced to explain condition‐dependent partial migration: the arrival time, dominance and body size hypotheses. In this study, we asked whether these hypotheses explained differences in migratory strategy among individuals in a partially migratory population of western bluebirds Sialia mexicana breeding in southern British Columbia, Canada. We used stable hydrogen isotope signatures in claw tissue to determine migratory strategy of individual bluebirds, and examined patterns of migration at both individual and population levels. The proportion of resident bluebirds varied significantly over the three years of the study, and across study sites. Several migrants switched to the resident strategy between years; however, we found no evidence of strategy switching in the opposite direction. Young birds were significantly more likely to be resident than older birds, a pattern which could arise if early arrival is particularly important for birds obtaining a territory for the first time. Furthermore, young females were the most likely of all sex–age classes to be resident, which may reflect a survival advantage of residency for young females. Finally, birds mated assortatively by migratory strategy and isotopic evidence suggests that members of a pair often wintered in the same place. Our results provided no support for the dominance or body size hypotheses, and only limited support for the arrival time hypothesis in bluebirds. However, taken together, we suggest that our findings indicate that social factors may influence migratory strategies in this system.     

Short‐distance partial migration of Neotropical birds: a community‐level test of the foraging limitation hypothesis

Partial migration of tropical birds was long believed to be driven by variation in food abundance. Recent evidence from a partially‐migratory species suggests that in contrast, limited foraging opportunities at high elevations during severe wet season storms drives the most metabolically‐challenged individuals down to elevations where rainfall is lighter. Here, I test community‐level predictions of this hypothesis by examining the relationship between high‐elevation rainfall in the second half of the year and counts of migrant birds in lowland forest during late December each year from 1990–2009. I contrast results derived from analysis of all migrant species with both analyses of only the frugivorous migrants, and analyses of resident species. Counts of migrant species were on average positively associated with montane rainfall with differences of up to 72% in the numbers of birds counted in drier or wetter years. Frugivores and smaller birds responded more strongly to variation in rainfall compared to the broader migrant species pool. Interestingly, counts of resident species were also higher following wetter montane wet seasons. Results of analyses exploring the cause of resident responses were not consistent with climatic effects on breeding productivity or short‐term weather effects on detectability. Results were, however, consistent with cryptic down‐slope migration of individuals breeding at higher elevations augmenting lowland resident populations in wet years. These results suggest that changes in rainfall amount, storm intensity, and timing of severe weather events would lead to large increases in or losses of an important behaviour.     

Directions in modelling partial migration: how adaptation can cause a population decline and why the rules of territory acquisition matter

Modelling of partial migration in birds has progressed from simple graphical representations to sophisticated analyses that use evolutionary invasion analysis to determine how the success of the two strategies (stay year round on the breeding grounds, or migrate) can become frequency dependent. Here I build two models to relax two assumptions commonly made in models and often violated in nature: that individuals do not vary in any trait other than their migratory propensity, and that the prior residence effect (which grants priority access of good habitats to non‐migrants) operates at maximum strength. The same framework can incorporate and merge aspects of various hypotheses proposed to explain partial migration (dominance, body size, arrival timing, and limited foraging opportunities), and shows that either small (subdominant) or large (dominant) individuals may emerge as the more likely migrants; the latter case occurs when it is easy for socially dominant migrants to win back prime breeding locations upon their arrival. The dynamics of territory acquisition is shown to be an important and understudied topic, as variations in the relative importance of prior residency versus resource holding power can shift a population from complete migration to complete year‐round residency. These models also highlight exceptions to a tacit assumption in discussions of evolution of migration under climate change, which is that populations can decline if genetic adaptation or phenotypic plasticity do not occur fast enough. Competition can also yield the opposite pattern where adaptation itself leads to a population decline.     

Flight by night or day? Optimal daily timing of bird migration

Many migratory bird species fly mainly during the night (nocturnal migrants), others during daytime (diurnal migrants) and still others during both night and day. Need to forage during the day, atmospheric structure, predator avoidance and orientation conditions have been proposed as explanations for the widespread occurrence of nocturnal migration. However, the general principles that determine the basic nocturnal-diurnal variation in flight habits are poorly known. In the present study optimal timing of migratory flights, giving the minimum total duration of the migratory journey, is evaluated in a schematic way in relation to ecological conditions for energy gain in foraging and for energy costs in flight. There exists a strong and fundamental advantage of flying by night because foraging time is maximized and energy deposition can take place on days immediately after and prior to the nocturnal flights. The increase in migration speed by nocturnal compared with diurnal migration will be largest for birds with low flight costs and high energy deposition rates. Diurnal migration will be optimal if it is associated with efficient energy gain immediately after a migratory flight because suitable stopover/foraging places have been located during the flight or if energy losses during flight are substantially reduced by thermal soaring and/or by fly-and-forage migration. A strategy of combined diurnal and nocturnal migration may be optimal when birds migrate across regions with relatively poor conditions for energy deposition (not only severe but also soft barriers). Predictions about variable timing of migratory flights depending on changing foraging and environmental conditions along the migration route may be tested for individual birds by analysing satellite tracking results with respect to daily travel routines in different regions. Documenting and understanding the adaptive variability in daily travel schedules among migrating animals constitute a fascinating challenge for future research.     

Breeding latitude predicts timing but not rate of spring migration in a widespread migratory bird in South America

相似文献   

The evolution of migration in a seasonal environment

Despite the fact that migration occurs in a wide variety of taxa worldwide, little is known about the conditions under which migration is expected to evolve from an ancestral resident population. We develop a model that focuses on ecological factors affecting the evolution of migration in a seasonal environment within a genetically explicit framework. We model the evolution of migration for two common types of migration: ‘shared breeding’ where migrants share a breeding ground with residents and migrate to a separate non-breeding area, versus ‘shared non-breeding’, where migrants share a non-breeding ground with residents and migrate to a separate breeding area. Ecologically, migration is more easily established in the shared-breeding case versus the shared-non-breeding case. Genetically, the additive effect of a migratory allele affects its establishment more in the shared-non-breeding case versus the shared-breeding case, whereas the dominance effect of the allele affects its establishment more in the shared-breeding case versus the shared-non-breeding case. Generally, migratory alleles can invade even when residents are competitively superior to migrants during the shared season. Partial migration occurs when the population is polymorphic for migratory and non-migratory alleles, and is dependent upon which season is shared and the additive and dominance behaviour of the migratory allele.     

Habitat selection and coexistence of migrants and Afrotropical residents

In this paper I discuss factors that influence the habitat choice of small migrant birds on their Afrotropical wintering grounds and the ecological isolation of migrants and residents. The main characteristic of migrants is the use of resources which are sporadic in space and time. The majority of migrants occur in seasonal savannas and open woodland, mostly using temporarily and locally abundant food sources generally unused by residents. Migrants are more eurytopic and exploit more open parts of the habitats than ecologically similar tropical species. In some guilds, the foraging speed and rate of migrants is higher and they use their wings more often in comparison to residents. There is weak evidence that niche shifts of residents are induced by the arrival of migrants. Overt interspecific interactions seem to be infrequent, except in a guild of ground-feeding birds which rely on a rather predictable but poor food supply. In this guild, residents, but not intra-African migrants, dominated Palaearctic migrants in aggressive encounters irrespective of body-size. In contrast to this, dominance was size-dependent among wintering Palaearctic migrants.     

Variation in songbird migratory behavior offers clues about adaptability to environmental change

For seasonally migrating birds, aspects of migratory behavior, such as the use of temperate versus tropical wintering areas, may influence their ability to respond to environmental change. Here, we infer potential flexibility in songbird migration from variation in two alternative stopover behaviors. Hierarchical Bayesian mark–recapture modeling was used to quantify stopover decisions over 19 years for four temperate and four tropical migratory species at a stopover site in southern Canada. Short-distance temperate migrants exhibited higher variability in behavior and greater responses to local weather than longer-distance tropical migrants, as measured by transience (the proportion of birds stopping <24 h, i.e. seeking brief sanctuary or subsequently relocating) and departure (re-initiation of migration by birds that stopped over for >24 h). In contrast to many previous works on climate–migration associations, annual variation in stopover behavior did not show strong links to broad-scale climatic fluctuations for either temperate or tropical migrants, nor was there any indication of directional changes in stopover behavior over the past two decades. In addition to suggesting that migratory songbirds—particularly tropical-wintering species—may face increasing threats with future climatic variability, our study highlights the potential importance of flexibility in en-route behavior for resilience to environmental change.     

Winter rainfall predicts phenology in widely separated populations of a migrant songbird

Climate change is affecting behaviour and phenology in many animals. In migratory birds, weather patterns both at breeding and at non-breeding sites can influence the timing of spring migration and breeding. However, variation in responses to weather across a species range has rarely been studied, particularly among populations that may winter in different locations. We used prior knowledge of migratory connectivity to test the influence of weather from predicted non-breeding sites on bird phenology in two breeding populations of a long-distance migratory bird species separated by 3,000 km. We found that winter rainfall showed similar associations with arrival and egg-laying dates in separate breeding populations on an east–west axis: greater rainfall in Jamaica and eastern Mexico was generally associated with advanced American redstart (Setophaga ruticilla) phenology in Ontario and Alberta, respectively. In Ontario, these patterns of response could largely be explained by changes in the behaviour of individual birds, i.e., phenotypic plasticity. By explicitly incorporating migratory connectivity into responses to climate, our data suggest that widely separated breeding populations can show independent and geographically specific associations with changing weather conditions. The tendency of individuals to delay migration and breeding following dry winters could result in population declines due to predicted drying trends in tropical areas and the tight linkage between early arrival/breeding and reproductive success in long-distance migrants.     

Drop-catch behaviour is play in herring gulls,Larus argentatus

Behaviours with no apparent adaptive function are sometimes described as play without rigorous testing of alternative explanations. One such behaviour is the repeated dropping and catching of objects by birds. We observed drop-catch behaviour by herring gulls over 3 years at a site where the birds frequently dropped clams to break them on hard surfaces below. We tested unique suites of predictions from three hypotheses, that the drop-catch behaviour is play, that it functions to expose potential kleptoparasites, or that it serves to reposition clams before foraging drops. We tested data from 72 drop-catch series and 504 typical foraging drop series to determine which suite of predictions most closely matched our observations. As predicted if the behaviour were play, drop-catches were performed more by younger birds, not necessarily over a hard substrate, and sometimes with nonfood objects. Clams that were subjected to drop-catches were generally not repositioned or eaten. These results suggest a motivation for drop-catching that is distinct from foraging. Finally, drop-catches were more frequent when it was warm and when there were high winds, also consistent with the play hypothesis. Drop-catch behaviour closely matched the predictions of the play hypothesis and we were able to reject the two alternative explanations.     

Cold tolerance,and not earlier arrival on breeding grounds,explains why males winter further north in an Arctic‐breeding songbird

Sex biases in distributions of migratory birds during the non‐breeding season are widespread; however, the proximate mechanisms contributing to broad‐scale sex‐ratio variation are not well understood. We analyzed a long‐term winter‐banding dataset in combination with spring migration data from individuals tracked by using geolocators to test three hypotheses for observed variation in sex‐ratios in wintering flocks of snow buntings Plectrophenax nivalis. We quantified relevant weather conditions in winter (temperature, snowfall and snow depth) at each banding site each year and measured body size and condition (fat scores) of individual birds (n > 5500). We also directly measured spring migration distance for 17 individuals by using light‐level geolocators. If the distribution pattern of birds in winter is related to interactions between individual body size and thermoregulation, then larger bodied birds (males) should be found in colder sites (body size hypothesis). Males may also winter closer to breeding grounds to reduce migration distance for early arrival at breeding sites (arrival timing hypothesis). Finally, males may be socially dominant over females, and thus exclude females from high‐quality wintering sites (social dominance hypothesis). We found support for the body size hypothesis, in that colder and snowier weather predicted both larger body size and higher proportions of males banded. Direct tracking revealed that males did not winter significantly closer to their breeding site, despite being slightly further north on average than females from the same breeding population. We found some evidence for social dominance, in that females tended to carry more fat than males, potentially indicating lower habitat quality for females. Global climatic warming may reduce temperature constraints on females and smaller‐bodied males, resulting in broad‐scale changes in distributional patterns. Whether this has repercussions for individual fitness, and therefore population demography, is an important area of future research.     

Rapid 'evolution' of migratory behaviour in the introduced house finch of eastern North America

The house finch (Carpodacus mexicanus) of eastern North America was introduced onto Long Island, New York, around 1940. The source is presumed to be southern California, where ca. 80% of individuals are completely sedentary. The eastern population has become migratory: by the early 1960s, 36% of eastern house finches were performing migratory movements (more than 80 km from their banding site) and that proportion has fluctuated between 28% and 54% in succeeding years. The movements of birds banded during the breeding season and recovered in winter were strongly orientated toward the south-west, and the same pattern was evident in the earliest recoveries (1958 to 1966); recoveries of birds banded during winter and recovered in the breeding season were orientated toward the north-east. The average distance of migration has continued to increase logarithmically. Areas colonized later, as the range expanded, were characterized by initial long migration distances and high proportions of migrants, suggesting that these traits have evolved in the eastern population. Eastern house finches are partial migrants: not all individuals migrate, and birds that migrate some winters remain in breeding areas in others. Younger birds exhibit a stronger tendency to migrate. A very few western (including southern California) house finches moved long distances, but they did so in directions consistent with seasonal migration, indicating that the machinery subserving migratory behaviour pre-existed in the parent population.     

Sex differences in the stopover ecology of Curlew Sandpipers Calidris ferruginea at a refuelling area during autumn migration

We investigated the stopover patterns of male and female Curlew Sandpipers at a stopover area in northeast Spain. Curlew Sandpipers were trapped and colour-ringed during autumn migration in 1992 and 1993. Stopover length was similar to those reported previously for this and other waders that migrate using a small number of widely separated staging areas, but were greater than stopovers reported for other waders that migrate using a large number of staging areas separated by short distances. The differences in stopover length between the birds using these two strategies could be related to the fuel reserves that have to be accumulated to reach the next staging area. Males stayed longer in the area than females. Seasonal changes in prey availability or sex differences in moulting and migratory patterns do not account for these differences in stopover ecology. Following a time-selected model of optimal migration, sex differences in stopover ecology could be related to a dominance of the larger females over the males or to a higher foraging efficiency or a shorter search and settling time in females. Whether these differences are restricted to the studied area or are widespread in other staging areas used by the species could be important for assessing the possible differences in the migration speed of Curlew Sandpipers. The finding that males leave the breeding grounds 21–35 days before females but arrive at the study area with only a 10-day difference supports the hypothesis that females migrate faster than males at least in the first half of their migration.     

Ancestry and evolution of seasonal migration in the Parulidae

Seasonal migration in birds is known to be highly labile and subject to rapid change in response to selection, such that researchers have hypothesized that phylogenetic relationships should neither predict nor constrain the migratory behaviour of a species. Many theories on the evolution of bird migration assume a framework that extant migratory species have evolved repeatedly and relatively recently from sedentary tropical or subtropical ancestors. We performed ancestral state reconstructions of migratory behaviour using a comprehensive, well-supported phylogeny of the Parulidae (the 'wood-warblers'), a large family of Neotropical and Nearctic migratory and sedentary songbirds, and examined the rates of gain and loss of migration throughout the Parulidae. Counter to traditional hypotheses, our results suggest that the ancestral wood-warbler was migratory and that losses of migration have been at least as prevalent as gains throughout the history of Parulidae. Therefore, extant sedentary tropical radiations in the Parulidae represent losses of latitudinal migration and colonization of the tropics from temperate regions. We also tested for phylogenetic signal in migratory behaviour, and our results indicate that although migratory behaviour is variable within some wood-warbler species and clades, phylogeny significantly predicts the migratory distance of species in the Parulidae.