Barn Swallows (Hirundo rustica) breed almost exclusively in the Northern Hemisphere. However, since the early 1980's, a small disjunct breeding population has become established in eastern Argentina, presumably by birds previously derived from those breeding in North America. Currently, it is unknown where these individuals go following breeding and how they have adjusted to a reversal in phenology. Their austral wintering period corresponds to the breeding period of the northern ancestral population and so they can potentially return to these more traditional breeding sites or they may occupy other South American wintering regions left vacant by conspecifics returning to the Northern Hemisphere.
We used a three-isotope (δ13C, δ15N, δ2H) approach to investigate potential wintering areas in Central and South America of individuals breeding in Argentina. Feather isotope values differed from those expected and measured at local breeding sites in Argentina indicating molt after the austral breeding period and away from the breeding grounds. Potential molting origins were identified applying likelihood-based assignment methods to a δ2H isoscape for South America and dichotomous prior information on the distribution of C3 and C4 vegetation types based on modeled vegetation-δ13C values. Barn Swallows now breeding in Argentina have changed their migratory behavior but presumably use the same cues as those used by the ancestral population, molting their feathers during the austral winter, likely in north-eastern South America.
Large numbers of the Globe Skimmer dragonfly (Pantala flavescens) appear in the Maldives every October–December. Since they cannot breed on these largely waterless islands, it has recently been suggested that they are “falling out” during a trans-oceanic flight from India to East Africa. In addition, it has been suggested that this trans-oceanic crossing is just one leg of a multi-generational migratory circuit covering about 14,000–18,000 km. The dragonflies are presumed to accomplish this remarkable feat by riding high-altitude winds associated with the Inter-tropical Convergence Zone (ITCZ). While there is considerable evidence for this migratory circuit, much of that evidence is circumstantial. Recent developments in the application of stable isotope analyses to track migratory dragonflies include the establishment of direct associations between dragonfly wing chitin δ2H values with those derived from long-term δ2H precipitation isoscapes. We applied this approach by measuring wing chitin δ2H values in 49 individual Pantala flavescens from the November–December migration through the Maldives. Using a previously established spatial calibration algorithm for dragonflies, the mean wing δ2H value of −117±16 ‰ corresponded to a predicted mean natal ambient water source of −81 ‰, which resulted in a probabilistic origin of northern India, and possibly further north and east. This strongly suggests that the migratory circuit of this species in this region is longer than previously suspected, and could possibly involve a remarkable trans-Himalayan high-altitude traverse.
How different functional responses of consumers exploiting pulsed resources affect community dynamics is an ongoing question in ecology. Tree masting is a common resource pulse in terrestrial ecosystems that can drive rodent population cycles. Using stable isotope (δ13C, δ15N) analyses, we investigated the dietary response of two fluctuating rodent species, the yellow-necked mouse Apodemus flavicollis and the bank vole Myodes glareolus, to mast events in Białowieża Forest (NE Poland). Rodent hair samples were obtained non-invasively from faeces of their predators for an 11-year period that encompassed two mast events. Spectacular seed crops of deciduous trees, namely oak Quercus robur and hornbeam Carpinus betulus, occur after several intermediate years of moderate seed production, with a post-mast year characterised by a nil crop. While a Bayesian isotopic (SIAR) mixing model showed a variety of potential vegetation inputs to rodent diets, the isotopic niche of the yellow-necked mouse was strongly associated with mast of deciduous trees (>80% of diet), showing no variation among years of different seed crop. However, bank voles showed a strong functional response; in mast years the vole shifted its diet from herbs in deciduous forest (∼66% of diet) to mast (∼74%). Only in mast years did the isotopic niche of both rodent species overlap. Previous research showed that bank voles, subordinate and more generalist than mice, showed higher fluctuations in numbers in response to masting. This study provides unique data on the functional response of key pulse consumers in forest food webs, and contributes to our understanding of rodent population fluctuations and the mechanisms governing pulse–consumer interactions.
Facultative, partially migratory animals provide a contemporary window into the evolution of migration, offering rare opportunities to examine the life-history trade-offs associated with migration. For the first time, to our knowledge, we describe the nature of these trade-offs, using a lek-breeding tropical bird, the white-ruffed manakin (Corapipo altera). Previous evidence indicated that weather drives post-breeding migration to lower elevations bringing condition-related benefits. Using elevation-sensitive stable isotope measurements and more than 1200 h of behavioural observations, we show that male manakins which migrate incur costs of diminished social status and matings with females the following breeding season. Because migratory tendency depends on inter-annual variation in weather, physical costs of displays and breeding prospects the following year, migratory decisions are subject to both natural and sexual selection, with the outcome of such decisions linked to changing climatic regimes.
carry-over effects; evolution of migration; life-history trade-offs
Current rates of wildlife habitat loss have placed increasing demands on managers to develop, validate and implement tools aimed at improving our ability to evaluate such impacts on wildlife. Here, we present a case study conducted at the Natural Area of Doñana (SW Spain) where remote sensing and stable isotope (δ13C, δ15N) analyses of individuals were combined to unravel (1) the effect of variations in availability of natural food resources (i.e. from natural marshes) on reproductive performance of a Slender-billed Gull (Chroicocephalus genei) population, and (2) the role of two adjacent, artificial systems (a fish farm and saltmines) as alternate anthropogenic feeding areas. Based on long-term (1983–2004) remote-sensing, we inferred the average extent of flooded area at the marshland (a proxy to natural resource availability) annually. Estimated flooded areas (ranging from extreme drought [ca. 151 ha, 1995] to high moisture [15,049 ha, 2004]) were positively related to reproductive success of gulls (estimated for the 1993–2004 period, and ranging from ca. 0 to 1.7 fledglings per breeding pairs), suggesting that habitat availability played a role in determining their reproductive performance. Based on blood δ13C and δ15N values of fledglings, 2001–2004, and a Bayesian isotopic mixing model, we conclude that saltmines acted as the main alternative foraging habitat for gulls, with relative contributions increasing as the extent of marshland decreased. Although adjacent, anthropogenic systems have been established as the preferred breeding sites for this gull population, dietary switches towards exploitation of alternative (anthropogenic) food resources negatively affected the reproductive output of this species, thus challenging the perception that these man-made systems are necessarily a reliable buffer against loss of natural feeding habitats. The methodology and results derived from this study could be extended to a large suite of threatened natural communities worldwide, thus providing a useful framework for management and conservation.
The ability to connect breeding, stopover and wintering locations of populations of migratory birds greatly enhances our understanding of the phenomenon of migration and improves our chances of effectively conserving these species. Among Palearctic-Afrotropical migratory species, aerial insectivores like the house martin (Delichon urbicum) are sensitive to factors influencing the availability of flying insects, and have declined in recent decades. The strict aerial behaviour of martins severely limits ring recoveries on wintering grounds and so there is a dearth of information on where European breeding populations over-winter in Africa, and the relative effects of population regulation on breeding vs. wintering grounds. We used a newly developed multi-isotope (δ2H, δ13C, δ15N) feather isoscape for Africa together with inferences from summarized ring return data based on longitude, to assign winter origins to birds captured at a breeding colony in The Netherlands.
Based on isotopic analyses of winter-grown martin feathers, we used a likelihood-based assignment approach to describe potential wintering locations where molt occurred of individual house martins from a Dutch colony by assigning them to four potential isotopically distinct clusters in Africa. We found the overwhelming majority of Dutch martins were assigned to a geographical cluster associated with West Africa.
The existence of strong isotopic gradients and patterns in African foodwebs that support migratory wildlife allows for the spatial assignment of tissues grown there. The assignment of Dutch house martins to wintering grounds primarily in West Africa was in strong agreement with independent and indirect methods used to infer winter origins of this species based on the association between the Normalized Difference Vegetation Index (NDVI) in Africa and population patterns in Italy and the United Kingdom. These confirmatory data-sets underscore the importance of suitable habitats in West Africa to the conservation of migratory aerial insectivores and other species.
An enduring problem in avian ecology and conservation is linking breeding and wintering grounds of migratory species. As migratory species and populations vary in the degree to which individuals from distinct breeding locales mix on stop-over sites and wintering grounds, establishing migratory connectivity informs our understanding of population demography and species management. We present a new Bayesian approach for inferring breeding grounds of wintering birds of unknown origins in North America. We incorporate prior information from analysis of genetic markers into geographic origin assignment based upon stable-hydrogen isotope analysis of feathers (δ2Hf), using the Loggerhead Shrike (Lanius ludovicianus). Likely geographic origins derived from analyses of DNA microsatellites were used as priors for Bayesian analyses in which birds were assigned to a breeding-ground origin using their δ2Hf values. As with most applications of Bayesian methods, our approach greatly improved the results (i.e. decreased the size of the potential area of origin). Area of origin decreased by 3 to 5-fold on average, but ranged up to a 10-fold improvement. We recommend this approach in future studies of migratory connectivity and suggest that our methodology could be applied more broadly to the study of dispersal, sources of productivity of migratory populations, and a range of evolutionary phenomena.
The mallard Anas platyrhynchos is a reservoir species for influenza A virus in the northern hemisphere, with particularly high prevalence rates prior to as well as during its prolonged autumn migration. It has been proposed that the virus is brought from the breeding grounds and transmitted to conspecifics during subsequent staging during migration, and so a better understanding of the natal origin of staging ducks is vital to deciphering the dynamics of viral movement pathways. Ottenby is an important stopover site in southeast Sweden almost halfway downstream in the major Northwest European flyway, and is used by millions of waterfowl each year. Here, mallards were captured and sampled for influenza A virus infection, and positive samples were subtyped in order to study possible links to the natal area, which were determined by a novel approach combining banding recovery data and isotopic measurements (δ2H) of feathers grown on breeding grounds. Geographic assignments showed that the core natal areas of studied mallards were in Estonia, southern and central Finland, and northwestern Russia. This study demonstrates a clear temporal succession of latitudes of natal origin during the course of autumn migration. We also demonstrate a corresponding and concomitant shift in virus subtypes. Acknowledging that these two different patterns were based in part upon different data, a likely interpretation worth further testing is that the early arriving birds with more proximate origins have different influenza A subtypes than the more distantly originating late autumn birds. If true, this knowledge would allow novel insight into the origins and transmission of the influenza A virus among migratory hosts previously unavailable through conventional approaches.
Tracking small migrant organisms worldwide has been hampered by technological and recovery limitations and sampling bias inherent in exogenous markers. Naturally occurring stable isotopes of H (δ2H) in feathers provide an alternative intrinsic marker of animal origin due to the predictable spatial linkage to underlying hydrologically driven flow of H isotopes into foodwebs. This approach can assess the likelihood that a migrant animal originated from a given location(s) within a continent but requires a robust algorithm linking H isotopes in tissues of interest to an appropriate hydrological isotopic spatio-temporal pattern, such as weighted-annual rainfall. However, a number of factors contribute to or alter expected isotopic patterns in animals. We present results of an extensive investigation into taxonomic and environmental factors influencing feather δ2H patterns across North America.
Stable isotope data were measured from 544 feathers from 40 species and 140 known locations. For δ2H, the most parsimonious model explaining 83% of the isotopic variance was found with amount-weighted growing-season precipitation δ2H, foraging substrate and migratory strategy.
This extensive H isotopic analysis of known-origin feathers of songbirds in North America and elsewhere reconfirmed the strong coupling between tissue δ2H and global hydrologic δ2H patterns, and accounting for variance associated with foraging substrate and migratory strategy, can be used in conservation and research for the purpose of assigning birds and other species to their approximate origin.
Each year, millions of monarch butterflies (Danaus plexippus) migrate up to 3000 km from their overwintering grounds in central Mexico to breed in eastern North America. Malcolm et al. (1993) articulated two non-mutually exclusive hypotheses to explain how Monarchs re-colonize North America each spring. The ‘successive brood’ hypothesis proposes that monarchs migrate from Mexico to the Gulf Coast, lay eggs and die, leaving northern re-colonization of the breeding range to subsequent generations. The ‘single sweep’ hypothesis proposes that overwintering monarchs continue to migrate northward after arriving on the Gulf coast and may reach the northern portion of the breeding range, laying eggs along the way. To examine these hypotheses, we sampled monarchs throughout the northern breeding range and combined stable-hydrogen isotopes (δD) to estimate natal origin with wing wear scores to differentiate between individuals born in the current vs. previous year. Similar to Malcolm et al. (1993), we found that the majority of the northern breeding range was re-colonized by the first generation of monarchs (90%). We also estimated that a small number of individuals (10%) originated directly from Mexico and, therefore adopted a sweep strategy. Contrary to Malcolm et al. (1993), we found that 62% of monarchs sampled in the Great Lakes originated from the Central U.S., suggesting that this region is important for sustaining production in the northern breeding areas. Our results provide new evidence of re-colonization patterns in monarchs and contribute important information towards identifying productive breeding regions of this unique migratory insect.
Each spring, millions of monarch butterflies (Danaus plexippus) migrate from overwintering sites in Mexico to recolonize eastern North America. However, few monarchs are found along the east coast of the USA until mid-summer. Brower (Brower, L. P. 1996 J. Exp. Biol. 199, 93–103.) proposed that east coast recolonization is accomplished by individuals migrating from the west over the Appalachians, but to date no evidence exists to support this hypothesis. We used hydrogen (δD) and carbon (δ13C) stable isotope measurements to estimate natal origins of 90 monarchs sampled from 17 sites along the eastern United States coast. We found the majority of monarchs (88%) originated in the mid-west and Great Lakes regions, providing, to our knowledge, the first direct evidence that second generation monarchs born in June complete a (trans-) longitudinal migration across the Appalachian mountains. The remaining individuals (12%) originated from parents that migrated directly from the Gulf coast during early spring. Our results provide evidence of a west to east longitudinal migration and provide additional rationale for conserving east coast populations by identifying breeding sources.
Danaus plexippus; insect migration; migratory connectivity; stable isotopes
Several felids are endangered and threatened by the illegal wildlife trade. Establishing geographic origin of tissues of endangered species is thus crucial for wildlife crime investigations and effective conservation strategies. As shown in other species, stable isotope analysis of hydrogen and oxygen in hair (δDh, δ18Oh) can be used as a tool for provenance determination. However, reliably predicting the spatial distribution of δDh and δ18Oh requires confirmation from animal tissues of known origin and a detailed understanding of the isotopic routing of dietary nutrients into felid hair.
We used coupled δDh and δ18Oh measurements from the North American bobcat (Lynx rufus) and puma (Puma concolor) with precipitation-based assignment isoscapes to test the feasibility of isotopic geo-location of felidae. Hairs of felid and rabbit museum specimens from 75 sites across the United States and Canada were analyzed. Bobcat and puma lacked a significant correlation between H/O isotopes in hair and local waters, and also exhibited an isotopic decoupling of δ18Oh and δDh. Conversely, strong δD and δ18O coupling was found for key prey, eastern cottontail rabbit (Sylvilagus floridanus; hair) and white-tailed deer (Odocoileus virginianus; collagen, bone phosphate).
Puma and bobcat hairs do not adhere to expected pattern of H and O isotopic variation predicted by precipitation isoscapes for North America. Thus, using bulk hair, felids cannot be placed on δ18O and δD isoscapes for use in forensic investigations. The effective application of isotopes to trace the provenance of feline carnivores is likely compromised by major controls of their diet, physiology and metabolism on hair δ18O and δD related to body water budgets. Controlled feeding experiments, combined with single amino acid isotope analysis of diets and hair, are needed to reveal mechanisms and physiological traits explaining why felid hair does not follow isotopic patterns demonstrated in many other taxa.
Trophic segregation has been proposed as a major mechanism explaining the coexistence of closely related animal taxa. However, how such segregation varies throughout the annual cycle is poorly understood. Here, we examined the feeding ecology of the two subspecies of Cory's shearwater, Calonectris diomedea diomedea and Calonectris diomedea borealis, breeding in sympatry in a Mediterranean colony. To study trophic segregation at different stages, we combined the analysis of isotope values (δ
13C) in blood obtained during incubation and in feathers moulted during chick-rearing and wintering periods with satellite-tracking data during the chick-rearing period. Satellite-tracking and stable isotope data of the first primary feather revealed that C. d. borealis foraged mainly in the Atlantic whereas C. d. diomedea foraged exclusively in the Mediterranean. This spatial segregation could reflect the foraging behaviour of the C. d. borealis individuals before they arrived at the Mediterranean colony. Alternatively, greater wing loading of C. d. borealis individuals may confer the ability to fly across the strong winds occurring at the at the Gibraltar strait. Isotope values of the eighth secondary feather also support segregation in wintering areas between the two forms: C. d. diomedea wintered mainly in association with the Canary current, whereas C. d. borealis wintered in the South African coast. Overall, our results show that spatial segregation in foraging areas can display substantial variation throughout the annual cycle and is probably a major mechanism facilitating coexistence between closely related taxa.
feeding ecology; migration; satellite tracking; seabirds; stable isotopes
Elucidating geographic locations from where migratory birds are recruited into adult breeding populations is a fundamental but largely elusive goal in conservation biology. This is especially true for species that breed in remote northern areas where field-based demographic assessments are logistically challenging.
Here we used hydrogen isotopes (δD) to determine natal origins of migrating hatch-year lesser scaup (Aythya affinis) harvested by hunters in the United States from all North American flyways during the hunting seasons of 1999–2000 (n = 412) and 2000–2001 (n = 455). We combined geospatial, observational, and analytical data sources, including known scaup breeding range, δD values of feathers from juveniles at natal sites, models of δD for growing-season precipitation, and scaup band-recovery data to generate probabilistic natal origin landscapes for individual scaup. We then used Monte Carlo integration to model assignment uncertainty from among individual δD variance estimates from birds of known molt origin and also from band-return data summarized at the flyway level. We compared the distribution of scaup natal origin with the distribution of breeding population counts obtained from systematic long-term surveys.
Our analysis revealed that the proportion of young scaup produced in the northern (above 60°N) versus the southern boreal and Prairie-Parkland region was inversely related to the proportions of breeding adults using these regions, suggesting that despite having a higher relative abundance of breeding adults, the northern boreal region was less productive for scaup recruitment into the harvest than more southern biomes. Our approach for evaluating population declines of migratory birds (particularly game birds) synthesizes all available distributional data and exploits the advantages of intrinsic isotopic markers that link individuals to geography.
Although there is increasing evidence that climatic variations during the non-breeding season shape population dynamics of seabirds, most aspects of their winter distribution and ecology remain essentially unknown. We used stable isotope signatures in feathers to infer and compare the moulting (wintering) habitat of subantarctic petrels breeding at two distant localities (South Georgia and Kerguelen). Petrels showed species-specific wintering habitat preferences, with a similar pattern of latitudinal segregation for all but one taxon. At both localities, δ13C values indicated that blue petrels (Halobaena caerulea) moult in Antarctic waters, South Georgian diving petrels (Pelecanoides georgicus) in the vicinity of the archipelagos and/or in the Polar Frontal Zone and Antarctic prions (Pachyptila desolata) in warmer waters. In contrast, common diving petrels (Pelecanoides urinatrix) showed divergent strategies, with low and high intrapopulation variation at South Georgia and Kerguelen, respectively. Birds from Kerguelen dispersed over a much wider range of habitats, from coastal to oceanic waters and from Antarctica to the subtropics, whereas those from South Georgia wintered mainly in waters around the archipelago. This study is the first to show such striking between-population heterogeneity in individual wintering strategies, which could have important implications for likely demographic responses to environmental perturbation.
moulting period; individual specialization; procellariiform seabird; Southern Ocean; Antarctica
Cephalopods play a key role in the marine environment but knowledge of their feeding habits is limited by lack of data. Here, we have developed a new tool to investigate their feeding ecology by combining the use of their predators as biological samplers together with measurements of the stable isotopic signature of their beaks. Cephalopod beaks are chitinous hard structures that resist digestion and the stable isotope ratios of carbon (δ13C) and nitrogen (δ15N) are indicators of the foraging areas and trophic levels of consumers, respectively. First, a comparison of δ13C and δ15N values of different tissues from the same individuals showed that beaks were slightly enriched in 13C but highly impoverished in 15N compared with lipid-free muscle tissues. Second, beaks from the same species showed a progressive increase in their δ15N values with increasing size, which is in agreement with a dietary shift from lower to higher trophic levels during cephalopod growth. In the same way, there was an increase in the δ15N signature of various parts of the same lower beaks in the order rostrum, lateral walls and wings, which reflects the progressive growth and chitinization of the beaks in parallel with dietary changes. Third, we investigated the trophic structure of a cephalopod community for the first time. Values of δ15N indicate that cephalopods living in slope waters of the subantarctic Kerguelen Islands (n=18 species) encompass almost three distinct trophic levels, with a continuum of two levels between crustacean- and fish-eaters and a distinct higher trophic level occupied by the colossal squid Mesonychoteuthis hamiltoni. δ13C values demonstrated that cephalopods grow in three different marine ecosystems, with 16 species living and developing in Kerguelen waters and two species migrating from either Antarctica (Slosarczykovia circumantarctica) or the subtropics (the giant squid Architeuthis dux). The stable isotopic signature of beaks accumulated in predators' stomachs therefore revealed new trophic relationships and migration patterns and is a powerful tool to investigate the role of the poorly known cephalopods in the marine environment.
Antarctica; community; octopus; ontogenic changes; Southern Ocean predators
Population studies assume that individuals belonging to a study population are homogeneous for natal and breeding origin, although this assumption is rarely tested. We tested for heterogeneity in stable-isotope profiles (delta15N, delta13C, deltaD) of feathers grown in the African winter quarters from a Danish breeding population of adult barn swallows, Hirundo rustica. Deuterium isotope values did not provide useful information on population segregation of wintering swallows in Africa. However, both delta15N and delta13C values showed a clearly bimodal distribution with 6% belonging to one category and the remaining birds belonging to another category, resulting in this population comprising three categories of birds. Adults belonging to the two categories of delta13C isotope profiles differed weakly in morphology for several different characters. The frequency and the size of second broods differed between categories of delta13C isotope profiles. Phenotypes of nestlings from the first brood in terms of tarsus length, body mass and T-cell response differed significantly between the two delta15N isotope categories, suggesting that conditions during winter carried over to the breeding season at least as late as the first brood. Polymorphism can be maintained only if fitness is similar for birds from categories of isotope profiles. We suggest that fluctuating selection or migration-selection balance may maintain the observed polymorphism.