András Kosztolányi

The influence of a hot environment on parental cooperation of a ground-nesting shorebird, the Kentish plover Charadrius alexandrinus

BackgroundParental care often increases offspring survival, but is costly to the parents. A trade-off between the cost and benefit of care is expected, so that when care provisioning by both parents is essential for the success of young, for instance in extremely cold or hot environments, the parents should rear their young together. We investigated the latter hypothesis in a ground nesting shorebird, the Kentish plover Charadrius alexandrinus in an extremely hot environment, the Arabian Desert. Midday ground temperature was often above 50°C in our study site in Abu Dhabi (United Arab Emirates), thus leaving the eggs unattended even for a few minute risks overheating and death of embryos.ResultsThrough the use of video surveillance systems we recorded incubation routines of male and female Kentish plovers at 28 nests over a full day (24 h). We show that ambient temperature had a significant influence on incubation behaviour of both sexes, and the relationships are often non-linear. Coordinated incubation between parents was particularly strong in midday with incubation shared approximately equally between the male and the female. The enhanced biparental incubation was due to males increasing their nest attendance with ambient temperature.ConclusionsOur results suggest biparental care is essential during incubation in the Kentish plover in extremely hot environments. Shared incubation may also help the parents to cope with heat stress themselves: they can relieve each other frequently from incubation duties. We suggest that once the eggs have hatched the risks associated with hot temperature are reduced: the chicks become mobile, and they gradually develop thermoregulation. When biparental care of young is no longer essential one parent may desert the family. The relaxed demand of the offspring may contribute to the diverse breeding systems exhibited by many shorebirds.

Conflict between genetic and phenotypic differentiation: the evolutionary history of a 'lost and rediscovered' shorebird.

Understanding and resolving conflicts between phenotypic and genetic differentiation is central to evolutionary research. While phenotypically monomorphic species may exhibit deep genetic divergences, some morphologically distinct taxa lack notable genetic differentiation. Here we conduct a molecular investigation of an enigmatic shorebird with a convoluted taxonomic history, the White-faced Plover (Charadrius alexandrinus dealbatus), widely regarded as a subspecies of the Kentish Plover (C. alexandrinus). Described as distinct in 1863, its name was consistently misapplied in subsequent decades until taxonomic clarification ensued in 2008. Using a recently proposed test of species delimitation, we reconfirm the phenotypic distinctness of dealbatus. We then compare three mitochondrial and seven nuclear DNA markers among 278 samples of dealbatus and alexandrinus from across their breeding range and four other closely related plovers. We fail to find any population genetic differentiation between dealbatus and alexandrinus, whereas the other species are deeply diverged at the study loci. Kentish Plovers join a small but growing list of species for which low levels of genetic differentiation are accompanied by the presence of strong phenotypic divergence, suggesting that diagnostic phenotypic characters may be encoded by few genes that are difficult to detect. Alternatively, gene expression differences may be crucial in producing different phenotypes whereas neutral differentiation may be lagging behind.

Kentish Versus Snowy Plover: Phenotypic and Genetic Analyses of Charadrius alexandrinus Reveal Divergence of Eurasian and American Subspecies

ABSTRACT. Many shorebird species have widespread geographic distributions comprising several continents. Because shorebirds are excellent flyers and can migrate large distances, it is often unclear whether reproductive barriers between subspecies and populations from different continents exist. Kentish-Snowy Plovers (Charadrius alexandrinus) are cosmopolitan shorebirds. Whether the American and Eurasian subspecies-Snowy Plover and Kentish Plover, respectively—constitute a single species is the subject of a longstanding debate. We examined the divergence between American and Eurasian populations to reassess the current taxonomy by comparing genetic and phenotypic characters of the American subspecies C. a. nivosus and the Eurasian subspecies C. a. alexandrinus from seven populations. Genetic analyses revealed that American and Eurasian populations have strongly diverged, the Kentish Plover being more closely related to the White-fronted Plover (C. marginatus) than to the Snowy Plover. These results were consistent across all assessed nuclear markers (26 microsatellites and a partial CHD sequence) and two mitochondrial markers (ND3 and ATPase 6/8). Within subspecies, populations sampled across large geographic distances were not genetically differentiated (all F st ≤ 0.01 and all &PHgr;st ≤ 0.06), which suggests panmixia. Snowy Plovers differed morphologically from Kentish Plovers, having significantly shorter tarsi and wings. Chick plumage and calls also may serve as diagnostic characters to distinguish Snowy and Kentish plovers, although more data are needed to quantify these differences. Our combined results suggest that the taxonomic status of C. alexandrinus needs to be revised, and we propose that Kentish Plover and Snowy Plover be recognized as separate species: C. alexandrinus and C. nivosus, respectively.

The effects of age and sex on the apparent survival of Kentish Plovers breeding in southern Turkey

Abstract Accurate estimates of annual survival are necessary for conservation of threatened species of migratory birds. We studied a large, stable population of Kentish Plovers (Charadrius alexandrinus) breeding in southern Turkey (36°43′N, 35°03′E) for five breeding seasons (1996–2000). Kentish Plovers of Eurasia and the conspecific Snowy Plover of North America are a species of conservation concern. We captured 2077 birds, and used time since marking models to estimate apparent survival (ϕ) and encounter rates (p) for juvenile and adult plovers. Return rates of young banded in their natal year were low (4%, 52 of 1176) and most philopatric young were recaptured as yearlings (69%, 36 of 52). Low return rates of shorebird young can be attributed to post-hatching mortality if apparent survival rates are ranked: chicks < fledglings = adults. We were unable to separate mortality from dispersal because apparent survival was ranked: chicks (ϕ̂1 = 0.08) < fledglings (ϕ̂1 = 0.15) < adults after banding (ϕ̂1 = 0.59) < adults in later intervals (ϕ̂2+ = 0.64). Time since marking models gave improved estimates of the apparent survival of adults that were higher than return rates in other populations of Kentish Plovers, but lower than estimates of apparent survival for other Charadrius plovers. Sex-biased mating opportunities in Kentish Plovers were not explained by biased sex ratios at hatching or differential apparent survival among adults. Instead, male-biased adult sex ratios were explained, in part, by differential survival of juveniles and by higher encounter rates among adult males (p̂ = 0.84) than females (p̂ = 0.74). Our baseline estimates of apparent survival will assist assessments of population viability for Kentish and Snowy Plovers throughout their geographic range. Efectos de la Edad y del Sexo sobre la Supervivencia Aparente de Charadrius alexandrinus en Áreas de Cría en el Sur de Turquía Resumen. Contar con estimaciones exactas de la supervivencia anual es necesario para la conservación de las aves migratorias amenazadas. Estudiamos una población grande y estable de Charadrius alexandrinus en un área de cría del sur de Turquía (36°43′N, 35°03′E) durante cinco épocas reproductivas (1996–2000). Charadrius alexandrinus es una especie con un estado de conservación preocupante tanto en Eurasia como en Norte América. En este estudio capturamos 2077 aves y empleamos modelos del tiempo transcurrido desde el marcado para estimar las tasas de supervivencia aparente (ϕ) y de encuentro (p) para individuos juveniles y adultos. Las tasas de regreso de juveniles anillados a su área de nacimiento fueron bajas (4%, 52 de 1176), y la mayoría de los individuos filopátricos fueron recapturados cuando tenían un año de edad (69%, 36 de 52). Las bajas tasas de regreso de los pichones de aves playeras pueden deberse a mortalidad post-eclosión si las tasas de supervivencia aparente son menores en los pichones que en los volantones y adultos, y si estos dos últimos tienen tasas de supervivencia similares. No estuvimos en capacidad de distinguir entre mortalidad y dispersión debido a que la supervivencia aparente fue mínima en los pichones (ϕ̂1 = 0.08) y subsecuentemente mayor en volantones (ϕ̂1 = 0.15), en adultos luego de ser marcados (ϕ̂1 = 0.59) y en adultos en intervalos posteriores (ϕ̂2+ = 0.64). Los modelos basados en el tiempo transcurrido desde el marcado arrojaron mejores estimados de la supervivencia aparente de los adultos. Estos estimados fueron mayores que las tasas de regreso estimadas para otras poblaciones de C. alexandrinus, pero menores que la supervivencia aparente estimada para otras especies de Charadrius. Las oportunidades de apareamiento sesgadas de acuerdo al sexo observadas en C. alexandrinus no se explicaron por cocientes de sexos sesgados al momento de la eclosión, ni por diferencias en la supervivencia aparente de individuos adultos. En cambio, los cocientes de sexos sesgados hacia los machos evidentes en los adultos se explicaron en parte por diferencias en la supervivencia de los juveniles y por tasas de encuentro mayores entre machos adultos (p̂ = 0.84) en comparación con las hembras (p̂ = 0.74). Nuestros estimados de la supervivencia aparente representan una base que contribuirá a examinar la viabilidad de las poblaciones de C. alexandrinus a través de su rango de distribución.

Using a transponder system to monitor incubation routines of Snowy Plovers

Abstract We investigated the incubation behavior of a ground-nesting shorebird, the Snowy Plover (Charadrius a. alexandrinus) by developing a transponder system that recorded the identity of parents on their nest over 24 h. The system consisted of a small chip glued on the tail of the parent, an antenna that was buried under the nest, and a recording device that was buried nearby. The transponder system was both accurate and reliable, since only 0.2% of records were false. The records of the transponder system were augmented by visual observations, and these data were analyzed by randomization tests. We found strong daily incubation routines: females incubated during the day, whereas males incubated mostly at night. Overall, the females spent significantly more time incubating the nest (11.3 h (median)/day) than the males (9.4 h/day). We discuss several hypotheses for the observed daily incubation routines of the sexes, and propose experimental studies to test these hypotheses.

Genetic mating system and timing of extra-pair fertilizations in the Kentish plover

It is still unclear why females in many bird species pursue extra-pair copulations. Current hypotheses focus mainly on indirect benefits such as obtaining particular “good genes” for their offspring or maximizing genetic compatibility between themselves and the father of their offspring. Supporting the latter, a recent study of shorebirds suggests that extra-pair matings may function to avoid the negative effects of genetic similarity between mates. Here, we further investigate genetic parentage in the Kentish plover, Charadrius alexandrinus, a shorebird with a highly variable social mating system. DNA fingerprinting revealed that most pairs were genetically monogamous: 7.9% of the broods (7/89) contained extra-pair young, comprising 3.9% of all chicks (9/229). These cases represented, however, three alternative reproductive behaviors: extra-pair paternity, quasi-parasitism (extra-pair maternity) and intraspecific brood parasitism. This is the first study showing the occurrence of all three behaviors in one shorebird species. We also found that extra-pair fertilizations (extra-pair paternity and quasi-parasitism) were more frequent later in the breeding season. There was no consistent relationship between genetic similarity of mates and laying date; the pattern, as well as the degree of genetic similarity, differed among breeding sites within the study population.

Unexpected diversity in socially synchronized rhythms of shorebirds

The behavioural rhythms of organisms are thought to be under strong selection, influenced by the rhythmicity of the environment. Such behavioural rhythms are well studied in isolated individuals under laboratory conditions, but free-living individuals have to temporally synchronize their activities with those of others, including potential mates, competitors, prey and predators. Individuals can temporally segregate their daily activities (for example, prey avoiding predators, subordinates avoiding dominants) or synchronize their activities (for example, group foraging, communal defence, pairs reproducing or caring for offspring). The behavioural rhythms that emerge from such social synchronization and the underlying evolutionary and ecological drivers that shape them remain poorly understood. Here we investigate these rhythms in the context of biparental care, a particularly sensitive phase of social synchronization where pair members potentially compromise their individual rhythms. Using data from 729 nests of 91 populations of 32 biparentally incubating shorebird species, where parents synchronize to achieve continuous coverage of developing eggs, we report remarkable within- and between-species diversity in incubation rhythms. Between species, the median length of one parent’s incubation bout varied from 1–19 h, whereas period length—the time in which a parent’s probability to incubate cycles once between its highest and lowest value—varied from 6–43 h. The length of incubation bouts was unrelated to variables reflecting energetic demands, but species relying on crypsis (the ability to avoid detection by other animals) had longer incubation bouts than those that are readily visible or who actively protect their nest against predators. Rhythms entrainable to the 24-h light–dark cycle were less prevalent at high latitudes and absent in 18 species. Our results indicate that even under similar environmental conditions and despite 24-h environmental cues, social synchronization can generate far more diverse behavioural rhythms than expected from studies of individuals in captivity. The risk of predation, not the risk of starvation, may be a key factor underlying the diversity in these rhythms.

High gene flow on a continental scale in the polyandrous Kentish plover Charadrius alexandrinus

Gene flow promotes genetic homogeneity of species in time and space. Gene flow can be modulated by sex‐biased dispersal that links population genetics to mating systems. We investigated the phylogeography of the widely distributed Kentish plover Charadrius alexandrinus. This small shorebird has a large breeding range spanning from Western Europe to Japan and exhibits an unusually flexible mating system with high female breeding dispersal. We analysed genetic structure and gene flow using a 427‐bp fragment of the mitochondrial (mtDNA) control region, 21 autosomal microsatellite markers and a Z microsatellite marker in 397 unrelated individuals from 21 locations. We found no structure or isolation‐by‐distance over the continental range. However, island populations had low genetic diversity and were moderately differentiated from mainland locations. Genetic differentiation based on autosomal markers was positively correlated with distance between mainland and each island. Comparisons of uniparentally and biparentally inherited markers were consistent with female‐biased gene flow. Maternally inherited mtDNA was less structured, whereas the Z‐chromosomal marker was more structured than autosomal microsatellites. Adult males were more related than females within genetic clusters. Taken together, our results suggest a prominent role for polyandrous females in maintaining genetic homogeneity across large geographic distances.

Persistence of an extreme male-biased adult sex ratio in a natural population of polyandrous bird

In a number of insects, fishes and birds, the conventional sex roles are reversed: males are the main care provider, whereas females focus on matings. The reversal of typical sex roles is an evolutionary puzzle, because it challenges the foundations of sex roles, sexual selection and parental investment theory. Recent theoretical models predict that biased parental care may be a response to biased adult sex ratios (ASRs). However, estimating ASR is challenging in natural populations, because males and females often have different detectabilities. Here, we use demographic modelling with field data from 2101 individuals, including 579 molecularly sexed offspring, to provide evidence that ASR is strongly male biased in a polyandrous bird with male‐biased care. The model predicts 6.1 times more adult males than females (ASR = 0.860, proportion of males) in the Kentish plover Charadrius alexandrinus. The extreme male bias is consistent between years and concordant with experimental results showing strongly biased mating opportunity towards females. Based on these results, we conjecture that parental sex‐role reversal may occur in populations that exhibit extreme male‐biased ASR.

Heterozygosity-fitness correlations of conserved microsatellite markers in Kentish plovers Charadrius alexandrinus

Heterozygosity‐fitness correlations (HFCs) are frequently used to examine the relationship between genetic diversity and fitness. Most studies have reported positive HFCs, although there is a strong bias towards investigating HFCs in genetically impoverished populations. We investigated HFCs in a large genetically diverse breeding population of Kentish plovers Charadrius alexandrinus in southern Turkey. This small shorebird exhibits highly variable mating and care systems, and it is becoming an ecological model species to understand breeding system evolution. Using 11 conserved and six anonymous microsatellite markers, we tested whether and how heterozygosity was associated with chick survival, tarsus and body mass growth controlling for nongenetic effects (chick sex, hatching date, length of biparental care and site quality) that influence survival and growth. There was no genome‐wide effect of heterozygosity on fitness, and we did not find any significant effects of heterozygosity on growth rates. However, two of the 11 conserved markers displayed an association with offspring survival: one marker showed a positive HFC, whereas the other marker showed a negative HFC. Heterozygosity at three further conserved loci showed significant interaction with nongenetic variables. In contrast, heterozygosity based on anonymous microsatellite loci was not associated with fitness or growth. Markers that were correlated with chick survival were not more likely to be located in exons or introns than other markers that lacked this association.