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Wednesday, 20 April 2016

The Auk. April 2016: Volume 133, Issue 2

The Auk

Published by: The American Ornithologists' Union

Apr 2016 : Volume , 133 Issue 2 


Comment on Jukema et al. (2015), “Geographic variation in morphometrics, molt, and migration suggests ongoing subspeciation in Pacific Golden-Plovers (Pluvialis fulva)”
Alice Cibois and Frederick H. Sheldon

Jukema and colleagues published in The Auk a study dealing with geographic variation within the Pacific Golden-Plover (Pluvialis fulva). We highlight a taxonomic problem created unwittingly by the last sentence of their article, in which the authors suggest a new name for the Siberian population.


Darker eggshell spotting indicates lower yolk antioxidant level and poorer female quality in the Eurasian Great Tit (Parus major) 
Rita Hargitai, Gergely Nagy, Márton Herényi, Zoltán Nyiri, Miklós Laczi, Gergely Hegyi, Zsuzsanna Eke and János Török

Protoporphyrin pigment causes the red-brown eggshell colors; however, for many species, the function of this pigment is unknown. It has been proposed that eggshell pigmentation may strengthen the shell or that it may be a sexually selected signal, which advertises the quality of the female and that of her offspring to the male parent. In this study, we aimed to discover whether protoporphyrin-based eggshell pigmentation patterns of Eurasian Great Tits (Parus major) were related to female or egg quality. Additionally, we tested whether different methods of eggshell pigmentation estimation could be reliable predictors of eggshell protoporphyrin levels. We found that spot intensity, spot size, spotting coverage, and brown spot chroma indicated the protoporphyrin pigment concentration of the eggshell. Our results revealed that Eurasian Great Tit females that laid eggs with darker pigmentation had more lymphocytes in their circulation and had paler yellow breast and lower UV plumage reflectance, possibly indicating poorer health and individual quality. However, we did not find evidence that eggshell pigmentation patterns indicated the body condition, body size, or plasma oxidative status of females. Furthermore, we found that eggs with darker spots contained lower concentrations of antioxidants in the yolk. High protoporphyrin levels may be detrimental to females as they may cause oxidative damage, and this may be why birds that laid eggs with darker spots deposited lower amounts of antioxidants into the egg yolk. Shell spot darkness may also indicate territory quality, as females that laid smaller clutches also laid eggs with higher eggshell pigmentation levels. Thus, our results suggest that shell spot darkness may indicate the state of health of the female, egg yolk antioxidant level, and possibly also the quality of the territory.

Nondestructive Raman spectroscopy confirms carotenoid-pigmented plumage in the Pink-headed Duck
Daniel B. Thomas and Helen F. James

A small group of pigment classes is responsible for the wide range of plumage colors in modern birds. Yellow, pink, and other “warm” feather colors of many species are attributed to carotenoid pigments, a plumage trait that has an uneven distribution across modern bird species. Carotenoid plumage pigments are especially rare among fowl (superorder Galloanseres), and until recently, the Pink-eared Duck (Malacorhynchus membranaceus) from Australia provided the only evidence that any species of waterfowl (order Anseriformes) exhibits carotenoid-pigmented plumage. We analyzed a Pink-headed Duck (Rhodonessa caryophyllacea) study skin using Raman spectroscopy, without plucking or otherwise damaging the specimen. Raman spectra confirmed that the pink feathers of Rhodonessa are pigmented with carotenoids. Spectra from Rhodonessa were similar to those from Malacorhynchus, which suggests that the same carotenoid is the primary plumage pigment in both species. Moreover, spectra from Rhodonessa were similar to spectra from other taxa pigmented with ketocarotenoids. Malacorhynchus and Rhodonessa are distant relatives within Anseriformes, so these findings indicate multiple evolutionary origins of plumage carotenoids within the waterfowl or (less likely) many losses of plumage carotenoids from duck species. Our results show that pigment chemistry can be studied in precious ornithological specimens without damaging the specimens, and provide new evidence that the (apparently extinct) Rhodonessa possessed what is evolutionarily an extremely rare trait among waterfowl.

Isolation and characterization of bacteria from the feathers of wild Dark-eyed Juncos (Junco hyemalis)
John W. Dille, Christopher M. Rogers and Mark A. Schneegurt

We dislodged microbes from samples of composites of ventral feathers from different birds of overwintering Dark-eyed Juncos (Junco hyemalis) after mist-net capture in south-central Kansas, USA. Bacterial loads were measured by standard plate counts and >300 isolates were purified by repetitive streak-plating on R2A medium (+ cycloheximide). Biochemical and physiological characterization included identification by 16S rRNA gene phylogeny. Nearly half of the isolates grew on keratin and 80% exhibited lipase activity, suggesting that these isolates can degrade feathers and thus may affect survival and reproduction. Individual bacterial loads from 8 juncos varied within a 3-fold range, 105–106 colony-forming units g−1 feather. At 97% DNA sequence identity (species-level), 63 operational taxonomic units were detected among 202 sequences; the Chao1 estimate was 123. The Shannon diversity index (H; 97% identity) was 3.75, Simpson's diversity index (1/D) was 16.1, and Good's coverage was 82.4. Gram-positive bacteria dominated the culture collection, balanced between low and high G+C clades. Bacillus spp. were abundant, including B. asahii, B. cereus, B. megaterium, and B. pumilus. Lysinibacillus, Paenibacillus, and Staphylococcus also were isolated. Remarkably, substantial numbers of Actinomycetes were isolated, including representatives of Clavibacter, Curtobacterium, Microbacterium, and Rathayibacter, genera recognized as being populated by xylem-filling crop plant pathogens. Apposed to these were feather isolates implicated as beneficial to host plants, Frigoribacterium and Kitasatospora, being antagonists to plant pathogens or acting as plant growth promoters. High G+C Gram-positive bacterial isolates included Blastococcus, Cellulomonas, Humicoccus, Nocardioides, Promicromonospora, and Rhodococcus. Proteobacteria dominated the Gram-negative bacteria, with Alphaproteobacteria most abundant, including the potential plant pathogens Agrobacterium and Sphingomonas, and the oligotrophs Aurantimonas, Brevundimonas, Methylobacterium, Rhizobium, and Rhodobacter. Gammaproteobacteria included Pantoea, Pseudomonas, and Stenotrophomonas. Ours is the first report of abundant helpful and harmful phyllosphere bacteria on wild bird feathers. The clear implication is that free-living migratory birds may carry bacteria throughout their geographic ranges and may transmit pathogens and beneficial bacteria to plants.

Diet reconstruction using next-generation sequencing increases the known ecosystem usage by a shorebird
Travis G. Gerwing, Jin-Hong Kim, Diana J. Hamilton, Myriam A. Barbeau and Jason A. Addison

Molecular scatology and next-generation sequencing identified previously unknown linkages among ecosystems in the diet of Semipalmated Sandpipers (Calidris pusilla) in the Bay of Fundy, Canada. During their annual migratory stopover, the birds consumed a wider range of prey items than previously reported, which suggests that they are not selecting for the amphipod Corophium volutator and are acting as generalist foragers. Our analysis identified several novel prey items—arachnids, crabs, bivalves, several terrestrial and freshwater insect species, ctenophores, cnidarians, and fish (likely eggs or juveniles)—indicating that Semipalmated Sandpipers consume prey from marine, freshwater, and terrestrial ecosystems. Connections between Semipalmated Sandpipers and freshwater and terrestrial ecosystems were previously unknown in the Bay of Fundy. Current conservation efforts for this species are focused on beach and intertidal habitats; however, we may also need to consider the surrounding freshwater and terrestrial habitat.

Dietary divergence in the most sexually size-dimorphic bird
Carolina Bravo, Carlos Ponce, Luis M. Bautista and Juan C. Alonso

In sexually size-dimorphic species, physiological constraints derived from differences in body size may determine different food requirements and thus a trophic niche divergence between males and females. These relationships between sexual size dimorphism (SSD) and dietary overlap are not well understood in birds. We analyzed differences between the sexes in diet composition, dietary diversity, diet selection, and volume and density of droppings, as well as the dietary overlap between sexes, in the Great Bustard (Otis tarda), the species showing the highest SSD among birds. We discuss the differences that we found in relation to various predictions derived from ecological and physiological differences between the sexes, under the hypothesis that these differences are ultimately determined by the strong SSD of this species. As expected, our best linear mixed-effects food selection models included sex as a main factor explaining differences in diet composition and dietary diversity of Great Bustards throughout the annual cycle. Both sexes were mostly herbivorous, consuming legumes when they were available. Males consumed fewer arthropods, but of significantly larger size, than females. The droppings of males were larger, heavier, and slightly denser than those of females. Males showed higher dietary diversity than females, except during the postmating season. The mean dietary overlap between the sexes was 0.7, one of the smallest values among birds. Overall, our results suggest that the species' extreme SSD along with the distinct reproductive role of each sex might explain the trophic niche divergence in the Great Bustard.

Nest size is not closely related to breeding success in Blue Tits: A long-term nest-box study in a Mediterranean oak habitat
Marcel M. Lambrechts, Pascal Marrot, Amélie Fargevieille, Pablo Giovannini, Annick Lucas, Virginie Demeyrier, Afiwa Midamegbe, Philippe Perret, Arnaud Grégoire, Anne Charmantier and Claire Doutrelant

Various components of breeding success are predicted to be related to avian nest size because (1) some individuals are physically able to build larger nests than other individuals or (2) larger nests provide more protection in the absence of predation than smaller nests. The results of an 18-yr correlative nest-box study in Blue Tits (Cyanistes caeruleus) show that nest size is not closely related to components that reflect breeding performance, after controlling for other female characteristics (first-egg date, clutch size, and female age) assumed to influence breeding performance in long-term studies. Our results support those of most short-term field studies that have reported weak associations between nest size and breeding performance in cavity-nesting passerines. We suggest that the absence of an association between nest size and breeding performance can be explained by the fact that the vast majority of nest-box studies have used small nest chambers that imposed physical constraints on the full expression of the nest. We recommend using a larger range of nest-chamber sizes that better reflect the characteristics of natural holes exploited by secondary cavity-nesting species.

Wing size-related reed habitat selection by Great Reed Warbler (Acrocephalus arundinaceus) males
Thomas Oliver Mérő, Antun Žuljević, Katalin Varga and Szabolcs Lengyel

In this study we explored the linkage between wing size of Great Reed Warbler males (Acrocephalus arundinaceus) and their habitat selection and relate these linkages to differences in reed habitat quality. We measured the wing sizes of males nesting in 6 different reed habitats. To explain reed habitat selection, we modeled male wing size as a function of 7 predictor variables describing reedbeds: proportion of managed reed; densities of mixed, old, and fresh reed; reed stem diameter; water depth; and fluctuation of water level. Mean wing size was greatest for males at large canals, intermediate at mining ponds and smaller canals, and lowest at marshes and very small canals. The proportion of managed reed and fluctuation of water level were negatively related to wing size, and water depth was positively related to wing size, which suggests that males with larger wings preferred reed habitats with little management in deep water with little fluctuation in water level. We concluded that the availability of stable, deep water and lack of management are primarily important in attracting larger-winged (presumably dominant) males.

How connectivity shapes genetic structure during range expansion: Insights from the Virginia's Warbler
Christine M. Bubac and Garth M. Spellman

Species range expansions facilitated by global climate change have been documented across many taxa. The ecological and evolutionary costs of range expansion in response to climate change are beginning to be teased apart, and have the potential to be strikingly different among taxa experiencing different types of range expansion across highly variable landscapes. We investigated how population expansion and connectivity have affected genetic diversity in the Virginia's Warbler (Oreothlypis virginiae), a recent colonist of the Black Hills of South Dakota, USA. To investigate population connectivity, we sampled Virginia's Warbler across their breeding range. Genetic data from the mtDNA NADH dehydrogenase subunit 2 (ND2) gene and 7 polymorphic microsatellite loci were used to characterize structure within and among populations and to investigate genetic variability associated with connectivity. The analyses suggested little genetic differentiation, minimal population structure, and similar mtDNA haplotype and nuclear heterozygosity diversities throughout all 7 of the sampled regions. Results from Tajima's D and Fu's FS neutrality tests and a starburst haplotype network indicated a demographic expansion similar to what would be expected in a species that underwent historical range expansion following the last glacial maximum. This study demonstrates that range expansion with recurring gene flow can curtail the loss of genetic diversity and prevent significant differentiation in newly colonized areas.

Association between nest defense and egg rejection behavior of Brown-breasted Bulbuls (Pycnonotus xanthorrhous)
Tongping Su, Canchao Yang, Guoxian Liang, Changqing Ding and Wei Liang

Different lines of host defense against parasites may be antagonistic or have additive benefits. For example, nest defense and egg rejection behaviors are important adaptations against brood parasitism in hosts that have been subject to much attention and numerous studies. However, the relationship between these 2 defensive behaviors within a single host population has hardly been elucidated. We investigated the correlation between nest defense and egg recognition behavior in Brown-breasted Bulbuls (Pycnonotus xanthorrhous) by conducting dummy and artificial-parasitism experiments. Our results illustrate that in Brown-breasted Bulbuls, rejecters of parasite eggs were more aggressive toward a cuckoo dummy than acceptors, which was opposite to the results of a previous study. We discuss the possible explanations for consistent and antagonistic defenses at the individual level of hosts and suggest that accumulated experience, sufficient to recognize harmful objects, may account for our results in Brown-breasted Bulbuls.


Stopover biology of Ruby-throated Hummingbirds (Archilochus colubris) during autumn migration
Theodore J. Zenzal Jr. and Frank R. Moore

Surprisingly little is known about the migration and stopover biology of Ruby-throated Hummingbirds (Archilochus colubris), and even less is known about their sex- or age-dependent migration. First, we provide basic information on the migration and stopover biology of this species along the northern coast of the Gulf of Mexico during autumn, including phenology, stopover duration, fuel deposition rate (FDR), arrival mass, and estimated flight ranges. Second, we investigate whether these stopover variables are influenced by age or sex. Age-dependent migration is expected because young, hatch-year birds on their first migration lack the experience of older individuals. Sex-dependent migration is expected because of sexually dimorphic characteristics in wing morphology and body size. We obtained information on arrival mass, phenology, FDR, stopover duration, and estimated flight ranges through banding data, passive integrated transponder tags, radio telemetry, and color marking at a long-term migration station along the northern coast of the Gulf of Mexico. Our data provide strong evidence for age-dependent migration and only weak evidence for sex-dependent migration. Older birds arrived earlier, had larger fuel loads, and had shorter stopover durations than younger birds. In younger birds, we found no effect of sex on FDR, arrival mass, stopover duration, or phenology. Older males arrived with larger fuel loads than females. Finally, we used flight simulation software and our data to estimate that males and older birds were capable of longer potential flight ranges than either females or younger birds.

Individual quality and double-brooding in a highly synchronous songbird population
Allison Cornell and Tony D. Williams

Multiple brooding, the production of more than one set of offspring per breeding season, is a life-history trait that potentially doubles or triples fecundity, but the factors responsible for variation in the occurrence of multiple brooding within species remain poorly understood. We investigated the potential causes and consequences of double-brooding in the highly synchronously breeding European Starling (Sturnus vulgaris), for which we predicted that clutch initiation date would have little effect on double-brooding propensity compared with individual quality. Double-brooding effectively doubled annual fecundity in European Starlings (based on the annual number of chicks fledged), but on average only 38% of individual females had a second brood. Furthermore, 39% of females that initiated a second clutch experienced total failure of their second brood, and thus accrued no advantage in fecundity from their decision to double-brood. As we predicted, variation in the propensity for, and success of, double-brooding was independent of laying date, but also of other putative measures of individual quality (clutch size, egg mass, relative female age, and nestling provisioning rate). However, we found no evidence of a cost of double-brooding; females that double-brooded had significantly higher return rates and similar breeding productivity in the year after double-brooding compared with single-brooding females. Thus, a small proportion (~20%) of ‘high-quality' female European Starlings effectively double their potential breeding productivity through double-brooding without apparently paying a cost or experiencing any simple tradeoffs.

Nestling growth rates in relation to food abundance and weather in the Arctic
Jonathan H. Pérez, Jesse S. Krause, Helen E. Chmura, Shae Bowman, Michaela McGuigan, Ashley L. Asmus, Simone L. Meddle, Kathleen E. Hunt, Laura Gough, Natalie T. Boelman and John C. Wingfield

Raising nestlings to fledging is energetically demanding for songbirds, requiring parents to balance several major tradeoffs. Nestling growth rates are highly susceptible to variation in environmental conditions and parental investment, and highly variable environments with short breeding seasons such as the Arctic magnify these tradeoffs. Arctic-nesting passerines provide a good model system in which to explore variation within and between species in growth rates with regard to environmental conditions and the timing of clutch initiation. Here we investigated interannual and interspecies variation in nestling mass gain for 2 species of Arctic-breeding passerine, Gambel's White-crowned Sparrow (Zonotrichia leucophrys gambelii) and Lapland Longspur (Calcarius lapponicus), across 2 years. The nestling period of 2014 was both colder (with lower minimum and maximum temperatures) and wetter (with 73% more rainfall) than 2013. Arthropod biomass was also reduced in shrub tundra in 2014 compared to 2013. Both species showed reductions in rate of daily mass gain of nestlings in 2014 compared to 2013, but we observed no significant difference between species. Furthermore, we found that in 2014 early nesting birds had higher rates of nestling growth than those initiating clutches later in the season. These findings suggest that overall environmental conditions were more challenging for raising nestlings in 2014 compared to 2013 and that these differences were manifested in a reduced rate of nestling mass gain in both species. Furthermore, both species showed a negative correlation between precipitation and growth rates, whereas only Lapland Longspur showed a positive correlation between growth rates and temperature.

Vocal imitation of mother's calls by begging Red-backed Fairywren nestlings increases parental provisioning
Diane Colombelli-Négrel, Michael S. Webster, Jenélle L. Dowling, Mark E. Hauber and Sonia Kleindorfer

Prenatal imitative learning is an emerging research area in both human and non-human animals. Previous studies in Superb Fairywrens (Malurus cyaneus) showed that mothers are vocal tutors to their embryos and that better imitation of maternal calls yields more parental provisions after hatching. To begin to test if such adaptive behavior is widespread amongst Australasian wrens in Maluridae, we investigated maternal in-nest calling patterns in Red-backed Fairywrens (Malurus melanocephalus). We first compared the structure of maternal and nestling call elements. Next, we examined how in-nest calling behavior varied with parental behaviors and ecological contexts (i.e. prevalence of brood parasitism and nest predation). All Red-backed Fairywren females called to their eggs during incubation and they continued to do so for several days after hatching at a lower rate. Embryos that received more calls per hour during the incubation period (but not the nestling period) developed into hatchlings with higher call element similarity between mother and young. Female call rate was mostly independent of nest predation but in years with more interspecific brood parasitism, nestling element similarity was greater and female call rates tended to be higher. Playback experiments showed that broods with higher element similarity to their mother received more successful feeds. The potential for prenatal tutoring and imitative begging calls in 2 related fairywren taxa sets the stage for a full-scale comparative analysis of the evolution and function of these behaviors across Maluridae and in other vocal-learning lineages.

Subtle benefits of cooperation to breeding males of the Red-backed Fairywren
Ahva L. Potticary, Jenélle L. Dowling, Douglas G. Barron, Daniel T. Baldassarre and Michael S. Webster

Cooperative breeding is a phenomenon whereby breeding and nonbreeding individuals collectively provision young. Nonbreeding group members (“helpers”) may gain indirect and/or direct fitness benefits by breeding in a group, but there has been conflicting evidence regarding the benefits to breeders. In fact, the presence of helpers may sometimes be detrimental to aspects of breeder fitness. For example, in some species of the chiefly Australian genus Malurus, breeding males with helpers have lower within-pair paternity than do males without helpers. Additionally, indirect benefits to breeding males are often limited by low relatedness to their helpers due to high extrapair paternity rates, and helpers often appear to have minimal impact on breeder reproductive success. However, the presence of helpers may allow breeding males to shift their behaviors from guarding and provisioning young to alternative behaviors that affect other components of fitness, such as extraterritory forays (which might increase extrapair mating success) and self-maintenance (which might increase survival). We investigated these possibilities in the facultatively cooperative Red-backed Fairywren (Malurus melanocephalus). Males with helpers spent significantly less time engaging in guarding behaviors and provisioning of young than did those without helpers, but there was no difference in the frequency of extrapair forays nor the number of young sired by males with vs. without helpers. Additionally, the decreased investment in nesting behaviors did not result in consistently higher survival, but may have increased survival in some years. Overall, the results of this study did not suggest any strong direct fitness benefits to breeding males, which may indicate that the costs of retaining helpers are negligible relative to the indirect benefits of helping a potentially related male.

Opportunistic conspecific brood parasitism in a box-nesting population of Prothonotary Warblers (Protonotaria citrea)
Anna M. Tucker, Rodney J. Dyer, Sarah K. Huber and Lesley P. Bulluck

Conspecific brood parasitism (CBP), although prevalent in some avian taxa, is easily overlooked when it occurs in low frequencies, and therefore the ecology of this behavior has only occasionally been described in passerines. We describe the occurrence of CBP in a population of Prothonotary Warblers (Protonotaria citrea) breeding in nest boxes, demonstrate associated fitness costs, and investigate parasite strategy. We genotyped individuals at 6 microsatellite loci and used Cervus software to determine log-likelihood of maternity (LOD scores) for offspring and social mothers. We set critical cutoff LOD scores at 95% confidence for exclusion of the social mother and assignment of a parasite mother from the breeding population. Of 805 nestlings (233 family groups during 2009–2013), we found that 12.7% had genotypes that were incompatible with their social mother. Females with unrelated nestlings (hosts) fledged fewer biological offspring within the host year than nonhost females despite fledging more total offspring, but being a host was not significantly associated with total reproductive success over 5 yr of breeding. We were able to identify only ∼30% of parasite females, which suggests that the majority of parasites may be floaters (i.e. non-nesters) in the population or nesting in nearby natural cavities. We found no evidence of host selection based on host age, arrival at the breeding site, or nest-box productivity in the previous year. This opportunistic behavior is likely facilitated by the nesting ecology of this population, in that nest sites are limited, conspicuous, and relatively dense. Future studies investigating CBP in populations using natural cavities can help elucidate the drivers of this behavior.

Red-crested Cardinals use color and width as cues to reject Shiny Cowbird eggs
Luciano N. Segura, Facundo G. Di Sallo, Bettina Mahler and Juan C. Reboreda

As part of the coevolutionary process between brood parasites and their hosts, the latter have developed different strategies to discriminate and reject parasitic eggs. This recognition–rejection process is the primary host defense against costly brood parasitism. The Red-crested Cardinal (Paroaria coronata) is an occasional host of the generalist Shiny Cowbird (Molothrus bonariensis) that successfully rejects all parasitic eggs. We studied the cues used by Red-crested Cardinals to recognize and reject foreign eggs by experimentally adding real parasite and host eggs painted as mimetic or nonmimetic of host eggs and analyzing whether eggshell coloration and/or shape were used as cues for egg rejection. Rejection rates, mostly through egg ejection, were high for all nonmimetic eggs (95% for unpainted cowbird eggs and 100% for painted nonmimetic cowbird and host eggs). On the contrary, they were low for mimetic host eggs (6% for unpainted host eggs and 20% for painted mimetic host eggs), but intermediate for painted mimetic cowbird eggs (55%). We also found that egg width significantly affected the probability of rejection, with wider parasitic eggs (i.e. more different from host eggs) more frequently rejected. We report for the first time that egg width is an important cue for recognition and ejection of cowbird eggs in an open-cup-nesting host. Our results show that coloration is a reliable cue used by Red-crested Cardinals to discriminate and reject parasitic eggs, but when coloration alone does not allow discrimination of foreign eggs, this host uses egg width as an additional cue.

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