Publications

2017

Geary, B., S.M. Longest, K. Ottewell, S.M. Lantz, S.T. Walter, J. Karubian, and P.L. Leberg. 2017. “Genetic Structure of Brown Pelicans (Pelecanus Occidentalis) in the Northern Gulf of Mexico in the Context of Human Management and Disturbance.”. PLoS ONE, 12(10): 0185309.

Environmental disturbances, both natural and anthropogenic, have the capacity to substantially impact animal behavior and abundance, which can in turn influence patterns of genetic diversity and gene flow. However, little empirical information is available on the nature and degree of such changes due to the relative rarity of longitudinal genetic sampling of wild populations at appropriate intervals. Addressing this knowledge gap is therefore of interest to evolutionary biologists, policy makers, and managers. In the past half century, populations of the brown pelican (Pelecanus occidentalis) in the southeastern United States have been exposed to regional extirpations, translocations, colony losses, and oil spills, but potential impacts on genetic diversity and population structure remain unknown. To investigate the cumulative impacts of recent disturbances and management actions, we analyzed seven microsatellite loci using genetic samples collected from 540 nestlings across twelve pelican colonies from two time periods, corresponding to before (n = 305) and after (n = 235) the 2010 Deepwater Horizon oil spill. Pre-2010 populations in Texas were significantly differentiated from Louisiana, Alabama, and Florida populations to the east, with reintroduced populations in southeastern Louisiana having less genetic diversity than sites in Texas, consistent with a recent bottleneck. In contrast, there was no evidence of a geographic component to genetic structure among colonies sampled after the spill, consistent with increased dispersal among sites following the event. This pattern may be associated with reduced philopatry in response to colony abandonment in the areas most heavily impacted by the Deepwater Horizon event, though other factors (e.g., rehabilitation and translocation of oiled birds or colony loss due to erosion and tropical storms) were likely also involved. Future monitoring is necessary to determine if bottlenecks and loss of genetic variation are associated with the oil spill over time, and is recommended for other systems in which disturbance effects may be inferred via repeated genetic sampling.

Botsch, J.C, S.T. Walter, J. Karubian, N. González, E. Dobbs, and B.J. Brosi. 2017. “Impacts of Forest Fragmentation on Orchid Bee Diversity (Hymenoptera: Apidae: Euglossini) in the Chocó Biodiversity Hotspot of Northwest Ecuador”. Journal of Insect Conservation, 21:633-643.

Habitat loss is a major driver of bee declines worldwide, and is of key relevance in the tropics given high deforestation rates, but we continue to have a poor understanding of the impact of land-cover change on tropical bee communities. Orchid bees (Apidae: Euglossini) are critical long-distance pollinators and may be highly susceptible to forest fragmentation given their reliance on forest habitat. Previous studies on the impact of forest fragmentation on euglossines have been geographically limited, have largely ignored β-diversity, and have not compared fragments with continuous forest. To contribute to addressing these gaps, we sampled male euglossine bees in 18 forest fragments (area range: 2.5–33 ha) and at eight locations within a large (3500 ha) continuous forest in the Chocó biodiversity hotspot of Ecuador during the dry season in 2014. We assessed how euglossine abundance, richness, and evenness related to fragment area, isolation, and edge:area ratio. We also compared fragments to continuous forest, in terms of α- and β-diversity. In fragments, a single species (Euglossa tridentata) comprised 78% of captures, and we found no significant effect of fragment area, isolation, or edge on abundance, richness, or evenness among fragments. Forest fragments and continuous forest differed in both community composition and evenness, but not in abundance or species richness. Spatial turnover (β-diversity) showed a non-significant trend toward changing more rapidly in continuous forest relative to fragments. These results underscore the conservation value of continuous forest for orchid bee diversity

Sexual ornaments, including plumage ornamentation, are often studied during breeding periods even though signal development can take place months earlier. This temporal disconnect potentially obscures the proximate mechanisms that underlie signal expression and development. We studied the correlation between androgen levels and expression of ornamented plumage in adult Red-backed Fairywrens (Malurus melanocephalus) 4–6 months before breeding, when signal production occurs in some, usually older, males. We found that, during this period, ornamented males, unornamented males and females all had low plasma androgen levels that did not differ from each other. Variation in androgen levels was unrelated to phenotype or moult. These findings differ from previous research conducted immediately prior to breeding in a different population of this species, which used correlative and experimental work to demonstrate that testosterone induces prenuptial moult and acquisition of ornamented plumage in younger males. Our study demonstrates that mechanisms contributing to signal production may vary within and among populations in relation to temporal, age-dependent, or geographic parameters. These results highlight the complexity of hormonal pathways to signal production, and the importance of studying signal acquisition throughout the entire period when signals are produced, as studies conducted at different time points may have quantitatively different results.

Albers, A.N., J.A. Jones, and L. Siefferman. 2017. “Behavioral Differences Among Eastern Bluebird Populations May Be a Consequence of Tree Swallow Presence: A Pilot Study”. Frontiers in Ecology and Evolution, 5:116.

Aggressive interference competition for limited resources is frequently observed among animals. However, these behavioral interactions within (intraspecific) and between (interspecific) species are costly as they can be energetically expensive and cause injury or death. To avoid these agonistic interactions, numerous species alter their behaviors and resource requirements. Spatial variation in nest site competition allows for investigation of concurrent variation in territorial defense behavior. Further, among species with bi-parental nest defense, behavioral similarity in territorial defense may benefit pairs. Here, we studied territorial aggression between two eastern bluebird (Sialia sialis) populations (North Carolina and Alabama, USA) that differ in avian community structure; those in North Carolina have recently begun to experience strong interspecific competition for nesting cavities by tree swallows (Tachycineta bicolor), a competitive pressure that is relatively new for North Carolina bluebirds (∼35–40 years) and is absent in Alabama populations. We found that bluebirds in North Carolina are more aggressive to simulated territorial intrusions compared to their Alabama counterparts. Behavioral similarity (here, in aggression) between partners is strong and similar in both populations. These results suggest that bluebirds in North Carolina may have to maintain higher baseline aggression during territory establishment and nest construction to co-occur with highly aggressive tree swallows, but that, in both populations, behavioral similarity between partners may be adaptive. Finally, we acknowledge the preliminary nature of this study and the need for expanding the behavioral studies to other sites in the southeastern United States. Greater regional coverage would exclude the possibility of alternative drivers of the observed behavioral differences between the North Carolina and Alabama populations.

E.D., Enbody, S.M. Lantz, and J. Karubian. 2017. “Production of Plumage Ornaments Among Males and Females of Two Closely Related Tropical Passerine Bird Species”. Ecology and Evolution, 7(11): 4024-4034.

The evolution of elaborate secondary sexual traits (i.e., ornaments) is well-studied in males but less so in females. Similarity in the appearance of ornaments between males and females supports the view that female ornaments arise as a neutral byproduct of selection on male traits due to genetic correlation between sexes, but recent research suggests an adaptive function of female ornaments in at least some contexts. Information on the degree to which production of ornaments differs between the sexes can shed light on these alternative perspectives. We therefore characterized the structural underpinnings of melanin-based plumage production in males and females of two closely related passerine bird species (genus Malurus). Importantly, both ornamented and unornamented phenotypes in each sex are present between these two species, providing an opportunity to test the null expectation of equivalent modes of production in male and female ornamented phenotypes. In Malurus alboscapulatus, ornamented females are qualitatively similar to males, but we describe a distinctive ornamented female phenotype that differs from that of males in lacking a blue sheen and in lower feather barbule density. In M. melanocephalus, unornamented males and females are also similar in appearance, and we describe a similarity between unornamented phenotypes of males and females in both color and underlying feather barbule structure and pigment composition. Unornamented male M. melanocephalus can flexibly transition to the ornamented phenotype in weeks, and we found extreme differences in color and feather structure between these two alternative male phenotypes. These results contradict the idea that female ornaments have evolved in this system following a simple switch to male-like plumage by demonstrating greater complexity in the production of the ornamented phenotype in males than in females.

Iverson, E.N.K., and J. Karubian. 2017. “The Role of Bare Parts in Avian Signaling”. Auk, 134.

Avian plumage has captivated scientists and the public alike for generations and has been a fundamental study system for research into signal evolution. By contrast, relatively little attention has been paid to avian bare parts such as exposed skin, bills, feet, and combs, despite considerable variation in structure and coloration within and between species. To better understand the potential signaling role of bare parts, we conducted a comprehensive literature search that returned 321 published studies. In reviewing these studies, we found that (1) bare-part color is widely distributed taxonomically and is produced by diverse mechanisms; (2) many bare parts are likely to be dynamic, honest signals of current condition or status and can also reflect genetic makeup and early developmental conditions; and (3) bare parts can function as pluripotent social signals, mediating interactions between competitors, mates, and kin. Differences between bare parts and plumage in phenology and information content support a multiple-messages interpretation of their respective signaling roles, in that bare parts may contain information that is complementary to, but distinctive from, information conveyed by plumage-based signals. We consider it likely that a great deal of barepart variation is ‘‘hidden in plain sight,’’ in that meaningful variation may not be recorded by many current studies. We urge more careful and extensive characterization of bare-part coloration in a wider range of species because of its potential to advance our understanding of signal function and constraints, with particular reference to the role of dynamic color signals and the evolution of multiple ornamentation.

Lantz, S.M., J. Boersma, H. Schwabl, and J. Karubian. 2017. “Early-Moulting Red-Backed Fairywrens Males Acquire Ornamented Plumage in the Absence of Elevated Androgens”. Emu.

Sexual ornaments, including plumage ornamentation, are often studied during breeding periods even though signal development can take place months earlier. This temporal disconnect potentially obscures the proximate mechanisms that underlie signal expression and development. We studied the correlation between androgen levels and expression of ornamented plumage in adult Red-backed Fairywrens (Malurus melanocephalus) 4–6 months before breeding, when signal production occurs in some, usually older, males. We found that, during this period, ornamented males, unornamented males and females all had low plasma androgen levels that did not differ from each other. Variation in androgen levels was unrelated to phenotype or moult. These findings differ from previous research conducted immediately prior to breeding in a different population of this species, which used correlative and experimental work to demonstrate that testosterone induces prenuptial moult and acquisition of ornamented plumage in younger males. Our study demonstrates that mechanisms contributing to signal production may vary within and among populations in relation to temporal, age-dependent, or geographic parameters. These results highlight the complexity of hormonal pathways to signal production, and the importance of studying signal acquisition throughout the entire period when signals are produced, as studies conducted at different time points may have quantitatively different results

McNeil, D.J., K.R. Aldinger, M.H. Bakermans, A.C. Tisdale, J.A. Jones, P.B. Wood, D.A. Buehler, C.G. Smalling, L. Siefferman, and J.L. Larkin. 2017. “An Evaluation and Comparison of Conservation Guidelines for an At-Risk Migratory Songbird”. Global Ecology and Conservation, 9: 90-103.

For at-risk wildlife species, it is important to consider conservation within the process of adaptive management. Golden-winged Warblers (Vermivora chrysoptera) are Neotropical migratory songbirds that are experiencing long-term population declines due in part to the loss of early-successional nesting habitat. Recently-developed Golden-winged Warbler habitat management guidelines are being implemented by USDA: Natural Resource Conservation Service (2014) and its partners through the Working Lands For Wildlife (WLFW) program. During 2012–2014, we studied the nesting ecology of Golden-winged Warblers in managed habitats of the eastern US that conformed to WLFW conservation practices. We evaluated five NRCS ‘‘management scenarios’’ with respect to nesting success and attainment of recommended nest site vegetation conditions outlined in the Golden-winged Warbler breeding habitat guidelines. Using estimates of territory density, pairing rate, nest survival, and clutch size, we also estimated fledgling productivity (number of fledglings/ha) for each management scenario. In general, Golden-winged Warbler nest survival declined as each breeding season advanced, but nest survival was similar across management scenarios. Within each management scenario, vegetation variables had little influence on nest survival. Still, percent Rubus cover and density of >2 m tall shrubs were relevant in some management scenarios. All five management scenarios rarely attained recommended levels of nest site vegetation conditions for Golden-winged, yet nest survival was high. Fledgling productivity estimates for each management scenario ranged from 2.1 to 8.6 fledglings/10 hectares. Our results indicate that targeted habitat management for Goldenwinged Warblers using a variety of management techniques on private lands has the capability to yield high nest survival and fledgling productivity, and thus have the potential to contribute to the species recovery

Jones, J.A., A.C. Tisdale, M.H. Bakermans, J.L. Larkin, C.G. Smalling, and L. Siefferman. 2017. “Multiple Plumage Ornaments As Signals of Intrasexual Communication in Golden-Winged Warblers”. Ethology, 123:145-156.

Avian plumage represents some of the greatest diversity in integument coloration of all animals. Plumage signals are diverse in function, including those that allow for assessing potential mates or the mitigation of agonistic interactions between rivals. Many bird species possess multiple ornamental traits that have the potential to serve as multiple or redundant signals. For example, male golden-winged warblers (Vermivora chrysoptera) have brilliant carotenoid-based yellow crowns, melanin-based black throats, and structurally based white patches on their outer tail feathers. Using a correlative approach, we investigated whether plumage ornaments have the potential to reliably signal ability to acquire higher quality territory, aggressive response to simulated territorial intrusions, and reproductive success. We found that both crown chroma and tail brightness were significantly related to habitat quality and aggression; more ornamented birds held territories with higher quality habitat and were less aggressive toward simulated conspecific stimuli. Older birds sang less threatening songs than younger birds and were more likely to sing their mate attraction song type (type 1) rather than songs typically reserved for agonistic interactions (type 2). Finally, despite our previous research demonstrating that habitat strongly predicts reproductive success in this warbler population, we found no evidence of a direct link between ornamentation and reproductive success. Overall, these data suggest that younger males, and those with lower quality ornaments, compensate with more aggressive behaviors. Additional research is needed to investigate the dynamics between behavioral traits and ornaments to better understand complex signaling and how golden wing signals function in conspecific interactions (male–male interactions and mate-choice).

2016

Hazlehurst, J., B. Tinoco, S. Cardenas, and J. Karubian. 2016. “Pollination Ecology of Oreocallis Grandiflora (Proteaceae) at the Northern and Southern Ends of Its Geographic Range”. Journal of Pollination Ecology, 19:71-80.

Geographic variation in pollination ecology is poorly documented, if at all, in many plant-pollinator systems. Great insights could be gained into the abiotic and biotic factors which impact the evolution of floral properties and their potential to lead to speciation by doing so, as both can vary naturally over the geographic range of a plant species. We characterized the pollination ecology of the Andean tree Oreocallis grandiflora (Family: Proteaceae) at the northern and southern ends of its range in Ecuador and Peru in terms of flower morphology, nectar properties, pollinators and plant reproduction. We found significant divergence in the two populations in terms of style length and flower openness, nectar standing crop and secretion rate, and pollinator community. We did not find a significant difference in the length of the pollen presenter or in nectar sucrose concentration by weight (% Brix). The observed divergence in floral traits between the two study populations may be related to a combination of factors, including genetic drift and isolation by distance, distinctive suites of pollinators, or heterospecific pollen competition, which future studies should further investigate. This study demonstrates that pollination ecology can vary substantially across the geographic range of a species, with implications for delimiting species and subspecific taxa.