Publications

2016

Karubian, J., and L. Browne. 2016. “Negative Frequency-Dependent Selection for Rare Genotypes Promotes Genetic Diversity of a Tropical Palm.”. Ecology Letters, 19:1439-1447.

Negative frequency-dependent selection among species is a key driver of community diversity in natural systems, but the degree to which negative frequency-dependent selection shapes patterns of survival and genetic diversity within species is poorly understood. In a 5-year field experiment, we show that seedlings of a tropical palm with rare genotypes had a pronounced survival advantage over seedlings with common genotypes, with effect sizes comparable to that of light availability. This ‘rare genotype advantage’ led to an increase in population-wide genetic diversity among seedlings compared to null expectations, as predicted by negative frequency-dependent selection, and increased reproductive success in adult trees with rare genotypes. These results suggest that within-species negative frequency-dependent selection of genotypes can shape genetic variation on ecologically relevant timescales in natural systems and may be a key, overlooked source of non-random mortality for tropical plants.

Hazlehurst, J., and J. Karubian. 2016. “Nectar Robbing Impacts Pollinator Behavior But Not Plant Reproduction.”. Oikos.

Trait-mediated indirect eff ects (TMIEs) refer to interactions in which the eff ect of one species on another is mediated by the behavior of a third species. A mechanistic approach that identifi es the direction and impact of TMIEs can shed light on why diff erent net outcomes are observed in the same general phenomena across systems. Nectar robbing has variable net eff ects through TMIEs on animal-pollinated plants across systems, but the mechanistic steps underlying this range of outcomes are often unclear. To address this knowledge gap, we assessed linkages between nectar robbing, pollinator behavior and plant reproductive success in the Andean tree, Oreocallis grandifl ora . We found that robbing in this system led to lower nectar volumes, higher nectar sucrose concentration, and higher nectar viscosity, which together negatively impact nectar quality. Th is drop in nectar quality was associated with decreased visitation rates by hummingbirds, which might be expected to impact plant reproduction negatively by pollen limitation. However, it was also associated with increased diversity (Shannon ’ s) and evenness in the pollinator community due to reduced visitation by a territorial hummingbird, which might be expected to impact reproduction positively via enhanced genetic diversity of pollen as non-territorial pollinators forage over greater areas. We measured seed set and mass to distinguish the relative intensity of these two possible outcomes, but found no detectable eff ect. We tentatively conclude that these two consequences of TMIEs may have balanced each other out to yield a neutral net eff ect of nectar robbing on plant reproduction, though other explanations are also possible. Th is study highlights ways in which ecologically important TMIEs may act in opposing directions to mask important ecological forces, and underscores the continued need for detailed study of the mechanisms through which TMIEs operate.

Browne, L., and J. Karubian. 2016. “Diversity of Palm Communities at Different Spatial Scales in a Recently Fragmented Tropical Landscape.”. Botanical Journal of the Linnean Society, 182: 451-464.

Habitat loss and landscape fragmentation are often associated with changes in biological communities at different spatial scales. Our goal in this study was to identify fragment characteristics and environmental variables linked to palm species richness, abundance and community similarity at local and landscape spatial scales and to contrast these patterns between adults and juveniles. We sampled palm communities in 22 fragments of Choco rainforest in and around the Mache-Chindul Ecological Reserve in north-western Ecuador, where we recorded 9991 individuals of 23 palm species. At the landscape scale, fragment size and surrounding forest cover were not associated with species richness or abundance for either adults or juveniles. However, community similarity of juveniles was related to surrounding forest cover and the abundance of juveniles and adults increased with elevation. At the local scale, adults and juveniles differed in their relationships to environmental variables and distance to fragment edge: juveniles showed reduced species richness and different community composition near fragment edges compared with interior habitat, but adults did not. These results provide baseline information on palm communities in a poorly studied conservation hotspot and highlight the importance of considering multiple spatial scales and life stages in studies of habitat fragmentation. © 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016

Karubian, J., L. Browne, D. Cabrera, M. Chambers, and J. Olivo. 2016. “Relative Influence of Relatedness, Conspecific Density, and Microhabitat on Seedling Survival and Growth of an Animal-Dispersed Neotropical Palm, Oenocarpus Bataua.”. Botanical Journal of the Linnean Society, 182: 425-438.

We report on a 6-year, field-based experiment in north-western Ecuador, evaluating the relative importance of relatedness, conspecific density and microhabitat on the growth and survival of seedlings of an ecologically and economically important palm, Oenocarpus bataua. We planted O. bataua seedlings in high-density seed deposition sites (leks) of the long-wattled umbrellabird (Cephalopterus penduliger) and randomly selected control sites. We analysed seedling performance in relation to conspecific relatedness, conspecific density and microhabitat. Among the parameters we measured, light availability was the most important determinant for survival and growth. Higher relatedness of neighbouring experimental seedlings and higher conspecific seedling densities were both associated with reduced growth, but did not influence survival, even in umbrellabird leks. These findings are consistent with a survival advantage of umbrellabird dispersal into lek sites (i.e. directed dispersal) that counterbalances negative density-dependent processes expected to occur at these high-density deposition sites. This study highlights the importance of a multi-tiered approach to understanding palm demography and underlines the importance of seed disperser behaviour in determining seedling fate. © 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 182, 425–438

Lantz, S.M., and J. Karubian. 2016. “Male Red-Backed Fairywrens Enhance a Plumage-Based Signal via Adventitious Molt.”. Auk, 133:338-346.

Phenotypically plastic signals that can be altered in response to changing environmental conditions provide animals with the ability to dynamically signal their current condition or status. Such flexibility might also provide a means of avoiding potential trade-offs between signal components. Among birds, for example, both the timing of expression and the coloration of nuptial plumage are often thought to be honest signals of condition. However, because plumage is a relatively static signal type, birds that express condition-dependent plumage signals may face a trade-off between timing of signal production and signal quality, in that signals produced relatively early may be of lower quality because of seasonal constraints. A related cost may be increased fading or wear of plumage associated with extended duration of signal expression. Male Red-backed Fairywrens (Malurus melanocephalus) exhibit asynchronous development of nuptial red–black plumage, with some individuals molting into nuptial plumage months earlier than others. We report that male Red-backed Fairywrens that molt into nuptial red–black plumage early during the nonbreeding season appear to increase their plumage coloration by replacing feathers outside of normal molt periods (i.e. adventitious molt). In this way, some male Red-backed Fairywrens may be able to molt into nuptial plumage in the nonbreeding season, which is likely to increase access to mates or resources, and to subsequently enhance the red hue of a plumage-based sexual signal to a putatively more attractive state. We suggest that adventitious molt may be a currently underappreciated mechanism that birds use to improve or maintain the quality of plumage-based signals over time, between periodic full-body molts.

Frumkin, N.B., T.W. Wey, M. Exnicios, C. Benham, M.G. Hinton, S. Lantz, C. Atherton, J. Karubian, and D. Forde. 2016. “Inter-Annual Patterns of Aggression and Pair Bonding in Captive American Flamingos(Phoenicopterus Ruber).”. Zoo Biology, 35: 111-119.

Because zoos typically house animals for extended periods of time, longitudinal studies can play an important role in evaluating and optimizing animal care and management. For example, information on patterns of aggression and mating behavior across years can be used to monitor well-being, assess response to changes to group composition, and promote successful reproduction. Here, we report on patterns of aggression and pair bonding by American flamingos (Phoenicopterus ruber) at the Audubon Zoo, New Orleans USA across 4 years (2012–2015), a period that included a simultaneous introduction and removal of individuals in 2014. At the population level, overall rates and social network indices of aggressive interactions were relatively stable over the study period, without a strong signal of the 2014 replacement event. At the individual level, flamingos exhibited a high degree of within-individual consistency in levels of aggression initiated (W ¼ 0.530, P < 0.001), and received (W ¼ 0.369, P ¼ 0.042). In terms of pair bonds, females re-paired with the same individuals across years more frequently (between 58% and 100% from year to year) than they switched mates, and no bonds were established between preexisting and introduced individuals. These findings indicate a high degree of stability in aggression and pair bonding behavior in this population of captive flamingos, at both the population and individual level. Longitudinal studies such as this one provide an opportunity to better our understanding of flamingos and other long-lived, group-living animals along with their management needs, especially in terms of maintaining social cohesion in captivity and improving captive breeding programs

2015

Koczur, L. M., G. M. Kent, B. Geary, B. M. Ballard, K. D. Meyer, and M. C. Green. 2015. “Measurements of Adult and Hatch-Year Reddish Egrets (Egretta Rufescens).”. Waterbirds, 38:308-311.

Measurements of live-captured adult and hatch-year Reddish Egrets (Egretta rufescens) from Texas (n = 29 and 25, respectively) and Florida (n = 7 and 3, respectively) are reported. Mass, tarsus length, and culmen length were used to compare sexes and ages of Reddish Egrets. Adult males (n = 17) were significantly larger than adult females (n = 19) in all parameters, and hatch-year Reddish Egrets were significantly smaller than adults in all parameters. Additionally, considerably larger measurements were recorded on average than those previously available for Reddish Egrets. These measurements provide updated information on the morphometry of Reddish Egrets that will be useful in understanding life history strategies and for planning future studies. Received 20 January 2015, accepted 25 March 2015.

Geary, B., C. Green, and B.M. Ballard. 2015. “Movements and Survival of Juvenile Reddish Egrets Egretta Rufescens on the Gulf of Mexico Coast.”. Endangered Species Research, 28:123-133.

Understanding natal dispersal patterns of animals is critical to development of effective species conservation plans, as it ensures that population management takes place at appropriate scales. The reddish egret Egretta rufescens is a threatened waterbird species lacking documentation on many aspects of its ecology, including movement behaviors at all life stages. We attached satellite transmitters to 25 juvenile reddish egrets on their natal colonies and observed their dispersal patterns and subsequent movements over a period of 115 wk (May 2010–August 2012). Birds exhibited the greatest movement rates in the remainder of the first breeding season (through July 2010, ~10 to 13 wk of age, 11.07 km d−1) and steadily decreased in the post-breeding period (4.87 km d−1) and winter (1.96 km d−1) of their first year. Movements of 1 to 2.5 km d−1 characterized the remainder of the tracking period, suggesting that surviving birds were able to establish local territories. Of the 25 tagged birds, 8 (32%) survived throughout the observation period, based on transmitter failure rates, with losses increasing each winter. The majority of birds remained on the Texas/ Mexico coast of the Gulf of Mexico, indicating that the population is largely resident and therefore vulnerable to coastal habitat alterations in the region. Due to a combination of infrequent long- distance migration, specialized behaviors, and apparent limited gene flow, habitat maintenance should be of primary importance for management of this rare species. This is among the first published studies of heron movement ecology using telemetry, and should be followed by further tracking with developing technologies to characterize high-resolution movements and habitat associations.

Karubian, J., K. Ottewell, A .Link, and A. DiFiori. 2015. “Genetic Consequences of Seed Dispersal to Sleeping Trees by Spider Monkeys”. Acta Oecologica, 68:50-58.

Frugivorous animals frequently generate clumped distributions of seeds away from source trees via ‘destination-based’ dispersal processes. For example, use of traditional sleeping trees by white-bellied spider monkeys Ateles belzebuth generates high densities of seeds of a preferred food source, the palm Oenocarpus bataua, at these sites. Little is known about the maternal seed source diversity and population genetic metrics of seed pools encountered at these sites. Given the repeated use of sleeping trees over time, and the fluid social organization and wide ranging movements exhibited by spider monkeys, we predicted that O. bataua seed pools beneath sleeping trees would be characterized by relatively high values of maternal seed source diversity and standard metrics of genetic diversity. Contrary to these expectations, we found relatively low average maternal seed source diversity beneath each of 6 sleeping trees we studied (weighted mean a ¼ 3.74), but considerable variation in diversity of maternal seed sources between sleeping trees (range ¼ 1.75e10.1) and high heterogeneity in standard genetic diversity measures between sleeping trees. There was no evidence for overlap in maternal seed sources between sleeping tree sites (d ¼ 1.0), resulting in significant genetic differentiation (Fst ¼ 0.055e0.319) between these sites. Observed variation between sleeping trees could not be explained by the number of individual spider monkeys whose core home ranges included a given tree, nor by distance to a central mineral lick, a focal point of spider monkey activity. These findings suggest that spider monkey seed dispersal to sleeping trees is spatially restricted, perhaps because the animals visit sleeping trees at the end of the day and therefore only disperse O. bataua fruits that they ingest late in the day. These results add to our growing appreciation of the ways frugivore behavior mechanistically shapes seed dispersal outcomes.