Publications by EEOB faculty August 1 - August 31

September 1, 2015
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Temporal patterns of Pederson shrimp (Ancylomenes pedersoni Chace 1958) cleaning interactions on Caribbean coral reefs

Benjamin M. Titus, Marymegan Daly, Dan A. Exton. 2015. Marine Biology 162(8):1651-1664. doi:10.​1007/​s00227-015-2703-z


Dozens of marine species have been identified as “cleaners” and many of these co-occur and have considerable overlap in clientele. Understanding the temporal patterns and processes of these cleaning symbioses can provide insight into differential service provision between cleaner species and the ultimate and proximate causes structuring these interactions. Considerable progress has been made in understanding the ecology and behavior of cleaner fish, yet little basic ecological and behavioral data exist for cleaner shrimp. We deployed remote underwater video cameras on coral reefs in the Bay Islands, Honduras, to explore temporal variation of cleaning interactions at Pederson shrimp (Ancylomenes pedersoni) stations. We recorded more than 650 individual cleaning interactions in over 190 h of video. We find no significant temporal variation in cleaning station usage patterns across 17 families of reef fish. Our findings are in contrast to previously published data for interactions of Caribbean cleaner gobies, which co-occur at the sites we studied and overlap significantly in client pool with A. pedersoni but which are most active at dawn. These data suggest that the services provided by cleaner shrimp and cleaner gobies, rather than client identity, independently structure these interactions and drive the discordance in usage patterns between cleaner type. We propose two non-exclusive hypotheses to explain the differences in the temporal patterns of activity between cleaner gobies and A. pedersoni: (1) the proximate causes driving fish visitation rate (e.g., parasite removal or tactile stimulation) to goby and shrimp stations differ, and (2) each cleaner type targets different ectoparasites that differ temporally in their diel infestation rate on reef fish. Our study provides an important rationale for pursuing these questions and broadens our understanding of cleaning services on Caribbean coral reefs.

Daly Lab

Toxicity in lead salt spiked soils to plants, invertebrates and microbial processes: Unraveling effects of acidification, salt stress and ageing reactions

Erik Smolders, Koen Oorts, Sofie Peeters, Roman Lanno, Karlien Cheyns. 2015. Science of The Total Environment 536:223–231. doi:10.1016/j.scitotenv.2015.07.067


The fate and effects of toxic trace metals in soil freshly spiked soluble metal salts do not mimic those of metals in the field. This study was set up to test the magnitude of effects of salinity, acidification, and ageing on toxicity of lead (Pb) to plants, invertebrates and soil microbial processes. Three soils were spiked with Pb2 + salts up to a concentration of 8000 mg Pb/kg and were tested either after spiking, after soil leaching followed by pH correction, or after a 5-year outdoor ageing period with free drainage followed by pH correction. Soil solution ionic strength exceeded 150 mmol/L in soils tested directly after spiking and this decreased partially after leaching and returned back to background values after 5-year outdoor equilibration. Chronic toxicity to two plants, two invertebrates, and three microbial endpoints was consistently found in all spiked soils that were not leached. This toxicity significantly decreased or became absent after 5 years of ageing in 19 of the 20 toxicity tests by a factor 8 (median factor; range: 1.4–>50), measured by the factor increase of total soil Pb dose required to induce 10% inhibition. The toxicity of Pb in leached soils was intermediate between the other two treatments. The lowest detectable chronic thresholds (EC10) in aged soils ranged 350–5300 mg Pb/kg. Correlation analysis, including data of Pb2 + speciation in soil solution, suggests that reduced ionic strength rather than acidification or true ageing is the main factor explaining the soil treatment effects after spiking. It is suggested that future toxicity studies should test fine PbO powder as a relevant source for Pb in soils to exclude the confounding salt effects.

Ubiquitous germination among common perennial species in response to facilitated and unfacilitated microhabitats

Natasha N. Woods, Maria N. Miriti. 2016. Journal of Arid Environments 124:72–79. doi:10.1016/j.jaridenv.2015.07.012


We present results from a study that examines species-specific facilitation of germination in an arid perennial community. This system suffered 64% adult mortality and the local extinction of two common species as a consequence of drought that occurred between 1999 and 2004. Ambrosia dumosa, Larrea tridentata, and Tetracoccus hallii are included as candidate benefactor species based on their high abundance and broad distribution at the study site. Using complementary field and greenhouse experiments, we measured the effects of facilitation, light and nitrogen on germination of four species common to the region, L. tridentata, A. dumosa, Sphaeralcea ambigua and Eriogonum fasciculatum.

Our results show that benefactor species do not uniquely influence germination. Species-specific effects among beneficiaries largely explained differences in percent germination in the field, and the interaction between beneficiary species and microhabitat was significant for only one species. E. fasciculatum consistently showed significantly higher germination than more abundant species and showed reduced germination in the interspace. In the greenhouse, germination responses differed at each light level, beneficiaries responding most uniquely at full light. These results refine expectations from previous studies of facilitation at this site by showing that facilitation does not strongly enhance germination.


Two new mite species of the subfamily Harpirhynchinae Dubinin, 1957 (Acariformes: Harpirhynchidae), parasites of the passerine birds (Aves: Passeriformes) in Australia and South Asia

Andre V. Bochkov, Hans Klompen. 2015. Systematic Parasitology 92(1):23-29. DOI 10.1007/s11230-015-9582-z


Two new mite species of the subfamily Harpirhynchinae Dubinin, 1957 (Acariformes: Harpirhynchidae) are described from passerine birds (Aves: Passeriformes): Harpirhynchoides artamus n. sp. from Artamus fuscus Vieillot (Artamidae) from an unknown locality in South Asia and Neharpyrhynchus domrowi n. sp. from three host species of the family Meliphagidae, Acanthorhynchus tenuirostris (Latham) (type-host) from Australia (New South Walles), Ptiloprora perstriata (De Vis) and Myzomela rosenbergii Schlegel from Papua New Guinea.

Acarology Lab


Fixed prey cue preferences among Dusky Pigmy Rattlesnakes (Sistrurus miliarius barbouri) raised on different long-term diets

Matthew L. Holding, Edward H. Kern, Robert D. Denton, H. Lisle Gibbs. 2015. Evolutionary Ecology. DOI 10.1007/s10682-015-9787-2


Chemoreception is often crucial to the interaction between predators and their prey. Investigating the mechanisms controlling predator chemical preference gives insight into how selection molds traits directly involved in ecological interactions between species. In snakes, prey cue preferences are influenced by both direct genetic control and experience-based plasticity. We assessed prey preference in a group of Dusky Pigmy Rattlesnakes that had eaten only mice or lizards over a 5 year period to test whether genetics or plasticity primarily determine the preference phenotype. Our results provide evidence for genetic determination of preference for lizard chemical cues in pigmy rattlesnakes. Snakes preferred the scent of lizards, regardless of their initial diet, and the response to mouse scent did not differ from the water-only control. We discuss these findings in light of previous studies that manipulated snake diets over shorter timescales.

Gibbs Lab

Geometric ergodicity of a hybrid sampler for Bayesian inference of phylogenetic branch lengths

David A. Spade, Radu Herbei, Laura S. Kubatko. Mathematical Biosciences. doi:10.1016/j.mbs.2015.07.002


One of the fundamental goals in phylogenetics is to make inferences about the evolutionary pattern among a group of individuals, such as genes or species, using present-day genetic material. This pattern is represented by a phylogenetic tree, and as computational methods have caught up to the statistical theory, Bayesian methods of making inferences about phylogenetic trees have become increasingly popular. Bayesian inference of phylogenetic trees requires sampling from intractable probability distributions. Common methods of sampling from these distributions include Markov chain Monte Carlo (MCMC) and Sequential Monte Carlo (SMC) methods, and one way that both of these methods can proceed is by first simulating a tree topology and then taking a sample from the posterior distribution of the branch lengths given the tree topology and the data set. In many MCMC methods, it is difficult to verify that the underlying Markov chain is geometrically ergodic, and thus, it is necessary to rely on output-based convergence diagnostics in order to assess convergence on an ad hoc basis. These diagnostics suffer from several important limitations, so in an effort to circumvent these limitations, this work establishes geometric convergence for a particular Markov chain that is used to sample branch lengths under a fairly general class of nucleotide substitution models and provides a numerical method for estimating the time this Markov chain takes to converge.


Variation in glucocorticoid levels in relation to direct and third-party interactions in a social cichlid fish

Isaac Y. Ligocki, Ryan L. Earley, Jennifer K. Hellmann, Ian M. Hamilton. Physiology & Behavior. 2015.151:386–394. doi:10.1016/j.physbeh.2015.08.004.


In complex animal societies, direct interactions between group members can influence the behavior and glucocorticoid levels of individuals involved. Recently, it has become apparent that third-party group members can influence dyadic interactions, and vice versa. Thus, glucocorticoid levels may vary depending on interactions of other members of the social group. Using the social cichlid fish Neolamprologus pulcher, we examined the relationship between levels of the glucocorticoid hormone cortisol in subordinate females and 1) direct interactions with dominant group members, as well as 2) dyadic interactions between the dominant male and female, in which the subordinate female was not directly involved. Subordinate females that frequently engaged in non-aggressive interactions with dominant females had lower cortisol levels. There was no relationship between subordinate female cortisol and agonistic interactions between the subordinate female and either dominant. Subordinate females had higher cortisol levels when in groups in which the dominant breeding pair behaved agonistically towards each other and performed fewer courtship behaviors. For subordinate females in this species, variation in cortisol levels is associated with their own affiliative behavior, but also can be explained by the broader social context of interactions between dominant members of the group.

Hamilton Lab

Perspectives on the membrane fatty acid unsaturation/pacemaker hypotheses of metabolism and aging

Elisabeth A. Calhoon, Jennifer Ro, Joseph B. Williams. 2015. Chemistry and Physics of Lipids 191:48–60. doi:10.1016/j.chemphyslip.2015.08.008.


The membrane pacemaker hypotheses of metabolism and aging are distinct, but interrelated hypotheses positing that increases in unsaturation of lipids within membranes are correlated with increasing basal metabolic rate and decreasing longevity, respectively. The two hypotheses each have evidence that either supports or contradicts them, but consensus has failed to emerge. In this review, we identify sources of weakness of previous studies supporting and contradicting these hypotheses and suggest different methods and lines of inquiry. The link between fatty acyl composition of membranes and membrane-bound protein activity is a central tenet of the membrane pacemaker hypothesis of metabolism, but the mechanism by which unsaturation would change protein activity is not well defined and, whereas fatty acid desaturases have been put forward by some as the mechanism behind evolutionary differences in fatty acyl composition of phospholipids among organisms, there have been no studies to differentiate whether desaturases have been more affected by natural selection on aging and metabolic rate than have elongases or acyltransferases. Past analyses have been hampered by potentially incorrect estimates of the peroxidizability of lipids and longevity of study animals, and by the confounding effect of phylogeny. According to some authors, body mass may also be a confounding effect that should be taken into account, though this is not universally accepted. Further research on this subject should focus more on mechanisms and take weaknesses of past studies into account.

Williams Lab

Ryan A. Folk, Jennifer R. Mandel and John V. Freudenstein. 2015. Applications in Plant Sciences 3(8):1500039. doi:


Phylogenetic inference is moving to large multilocus data sets, yet there remains uncertainty in the choice of marker and sequencing method at low taxonomic levels. To address this gap, we present a method for enriching long loci spanning intron-exon boundaries in the genus Heuchera. Two hundred seventy-eight loci were designed using a splice-site prediction method combining transcriptomic and genomic data. Biotinylated probes were designed for enrichment of these loci. Reference-based assembly was performed using genomic references; additionally, chloroplast and mitochondrial genomes were used as references for off-target reads. The data were aligned and subjected to coalescent and concatenated phylogenetic analyses to demonstrate support for major relationships. Complete or nearly complete (>99%) sequences were assembled from essentially all loci from all taxa. Aligned introns showed a fourfold increase in divergence as opposed to exons. Concatenated analysis gave decisive support to all nodes, and support was also high and relationships mostly similar in the coalescent analysis. Organellar phylogenies were also well-supported and conflicted with the nuclear signal. Our approach shows promise for resolving a recent radiation. Enrichment for introns is highly successful with little or no sequencing dropout at low taxonomic levels despite higher substitution and indel frequencies, and should be exploited in studies of species complexes.

Freudenstein Lab

Evolution and function of the upper molar talon and its dietary implications in microbats

Sarah C. Gutzwiller and John P. Hunter. 2015. Journal of Morphology. DOI: 10.1002/jmor.20424


The evolution of mammalian molars has been marked by transitions representing significant changes in shape and function. One such transition is the addition and elaboration of the talon, the distolingual region of the ancestral tribosphenic upper molar of therian mammals and some extinct relatives. This study uses suborder Microchiroptera as a case study to explore the adaptive implications of the expansion of the talon on the tribosphenic molar, specifically focusing on the talon's role in the compression and shear of food during breakdown. Three-dimensional computer renderings of casts of the upper left first molars were created for microbat species of a variety of dietary categories (frugivore, etc.) and physical properties of food (hard and soft). Relief Index (RFI) was measured to estimate the topography and function of the whole tooth and of the talon and trigon (the remaining primitive tribosphenic region) individually, in order to examine 1) how the shape of the whole tooth, trigon, and talon reflects the compromise between their crushing and shearing functions, 2) how whole tooth, trigon, and talon function differs according to diet, and 3) how the presence of the talon affects overall molar function. Results suggest that RFI of both the whole tooth and the trigon varies according to dietary groups, with frugivores having greater crushing function when compared with the other groups. The talon, however, consistently has low RFI (a flatter topography), and its presence lowers the RFI of the whole tooth across all dietary categories, suggesting that the talon is primarily functioning in crushing during food breakdown. The potential benefits of a crushing talon for microbats of various dietary groups are discussed.

Checklist of the genera of Hymenoptera (Insecta) from Espírito Santo state, Brazil

Celso O. Azevedo, Ana Dal Molin, Angélica Penteado-Dias, Antonio C.C. Macedo, Beatriz Rodriguez-V., Bianca Z.K. Dias, Cecilia Waichert, Daniel Aquino, David R. Smith, Eduardo M. Shimbori, Fernando B. Noll, Gary Gibson, Helena C. Onody, James M. Carpenter, John E. Lattke, Kelli dos S. Ramos, Kevin Williams, Lubomir Masner, Lynn S. Kimsey, Marcelo T. Tavares, Massimo Olmi, Matthew L. Buffington, Michael Ohl, Michael Sharkey, Norman F Johnson, Ricardo Kawada, Rodrigo B. Gonçalves, Rodrigo M. Feitosa, Steve Heydon,Tânia M. Guerra, Thiago S.R. da Silva, and Valmir Costa. Bol. Mus. Biol. Mello. Leitao. 37(3):313-343.


The first checklist of genera of Hymenoptera from Espírito Santo state, Brazil is presented. A total of 973 genera of Hymenoptera is listed, of which 555 (57%) are recorded for the first time from this state. Ichneumonoidea and Chalcidoidea are the two superfamilies with the most genera, 241 and 203 respectively. Braconidae, with 141 genera, are the richest family.

Johnson lab

Female choice for male cuticular hydrocarbon profile in decorated crickets is not based on similarity to their own profile

S. Steiger, A. Capodeanu-Nägler, S.N. Gershman, C.B. Weddle, J. Rapkin, S. K. Sakaluk and J. Hunt. 2015. Journal of Evolutionary Biology. DOI: 10.1111/jeb.12740


Indirect genetic benefits derived from female mate choice comprise additive (good genes) and non-additive genetic benefits (genetic compatibility). Although good genes can be revealed by condition-dependent display traits, the mechanism by which compatibility alleles are detected is unclear because evaluation of the genetic similarity of a prospective mate requires the female to assess the genotype of the male and compare it to her own. Cuticular hydrocarbons (CHCs), lipids coating the exoskeleton of most insects, influence female mate choice in a number of species and offer a way for females to assess genetic similarity of prospective mates. Here, we determine whether female mate choice in decorated crickets is based on male CHCs, and whether it is influenced by females’ own CHC profiles. We used multivariate selection analysis to estimate the strength and form of selection acting on male CHCs through female mate choice, and employed different measures of multivariate dissimilarity to determine whether a female's preference for male CHCs is based on similarity to her own CHC profile. Female mating preferences were significantly influenced by CHC profiles of males. Male CHC attractiveness was not, however, contingent on the CHC profile of the choosing female, as certain male CHC phenotypes were equally attractive to most females, evidenced by significant linear and stabilizing selection gradients. These results suggest that additive, rather than non-additive genetic benefits accrue to female mate choice, in support of earlier work showing that CHC expression of males, but not females, are condition dependent.

Gershman Lab