Recent Faculty Publications

The Biology Department Faculty maintain active research labs, collaborating with Puget Sound undergraduate research students, as well as scholars across the country and around the world. Below are some of the most recent publications from our faculty. To learn more about an individual faculty member’s lab, or to see complete lists of publications, please explore our faculty research pages.

Stacey Weiss & Marie Bunker: Wild Microbiomes of Striped Plateau Lizards Vary With Reproductive Season, Sex, and Body Size.

Published: 2022

Summary: This paper tracks the microbiome of striped plateau lizards across the species’ entire active period, from March to October, with sampling occurring every other week. A project like this can only happen with sabbatical support from the institution! We found that microbial diversity is lowest during the reproductive season, was higher in females than in males, and was lowest in females when they were vitellogenic (i.e., making eggs). The microbiome composition was affected by season, sex, and body size.

Bunker, M.E., Arnold, and S.L. Weiss. 2022. Wild microbiomes of striped plateau lizards vary with reproductive season, sex, and body size. Scientific Reports 12, 20643. DOI: 10.1038/s41598-022-2418-6

Katherine Crocker: Study the forest, not only the trees: Environmental exposures, not genomes, generate most health disparities.

Published: August 19, 2022

Summary: As sequencing and analysis techniques provide increasingly detailed data at a plummeting cost, it is increasingly popular to seek the answers to medical and public health challenges in the DNA sequences of affected populations. This is methodologically attractive in its simplicity, but a genomics-only approach ignores environmentally mediated health disparities, which are well-documented at multiple national and global scales. While genetic differences exist among populations, it is unlikely that these differences overcome social and environmental factors in driving the gap in health outcomes between privileged and oppressed communities. We advocate for following the lead of communities in addressing their self-identified interests, rather than treating widespread suffering as a convenient natural experiment.

Taylor V. Thompson and Katherine C. Crocker. Study the forest, not only the trees: Environmental exposures, not genomes, generate most health disparities. August 2022 Frontiers in Genetics 13:817899. DOI:10.3389/fgene.2022.817899. License CC BY 4.0.

Stacey Weiss: Recovered microbiome of an oviparous lizard differs across gut and reproductive tissues, cloacal swabs, and faeces

Published: December 11, 2021

Summary: This paper has two main findings about the microbiome of female striped plateau lizards. First, we show that the cloacal microbiome, which is known to provide antifungal protection to eggshells, is distinct from the microbiome of upper intestine and oviductal tissues. Second, although cloacal swabs and fecal samples are both commonly used to estimate the gut microbiome, swabs only provided an accurate representation of the cloacal and lower intestinal tissues, and fecal samples were distinct from all tissues. Our results serve as a caution to others in the field against using fecal microbes to make conclusions about gut microbes.

Bunker ME, Martin MO, Weiss SL. Recovered microbiome of an oviparous lizard differs across gut and reproductive tissues, cloacal swabs, and faeces. Mol Ecol Resour. 2021 Dec 11. doi: 10.1111/1755-0998.13573. Epub ahead of print. PMID:34894079.

Carrie Woods: A case for studying biotic interactions in epiphyte ecology and evolution

Published: 2022

Biotic interactions, including both within and across trophic levels, are poorly explored in epiphytes despite being an importance driver of ecology and evolution. This is a topic of broad interest because epiphytes - including vascular plants, bryophytes, and lichens - exist in practically all terrestrial ecosystems throughout the world. In this review article led by the post-doctoral researcher in my lab, we state the importance of biotic interactions in epiphyte ecology and evolution through a systematic review of the literature that summaries our current knowledge and highlights gaps in our understanding. We also provide a conceptual framework for future directions.

Spicer, M.E. and C. L. Woods. A case for studying biotic interactions in epiphyte ecology and evolution. Perspectives in Plant Ecology, Evolution and Systematics 54:125658

Carrie Woods: Putting vascular epiphytes on the traits map

Published: April 23, 2021

Plant functional traits impact the fitness and environmental niche of plants and inform plant functional types. Yet trait data on epiphytes are scarce despite epiphytes representing almost 10% of vascular plants. In a large collaboration among epiphyte researchers, we collated 76,561 trait observations for 2,882 species of vascular epiphytes and compared these to non-epiphytic herbs and trees to test hypotheses related to how the epiphytic habit affects traits, and and if epiphytes occupy a distinct region in the global trait space. Epiphytes differ from ground-rooted plants mainly in traits related to water relations and exhibit variation among major epiphyte groups.

Hietz, P., K. Wagner, F.N. Ramos, J. S. Cabral, (alphabetical from here) C. Agudelo, A.M. Benavides, M. J. Cach-Perez, C. Cardelus, N. C. Galvan, L. E. Nascimiento da Costa, R. de Paula Oliveira, G. J. R. Einzmann, R. de Paiva Farias, V. G. Jacob, J. Kattge, M. Kessler, C. Kirby, H. Kreft, T. Kromer, J. Males, S. M. Correa, M. Moreno-Chacon, G. Petter, C. Reyes-Garcia, A. Saldana, D. S. Costa, A. Taylor, N. V. Rosas, W. Wanek, C. L. Woods, and G. Zotz. (2021) Putting vascular epiphytes on the traits map. Journal of Ecology. 110:340-358

Stacey Weiss: Vertically transmitted microbiome protects eggs from fungal infection and egg failure

a striped plateau lizard in a specimen dish

Published: 16 June 2021

The striped plateau lizard lays their eggs in soil burrows, right at the start of the hot and wet monsoon season, and then they leave the nest site — providing no further parental care. How do the eggs survive their two month incubation period in the soil, surrounded by potential fungal pathogens? In this paper, coauthored with two undergraduate students, we show that maternal microbes are transferred from mom to eggshell during egg-laying, and that these beneficial bacteria provide antifungal protection to the eggs. Eggs with maternal microbes are better able to fend off attachment of pathogenic fungi, resulting in higher hatch success and better offspring quality.

Bunker, M.E., G. Elliott*, H. Heyer-Gray*, M.O. Martin, A.E. Arnold, and S.L. Weiss. 2021. Vertically transmitted microbiome protects eggs from fungal infection and egg failure. Animal Microbiome 3:43.

Carrie Woods: Plant–plant interactions change during succession on nurse logs in a northern temperate rainforest

Accepted: 26 May 2021

Summary: Nurse logs are fallen trees that promote forest regeneration because they act as a preferred site for tree seedlings in many forests. Bryophyte communities (mosses and liverworts) are abundant on nurse logs in the Hoh rainforest and may interact with tree seedlings in various ways. Two recent Puget Sound graduates and I surveyed bryophytes and tree seedlings on nurse logs at various stages of decay and found that bryophytes on young nurse logs were thin and had many tree seedlings and bryophytes on old, decayed logs were thick and had few tree seedlings. Bryophytes seem to facilitate tree seedlings on young logs but out-compete them on old logs. The tiniest plants, therefore, impact the dynamics of the regions giant trees.

Woods, C. L., K. Maleta and K. Ortmann. (2021) Plant-plant interactions change during succession on nurse logs in a northern temperate rainforest. Ecology and Evolution https://doi.org/10.1002/ece3.7786.

Stacey Weiss: Wildfire as a natural stressor and its effect on female phenotype and ornament development

A wildfire raging across a research station

Accepted: 1 March 2021

When a wildfire burned through Stacey’s long-term study site, she and her students had to throw away their research plans and make the best out of a bad situation. This paper is the result of some of that work. They found that the reproductive ornament produced by female striped plateau lizards was significantly smaller on the burned site than on a nearby unburned site.

Weiss, S.L. and R.M. Brower. 2021. Wildfire as a natural stressor and its effect on female phenotype and ornament development. Ecol Evol 11:6223-6232.

Rachel Pepper: The effect of external flow on the feeding currents of sessile microorganisms

Microscopic aquatic organism with water flow diagram

Published: 24 February 2021

Many microscopic aquatic organisms attach to surfaces where they clean the water by eating bacteria. We show how the water flow produced by these microorganisms to carry food towards them interacts with ambient water currents. This interaction increases or decreases feeding rates depending on the ability of the organisms to adjust their orientation relative to the flow. These results can help us understand how bodies of water stay clean and in balace.

R. E. Pepper, E. E. Riley, M. Baron, L.T. Nielsen, M.A.R. Koehl, T. Kiørboe, and A. Andersen The effect of external flow on the feeding currents of sessile microorganisms. J. R. Soc. Interface, 18, 20200953 (2021).

Oscar Sosa: A sensitive fluorescent assay for measuring carbon-phosphorus lyase activity in aquatic systems

Data of carbon-phosphorus lyase activity

First published: 25 January 2021

This paper describes a biochemical assay to detect and quantify the activity of the C-P lyase multi-protein compled in the environment, a bacterial enzyme responsible for the degradation of phosphonates in marine organic matter and the release of hydrocarbons like methane and ethylene in oceanic waters.

Granzow B.N., Sosa O.A., Gonnelli M., Santinelli C., Karl D.M., Repeta D.J. (2021) A sensitive fluorescent assay for measuring carbon-phosphorus lyase activity in aquatic systems. Limnology and Oceanography: Methods 19(4), 235-244.

Carrie Woods: Tree Community Composition and Dispersal Syndrome Vary with Human Disturbance in Sacred Church Forests in Ethiopia

Published: 10 October 2020

Summary: Along with a recent graduate, Robyn Thomas, and an interdisciplinary team of ecologists, geographers, and social scientists, we examined the drivers of woody species composition among 46 church forests in northern Ethiopia. Variations in species composition across church forests were driven more by variations in human disturbance and community forest management than forest size. The degree of human disturbance acted as an environmental filter that selected for weedy, exotic, and wind-dispersed species regardless of forest size.

Woods, C. L. , A. Bitew Mekonnen, M. Baez-Schon*, R. Thomas**, P. Scull, B. Abraha Tsegay, and C. L. Cardelús. (2020). Tree community composition and dispersal syndrome vary with human disturbance in sacred church forests in Ethiopia. Forests 11:1082.

Stacey Weiss: Teaching animal behavior online: A primer for the pandemic and beyond

First published: 05 October 2020

When the pandemic struck, Weiss and her professional colleagues dove into research concerning best practices in remote teaching of organismal-based courses, which typically stress experiential learning and have labs involving hands-on work with live animals. This paper serves as a primer for other faculty needing to rapidly revamp their courses to an online format due to COVID, with a focus on generating inclusive and engaging online learning environments for their students.

Hughes, M., S.M. Bertram, A.M. Young*, J.W. Merry*, G.R. Kolluru*, A.S. Dunlap*, A. Danielson-Francois*, and S.L. Weiss*. 2021. Teaching animal behavior in the midst of a pandemic: A primer. Ethology 127:14-31. (https://doi.org/10.1111/eth.13096; ^aEqual co-authors; order decided randomly)

Oscar Sosa: Phosphonate cycling supports methane and ethylene supersaturation in the phosphate-depleted western North Atlantic Ocean

First published: 20 May 2020

This paper describes the results of a field study that linked the degradation of organic matter phosphonates by bacteria containing C-P lyase enzyme to the production of methane and ethylene gas in marine surface waters particularly devoid of the nutrient phosphate. The study employed an interdisciplinary approach to draw this connection.

Sosa O.A., Burrell T.J., Wilson S.T., Foreman R.K., Karl D.M., Repeta D.J. (2020). Phosphonate cycling supports methane and ethylene supersaturation in the phosphate-depleted western North Atlantic Ocean. Limnology and Oceanography 65(10), 2443-2459.

Andreas Madlung: Subfunctionalization of phytochrome B1/B2 leads to differential auxin and photosynthetic responses

First published: 28 February 2020

Gene duplication and polyploidization are genetic mechanisms that instantly add genetic material to an organism’s genome on which evolution can then act. In this paper we describe how the two light receptor genes phytochrome B1 and B2 have diverged since their duplication both in their phenotypic functions and their transcriptional regulation of gene networks in response to light.

Carlson, KD, Bhogale, S, Anderson, D, Zaragoza-Mendoza, A, Madlung, A. Subfunctionalization of phytochrome B1/B2 leads to differential auxin and photosynthetic responses. (2020) Plant Direct 4(2): e00205.

Carrie Woods: Structural heterogeneity of trees influences epiphyte distributions in a northern temperate rainforest

First published: 30 July 2019

In this study we examined the distribution of epiphytic bryophytes in bigleaf maple trees in the Olympic temperate rainforest along with the factors that drive their distribution. We found differences in epiphyte communities between the trunks and branches with more species found on the trunk. Structural features of the tree, including branch size, height, and moss depth, influenced epiphyte distributions more than microclimate.

Woods, C. L., L. M. Nevins, and E. J. Didier. (2019). Structural heterogeneity of trees influences epiphyte distributions in a northern temperate rainforest. Journal of Vegetation Science 30:1134-1142.

Oscar Sosa: Methylphosphonate Oxidation in Prochlorococcus Strain MIT9301 Supports Phosphate Acquisition, Formate Excretion, and Carbon Assimilation into Purines

17 June 2019

So far, the marine bacterial species known to metabolize a marine natural product known as methylphosphonate accomplish this through the carbon-phosphorus lyase enzyme, a mechanism that releases the greenhouse gas methane as a byproduct. This study describes an alternative pathway by which the marine photosynthetic bacterium Prochlorococcusmetabolizes methylphosphonate. The new pathway consists of oxidizing methylphosphonate into formate and phosphate, avoiding the release of methane. This result is relevant to our understanding of the role of marine phosphonates and oceanic microbes in climate, because it demonstrates that not all methylphosphonate in the ocean is degraded into methane. Some of it must be converted to formic acid, a compound that can be easily utilized by other marine microbes as fuel for cellular processes or as a biomass building block.

Oscar Sosa: Phosphate-limited ocean regions select for bacterial populations enriched in the carbon-phosphorus lyase pathway for phosphonate degradation

First published: 10 April 2019

Microbes are the basis of the plankton communities and marine food webs. In order to grow and support their metabolism, these microbes require nutrients typically found dissolved in seawater. However, in the open ocean, away from land and coasts, the supply of a key nutrient for microbes, phosphate, can be very scarce and yet microbes have adapted to live in these ecosystems. This study uses metagenomics data to quantify genes that allow marine microbes to scavenge phosphate from organic compounds containing phosphorus. One of the genes quantified codes for an enzyme known as the carbon-phosphorus lyase which has evolved mainly in bacteria to breakdown phosphorus-containing compounds known as phosphonates. A key finding of this study was that the carbon-phosphorus lyase genes were highly selected for in parts of the ocean that contain very little phosphate. This result is relevant to understanding the role of the ocean in climate, because one of the byproducts released during phosphonate degradation is the greenhouse gas methane. The results of this study suggest that when the supply of phosphate is very low in oceanic waters, the potential release of methane by bacteria may increase.

Carrie Woods: Human disturbance impacts the integrity of sacred church forests, Ethiopia

Published: March 6, 2019

The presence of humans can profoundly change landscapes. In the South Gondar region of the northern highlands in Ethiopia, the last remaining forests are small fragments of 5 ha that surround churches. These forests are protected by the Ethiopian Orthodox Tewahido church, and are integral to their livelihoods and cultural heritage. In this paper we examined the influence of human presence on forest integrity and found that human disturbance negatively affected forest diversity and regeneration potential. Forest management strategies focusing on reducing trail systems and clearings within forests and conserving large trees as seed sources could benefit both the forest and church communities.

Andreas Madlung: Phytochrome A regulates carbon flux in dark grown tomato seedlings

27 February 2019

In this paper, we describe our findings that the plant-specific light receptor phytochrome appears to have functions even in the dark. Additionally, we show that phytochrome plays a role in the balancing of sucrose distribution in the germinating seedling.

Joel Elliot: A Novel Phagomyxid Parasite Produces Sporangia in Root Hair Galls of Eelgrass (Zostera marina)

Available online 10 December 2018.

As part of our research into the microbes living with native and introduced species of eelgrass, we used a combination of field research, microscopy, and genetics to discover a new type of protist that produces root hair galls in the native eelgrass species Zostera marina. We are continuing to study this protist and its effects on local eelgrass populations.

Joel K. Elliott, Hunter Simpson*, Alex Teesdale*, Amy Replogle, Marianne Elliott, Kathryn Coats, and Gary Chastagner. 2019. A Novel Phagomyxid Parasite Produces Sporangia in Root Hair Galls of Eelgrass (Zostera marina). Protist 170: 64-81.

Carrie Woods: Fertilization influences the nutrient acquisition strategy of a nomadic vine in a lowland tropical forest understory

Published: 11 August 2018

A nomadic vine in the light-limited understory showed a response to nutrient addition that suggests nutrient limitation. Thus, limitation by multiple factors seems to be the rule rather than the exception in many plant groups.

Woods, C. L., S. J. DeWalt, C. L. Cardelús, K. E. Harms, J. B. Yavitt, and S. J. Wright. (2018). Fertilization influences the nutrient acquisition strategy of a hemiepiphytic aroid in a lowland tropical forest understory. Plant and Soil.

Stacey Weiss: Do small classes in higher education reduce performance gaps in STEM?

Published: 27 June 2018

Does class size matter? Puget Sound was part of a multi-institution study to determine the effect of class size on performance in Introductory Biology class rooms. We found that as class sizes decreases, so does the gender gap in performance on high stakes exams. We also found that women tend to perform better than men on non-exam assignments, regardless of class size. These findings have important implications for equitable pedagogy and caps on classroom sizes.

Ballen, C.J., S. Aguillon, R. Brunelli, A.G. Drake, D. Wassenberg, S.L. Weiss, K.R. Zamudio, and S. Cotner. 2018. Do small classes in higher education reduce performance gaps in STEM? BioScience biy056

Stacey Weiss: Male mate choice as differential investment in contest competition is affected by female ornament expression

June 2018

Female striped plateau lizards express ornaments that may advertise the quality of the female and her future offspring to potential mates. In this paper, a senior thesis student and I asked whether males pay attention to this ornament and alter their behavior accordingly. By placing two males together with an ornamented female, we found that males perform more male-male display behaviors more quickly when in the presence of large-ornamented female. We discuss these results in the context of sexual selection on female traits and male mate choice.

Weiss, S.L. and M. Dubin*. 2018. Male mate choice as differential investment in contest competition is affected by female ornament expression. Current Zoology 64:335-344.

Mark Martin: Elementary Student Outreach Activity Demonstrating the Use of ‘Phage Therapy Heroes’ to Combat Bacterial Infections

Colored substances in four specimen trays: orange, brown, black, and green

30 March 2018

Developing a series of colorful and engaging elementary school exercises to promote the idea that some viruses can fight disease, as well appreciate the microbial world.

Breitbart, M., Malki, K., Sawaya, N.A., Bonnain, C., and M.O. Martin (2018). “Elementary Student Outreach Activity Demonstrating the Use of ‘Phage Therapy Heroes’ to Combat Bacterial Infections.” J. Microbiol. Bio. Education. 19(1). pii: 19.1.30. doi: 10.1128/jmbe.v19i1.1407

Joel Elliot: Size-dependent interference competition between two sea star species demographically affected by wasting disease

specimen suffering from sea star wasting disease

Online publication date: February 23, 2018

We have been studying the ecology of local sea star populations in Puget Sound and when sea star wasting disease (SSWD) influenced the survival of sea stars it provided an opportunity for us to examine interference competition between two species. Our results suggest that sea star wasting disease (SSWD) has decreased the intensity of potential competitive interactions between Pisaster and Evasteriasby reducing not only population density, but also body size. The ability of Pisaster to dominate Evasterias will likely depend on size related recovery success of each species from SSWD.

*Rogers TL, *Schultz HK, Elliott, JK. 2018. Size-dependent interference competition between two sea star species demographically affected by wasting disease. Mar. Ecol. Prog. Ser. 589: 167-177.

Andreas Madlung: Assessing an effective undergraduate module teaching applied bioinformatics to biology students

Andreas Madlung publication diagram, 2018

Published: January 11, 2018

In this paper I present a lab exercise I developed and tested with my students in here at the University of Puget Sound. I show results from assessing in what ways the exercise furthered student learning in bioinformatics and discuss the overall state of bioinformatics instruction in undergraduate Biology education.

Madlung, A. Assessing an effective undergraduate module teaching applied bioinformatics to biology students. (2018) PLoS Computational Biology 14(1): e1005872. https://doi.org/10.1371/journal.pcbi.1005872

Mark Martin: Complete Genome Sequence of the Predatory Bacterium Ensifer adhaerens Casida A

Published 22 November 2017

The first published genome of Ensifer, a predator of Gram positive bacteria. Though related to beneficial alpha proteobacteria, Ensifer has a number of interesting properties, including predation, synthesis of exopolysaccharide, and "tracking motility.

Williams, L.E., Baltrus, D.A., O’Donnell, S.D., Skelly, T.J., and M.O. Martin (2017). “Complete Genome Sequence of the Predatory Bacterium Ensifer adhaerens Casida A.” Genome Announc. 5: e01344-17.

Andreas Madlung: Natural variation in stress response gene activity in the allopolyploid Arabidopsis suecica

Andreas Madlung publication diagram, 2017

Published: 23 August 2017

In this paper we tested the hypothesis that allopolyploidization (the hybridization of two different species concurrent with genome duplication) not only is a pathway to instant speciation, but, possibly due to the genomic shock during the initial polyploid formation, might create diversity early on in the evolution of the new species. We identify a large number of stress-response related genes, including genes responding to drought stress, that are differentially expressed between sister populations of the same cross. We conclude that allopolyploidy might allow these sister populations to functionally diverge from each other – for example in dry versus wet conditions - and might provide a mechanism for niche specialization as a first step towards speciation.

Carlson, KD, Fernandez-Pozo, N, Bombarely, A, Pisupati, R., Mueller, LA, Madlung, A. Natural variation in stress response gene activity in the allopolyploid Arabidopsis suecica. (2017) BMC Genomics 18:653 doi.org/10.1186/s12864-017-4067-x

Carrie Woods: Primary ecological succession in vascular epiphytes: the species accumulation model.

First published: 21 April 2017

As trees increase in size, they create microhabitats that enable more and more epiphyte species to accumulate in the tree crown. This paper examines epiphyte succession at two scales: the inner crown whereby it follows replacement models and the entire tree crown whereby it follows a species accumulation model.

Woods, C. L. (2017) Primary ecological succession in vascular epiphytes: the species accumulation model. Biotropica 49:452-460.

Carrie Woods: Shadow conservation and the persistence of church forests in Northern Ethiopia

First published: 10 April 2017

In the south Gondar region of northern Ethiopia the remaining forests are protected because they surround churches and are an integral component of the Ethiopian Orthodox Tewahido church. We found that these forests have persisted on the landscape and increased in area over the past 50 years. However, forests have a high degree of human presence and some were increasing due to the planting of exotic Eucalyptus, which could compromise their continued persistence on the landscape.

Cardelús, C. L., P. Scull, A. Wassie Eshete, C.L. Woods, P. Klepeis E. Kent and I. Orlowska. (2017) Shadow conservation and the persistence of church forests in Northern Ethiopia. Biotropica 49:726-733.

Carrie Woods: Stone walls and sacred forest conservation in Ethiopia

Published: 31 October 2016

The church community has built walls around some of their sacred forests in northern Ethiopia. Walls benefited the seedlings of many tree species but some trees will require facilitated regeneration.

Woods, C. L., C. L. Cardelús, P. S. Scull, A. Wassie, M. Baez*, and P. Klepeis. (2017) Stone walls and sacred forest conservation in Ethiopia. Biodiversity and Conservation 26:209-221.