Integrative Biology Commons^™

The Influence Of Landscape And Environmental Factors On Ranavirus Epidemiology In A California Amphibian Assemblage, Brian J. Tornabene, Andrew R. Blausten, Cheryl J. Briggs, Dana M. Calhoun, Pieter T. J. Johnson, Travis Mcdevitt-Galles, Jason R. Rohr, Jason T. Hoverman

Integrative Biology Faculty and Staff Publications

1. A fundamental goal of disease ecology is to determine the landscape and environmental processes that drive disease dynamics at different biological levels to guide management and conservation. Although ranaviruses (family Iridoviridae) are emerging amphibian pathogens, few studies have conducted comprehensive field surveys to assess potential drivers of ranavirus disease dynamics.
2. We examined the factors underlying patterns in site‐level ranavirus presence and individual‐level ranavirus infection in 76 ponds and 1,088 individuals representing five amphibian species within the East Bay region of California.
3. Based on a competing‐model approach followed by variance partitioning, landscape and biotic variables explained the most variation in …

Using Multi‐Response Models To Investigate Pathogen Coinfections Across Scales: Insights From Emerging Diseases Of Amphibians, William E. Stutz, Andrew R. Blaustein, Cheryl J. Briggs, Jason T. Hoverman, Jason R. Rohr, Pieter T. J. Johnson

Integrative Biology Faculty and Staff Publications

1. Associations among parasites affect many aspects of host–parasite dynamics, but a lack of analytical tools has limited investigations of parasite correlations in observational data that are often nested across spatial and biological scales.
2. Here we illustrate how hierarchical, multiresponse modelling can characterize parasite associations by allowing for hierarchical structuring, offering estimates of uncertainty and incorporating correlational model structures. After introducing the general approach, we apply this framework to investigate coinfections among four amphibian parasites (the trematodes Ribeiroia ondatrae and Echinostoma spp., the chytrid fungus Batrachochytrium dendrobatidis and ranaviruses) and among >2,000 individual hosts, 90 study sites and five amphibian host …

Do Host‐Associated Gut Microbiota Mediate The Effect Of An Herbicide On Disease Risk In Frogs?, Sarah A. Knutie, Caitlin R. Gabor, Kevin D. Kohl, Jason R. Rohr

Integrative Biology Faculty and Staff Publications

1. Environmental stressors, such as pollutants, can increase disease risk in wildlife. For example, the herbicide atrazine affects host defences (e.g. resistance and tolerance) of the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd), but the mechanisms for these associations are not entirely clear. Given that pollutants can alter the gut microbiota of hosts, which in turn can affect their health and immune systems, one potential mechanism by which pollutants could increase infection risk is by influencing host‐associated microbiota.
2. Here, we test whether early‐life exposure to the estimated environmental concentration (EEC; 200 μg/L) of atrazine affects the gut bacterial composition of …

Agrochemicals Increase Risk Of Human Schistosomiasis By Supporting Higher Densities Of Intermediate Hosts, Neal T. Halstead, Christopher M. Hoover, Arathi Arakala, David J. Civitello, Guilio A. De Leo, Manoj Gambhir, Steve A. Johnson, Nicolas Jouanard, Kristin A. Loerns, Karena Nguyen, Jason R. Rohr

Integrative Biology Faculty and Staff Publications

Schistosomiasis is a snail-borne parasitic disease that ranks among the most important water-based diseases of humans in developing countries. Increased prevalence and spread of human schistosomiasis to non-endemic areas has been consistently linked with water resource management related to agricultural expansion. However, the role of agrochemical pollution in human schistosome transmission remains unexplored, despite strong evidence of agrochemicals increasing snail-borne diseases of wildlife and a projected 2- to 5-fold increase in global agrochemical use by 2050. Using a field mesocosm experiment, we show that environmentally relevant concentrations of fertilizer, a herbicide, and an insecticide, individually and as mixtures, increase densities …

The Ecology And Economics Of Restoration: When, What, Where, And How To Restore Ecosystems, Jason R. Rohr, Emily S. Bernhardt, Marc W. Cadotte, William H. Clements

Integrative Biology Faculty and Staff Publications

Restoration ecology has provided a suite of tools for accelerating the recovery of ecosystems damaged by drivers of global change. We review both the ecological and economic concepts developed in restoration ecology, and offer guidance on when, what, where, and how to restore ecosystems. For when to restore, we highlight the value of pursuing restoration early to prevent ecosystems from crossing tipping points and evaluating whether unassisted natural recovery is more cost-effective than active restoration. For what to restore, we encourage developing a restoration plan with stakeholders that will restore structural, compositional, and functional endpoints, and whose goal is a …

A Faculty Professional Development Model That Improves Student Learning, Encourages Active-Learning Instructional Practices, And Works For Faculty At Multiple Institutions, Karen N. Pelletrau, Jennifer K. Knight, Paula P. Lemons, Jill S. Mccourt, John E, Merrill, Ross H. Nehm, Luanna B Prevost, Mark Urban-Lurain, Michelle K. Smith

Integrative Biology Faculty and Staff Publications

Helping faculty develop high-quality instruction that positively affects student learning can be complicated by time limitations, a lack of resources, and inexperience using student data to make iterative improvements. We describe a community of 16 faculty from five institutions who overcame these challenges and collaboratively designed, taught, iteratively revised, and published an instructional unit about the potential effect of mutations on DNA replication, transcription, and translation. The unit was taught to more than 2000 students in 18 courses, and student performance improved from preassessment to postassessment in every classroom. This increase occurred even though faculty varied in their instructional practices …

Resilience In Moving Water: Effects Of Turbulence On The Predatory Impact Of The Lobate Ctenophore Mnemiopsis Leidyi, Cornelia Jaspers, John H. Costello, Kelly R. Sutherland, Brad J. Gemmell, Kelsey N. Lucas, Jennifer Tackett, Kara Dodge, Sean P. Colin

Integrative Biology Faculty and Staff Publications

Despite its delicate morphology, the lobate ctenophore Mnemiopsis leidyi thrives in coastal ecosystems as an influential zooplankton predator. Coastal ecosystems are often characterized as energetic systems with high levels of natural turbulence in the water column. To understand how natural wind‐driven turbulence affects the feeding ecology of M. leidyi, we used a combination of approaches to quantify how naturally and laboratory generated turbulence affects the behavior, feeding processes and feeding impact of M. leidyi. Experiments using laboratory generated turbulence demonstrated that turbulence can reduce M. leidyi feeding rates on copepods and Artemia nauplii by > 50%. However, detailed feeding …

Author Correction: Evolutionary History Of Plant Hosts And Fungal Symbionts Predicts The Strength Of Mycorrhizal Mutualism, Jason D. Hoeksema, James D. Bever, Sounak Chakraborty, V. Bala Chaudhary, Monique Gardes, Catherine A. Gehring, Miranda M. Hart, Elizabeth A. Housworth, Wittaya Kaonongbua, Marc J. Lajeunesse

Integrative Biology Faculty and Staff Publications

In the original published version of the article, the description of the fixed-effect predictor Inoculum Complexity presented in the Methods was incorrect. The incorrect description given was: “single fungal genus, multiple fungal genera, or whole soil inoculum”. The correct description is: “single fungal species, multiple fungal species, or whole soil inoculum”. The error does not affect any of the results presented in the paper. The correction has been made to the HTML and PDF versions of the paper.

Changing Measurements Or Changing Movements? Sampling Scale And Movement Model Identifiability Across Generations Of Biologging Technology, Leah R. Johnson, Philipp H. Boersch-Supan, Richard A. Phillips, Sadie J. Ryan

Integrative Biology Faculty and Staff Publications

Animal movement patterns contribute to our understanding of variation in breeding success and survival of individuals, and the implications for population dynamics. Over time, sensor technology for measuring movement patterns has improved. Although older technologies may be rendered obsolete, the existing data are still valuable, especially if new and old data can be compared to test whether a behavior has changed over time. We used simulated data to assess the ability to quantify and correctly identify patterns of seabird flight lengths under observational regimes used in successive generations of wet/dry logging technology. Care must be taken when comparing data collected …

Genetic And Epigenetic Variation In Spartina Alterniflora Following The Deepwater Horizon Oil Spill, Marta Robertson, Aaron Schrey, Ashley Shayter, Christina J. Moss, Christina Richards

Integrative Biology Faculty and Staff Publications

Catastrophic events offer unique opportunities to study rapid population response to stress in natural settings. In concert with genetic variation, epigenetic mechanisms may allow populations to persist through severe environmental challenges. In 2010, the Deepwater Horizon oil spill devastated large portions of the coastline along the Gulf of Mexico. However, the foundational salt marsh grass, Spartina alterniflora, showed high resilience to this strong environmental disturbance. Following the spill, we simultaneously examined the genetic and epigenetic structure of recovering populations of S. alterniflora to oil exposure. We quantified genetic and DNA methylation variation using amplified fragment length polymorphism and methylation …

Microbe Biogeography Tracks Water Masses In A Dynamic Oceanic Frontal System, Anni Djurhuus, Philipp H. Boersch-Supan, Svein-Ole Mikalse, Alex D. Rogers

Integrative Biology Faculty and Staff Publications

Dispersal limitation, not just environmental selection, plays an important role in microbial biogeography. The distance–decay relationship is thought to be weak in habitats where dispersal is high, such as in the pelagic environment, where ocean currents facilitate microbial dispersal. Most studies of microbial community composition to date have observed little geographical heterogeneity on a regional scale (100 km). We present a study of microbial communities across a dynamic frontal zone in the southwest Indian Ocean and investigate the spatial structure of the microbes with respect to the different water masses separated by these fronts. We collected 153 samples of free-living …

Suitability Of Laurentian Great Lakes For Invasive Species Based On Global Species Distribution Models And Local Habitat, Andrew M. Kramer, Gust Annis, Marion E. Wittmann, William L. Chadderton, Edward S. Rutherford, David M. Lodge, Lacey Mason, Dmitry Beletsky, Catherine Riseng, John M. Drake

Integrative Biology Faculty and Staff Publications

Efficient management and prevention of species invasions requires accurate prediction of where species of concern can arrive and persist. Species distribution models provide one way to identify potentially suitable habitat by developing the relationship between climate variables and species occurrence data. However, these models when applied to freshwater invasions are complicated by two factors. The first is that the range expansions that typically occur as part of the invasion process violate standard species distribution model assumptions of data stationarity. Second, predicting potential range of freshwater aquatic species is complicated by the reliance on terrestrial climate measurements to develop occurrence relationships …

Accuracy Of Climate-Based Forecasts Of Pathogen Spread, Annakate M. Schatz, Andrew M. Kramer, John M. Drake

Integrative Biology Faculty and Staff Publications

Species distribution models (SDMs) are a tool for predicting the eventual geographical range of an emerging pathogen. Most SDMs, however, rely on an assumption of equilibrium with the environment, which an emerging pathogen, by definition, has not reached. To determine if some SDM approaches work better than others for modelling the spread of emerging, non-equilibrium pathogens, we studied time-sensitive predictive performance of SDMs for Batrachochytrium dendrobatidis, a devastating infectious fungus of amphibians, using multiple methods trained on time-incremented subsets of the available data. We split our data into timeline-based training and testing sets, and evaluated models on each set …

Human-Associated Bacteroides Spp. And Human Polyomaviruses As Microbial Source Tracking Markers In Hawaii, Marek Kirs, Roberto A Caffaro-Filho, Mayee Wong, Valerie J. Harwood, Philip Moravcik, Roger S Fujioka

Integrative Biology Faculty and Staff Publications

Identification of sources of fecal contaminants is needed to (i) determine the health risk associated with recreational water use and (ii) implement appropriate management practices to mitigate this risk and protect the environment. This study evaluated human-associated Bacteroides spp. (HF183TaqMan) and human polyomavirus (HPyV) markers for host sensitivity and specificity using human and animal fecal samples collected in Hawaii. The decay rates of those markers and indicator bacteria were identified in marine and freshwater microcosms exposed and not exposed to sunlight, followed by field testing of the usability of the molecular markers. Both markers were strongly associated with sewage, although …

Home-Field Advantage? Evidence Of Local Adaptation Among Plants, Soil, And Arbuscular Mycorrhizal Fungi Through Meta-Analysis, Megan A. Rúa, Anita Antoninka, Pedro M. Antunes, V Bala Chaudhary, Catherine Gehring, Louis J. Lamit, Bridget J. Piculell, James D. Bever, Cathy Zabinski, James F. Meadow, Marc J. Lajeunesse, Brook G. Milligan, Justine Karst, Jason D. Hoeksema

Integrative Biology Faculty and Staff Publications

BACKGROUND: Local adaptation, the differential success of genotypes in their native versus foreign environment, arises from various evolutionary processes, but the importance of concurrent abiotic and biotic factors as drivers of local adaptation has only recently been investigated. Local adaptation to biotic interactions may be particularly important for plants, as they associate with microbial symbionts that can significantly affect their fitness and may enable rapid evolution. The arbuscular mycorrhizal (AM) symbiosis is ideal for investigations of local adaptation because it is globally widespread among most plant taxa and can significantly affect plant growth and fitness. Using meta-analysis on 1170 studies …

Current Status Of Marker Genes Of Bacteroides And Related Taxa For Identifying Sewage Pollution In Environmental Waters, Warish Ahmed, Bridie Hughes, Valerie J. Harwood

Integrative Biology Faculty and Staff Publications

Microbial source tracking (MST) endeavors to determine sources of fecal pollution in environmental waters by capitalizing on the association of certain microorganisms with the gastrointestinal tract and feces of specific animal groups. Several decades of research have shown that bacteria belonging to the gut-associated order Bacteroidales, and particularly the genus Bacteroides, tend to co-evolve with the host, and are, therefore, particularly suitable candidates for MST applications. This review summarizes the current research on MST methods that employ genes belonging to Bacteroidales/Bacteroides as tracers or “markers” of sewage pollution, including known advantages and deficiencies of the many polymerase chain …

Transforming Ecosystems: When, Where, And How To Restore Contaminated Sites, Jason R. Rohr, Aïda M. Farag, Marc W. Cadotte, William H. Clements, James R. Smith, Cheryl P. Ulrich, Richard Woods

Integrative Biology Faculty and Staff Publications

Chemical contamination has impaired ecosystems, reducing biodiversity and the provisioning of functions and services. This has spurred a movement to restore contaminated ecosystems and develop and implement national and international regulations that require it. Nevertheless, ecological restoration remains a young and rapidly growing discipline and its intersection with toxicology is even more nascent and underdeveloped. Consequently, we provide guidance to scientists and practitioners on when, where, and how to restore contaminated ecosystems. Although restoration has many benefits, it also can be expensive, and in many cases systems can recover without human intervention. Hence, the first question we address is: "When …

Hunting, Food Subsidies, And Mesopredator Release: The Dynamics Of Crop-Raiding Baboons In A Managed Landscape, Rachel A. Taylor, Sadie J. Ryan, Justin S. Brashares, Leah R. Johnson

Integrative Biology Faculty and Staff Publications

The establishment of protected areas or parks has become an important tool for wildlife conservation. However, frequent occurrences of human-wildlife conflict at the edges of these parks can undermine their conservation goals. Many African protected areas have experienced concurrent declines of apex predators alongside increases in both baboon abundance and the density of humans living near the park boundary. Baboons then take excursions outside of the park to raid crops for food, conflicting with the human population. We model the interactions of mesopredators (baboons), apex predators, and shared prey in the park to analyze how four components affect the proportion …

Combined Effects Of Pesticides And Trematode Infections On Hourglass Tree Frog Polypedates Cruciger., Uthpala A. Jayawardena, Jason R. Rohr, Ayanthi N. Navaratne, Priyanie H. Amerasinghe, Rupika S. Rajakaruna

Integrative Biology Faculty and Staff Publications

The impact of widespread and common environmental factors, such as chemical contaminants, on infectious disease risk in amphibians is particularly important because both chemical contaminants and infectious disease have been implicated in worldwide amphibian declines. Here we report on the lone and combined effects of exposure to parasitic cercariae (larval stage) of the digenetic trematode, Acanthostomum burminis, and four commonly used pesticides (insecticides: chlorpyrifos, dimethoate; herbicides: glyphosate, propanil) at ecologically relevant concentrations on the survival, growth, and development of the common hourglass tree frog, Polypedates cruciger Blyth 1852. There was no evidence of any pesticide-induced mortality on cercariae because all …

Darwinian Sex Roles Confirmed Across The Animal Kingdom, Tim Janicke, Ines K. Häderer, Marc J. Lajeunesse, Nils Anthes

Integrative Biology Faculty and Staff Publications

Since Darwin's conception of sexual selection theory, scientists have struggled to identify the evolutionary forces underlying the pervasive differences between male and female behavior, morphology, and physiology. The Darwin-Bateman paradigm predicts that anisogamy imposes stronger sexual selection on males, which, in turn, drives the evolution of conventional sex roles in terms of female-biased parental care and male-biased sexual dimorphism. Although this paradigm forms the cornerstone of modern sexual selection theory, it still remains untested across the animal tree of life. This lack of evidence has promoted the rise of alternative hypotheses arguing that sex differences are entirely driven by environmental …

Dynamics And Thermal Sensitivity Of Ballistic And Non-Ballistic Feeding In Salamanders, Stephen M, Deban, Jeffrey A. Scales

Integrative Biology Faculty and Staff Publications

Low temperature reduces the performance of muscle-powered movements, but in movements powered by elastic recoil mechanisms, this effect can be mitigated and performance can be increased. To better understand the morphological basis of high performance and thermal robustness of elastically powered movements, we compared feeding dynamics at a range of temperatures (5-25°C) in two species of terrestrial plethodontid salamanders, Plethodon metcalfi and Ensatina eschscholtzii, which differ in tongue muscle architecture and the mechanism of tongue projection. We found that Ensatina is capable of ballistic projection with a mean muscle mass-specific power of 2100 W kg(-1), revealing an elastic mechanism. Plethodon, …

Predator Diet And Trophic Position Modified With Altered Habitat Morphology, Alexander Tewfik, Susan S. Bell, Kevin S. Mccann, Kristina Morrow

Integrative Biology Faculty and Staff Publications

Empirical patterns that emerge from an examination of food webs over gradients of environmental variation can help to predict the implications of anthropogenic disturbance on ecosystems. This “dynamic food web approach” is rarely applied at the coastal margin where aquatic and terrestrial systems are coupled and human development activities are often concentrated. We propose a simple model of ghost crab (Ocypode quadrata) feeding that predicts changing dominant prey (Emerita talpoida, Talorchestia sp., Donax variablis) along a gradient of beach morphology and test this model using a suite of 16 beaches along the Florida, USA coast. …

Ultrafiltration And Microarray For Detection Of Microbial Source Tracking Marker And Pathogen Genes In Riverine And Marine Systems, Xiang Li, Valerie J. Harwood, Bina Nayak, Jennifer L Weidhaas

Integrative Biology Faculty and Staff Publications

Pathogen identification and microbial source tracking (MST) to identify sources of fecal pollution improve evaluation of water quality. They contribute to improved assessment of human health risks and remediation of pollution sources. An MST microarray was used to simultaneously detect genes for multiple pathogens and indicators of fecal pollution in freshwater, marine water, sewage-contaminated freshwater and marine water, and treated wastewater. Dead-end ultrafiltration (DEUF) was used to concentrate organisms from water samples, yielding a recovery efficiency of > 95% for Escherichia coli and human polyomavirus. Whole-genome amplification (WGA) increased gene copies from ultrafiltered samples and increased the sensitivity of the microarray. …

Synthetic Biology Open Language (Sbol) Version 2.1.0, Zhen Zhang

Integrative Biology Faculty and Staff Publications

Synthetic biology builds upon the techniques and successes of genetics, molecular biology, and metabolic engineering by applying engineering principles to the design of biological systems. The field still faces substantial challenges, including long development times, high rates of failure, and poor reproducibility. One method to ameliorate these problems would be to improve the exchange of information about designed systems between laboratories. The Synthetic Biology Open Language (SBOL) has been developed as a standard to support the specification and exchange of biological design information in synthetic biology, filling a need not satisfied by other pre-existing standards. This document details version 2.1 …

Effects Of Nutrient Supplementation On Host-Pathogen Dynamics Of The Amphibian Chytrid Fungus: A Community Approach, Julia C. Buck, Jason R. Rohr, Andrew R. Blaustein

Integrative Biology Faculty and Staff Publications

1. Anthropogenic stressors may influence hosts and their pathogens directly or may alter host–pathogen dynamics indirectly through interactions with other species. For example, in aquatic ecosystems, eutrophication may be associated with increased or decreased disease risk. Conversely, pathogens can influence community structure and function and are increasingly recognised as important members of the ecological communities in which they exist.
2. In outdoor mesocosms, we experimentally manipulated nutrients (nitrogen and phosphorus) and the presence of a fungal pathogen, Batrachochytrium dendrobatidis (Bd), and examined the effects on Bd abundance on larval amphibian hosts (Pseudacris regilla: Hylidae), amphibian traits and community dynamics. We …

An Experiment In Graduate Education: A Marine Science Adventure Across The Indian Ocean, Vicki Buchsbaum Pearse, John C. Ogden, Sharon J. Proctor

Integrative Biology Faculty and Staff Publications

In the fall of 1964, Stanford University’s R/V Te Vega Cruise 5 crossed the equatorial Indian Ocean from Mombasa to Singapore, one of many ships participating in the International Indian Ocean Expedition. The cruise achieved two goals: (1) it provided hands-on oceanography training for graduate students in marine sciences, and (2) it documented the deep scattering layers of the Indian Ocean, only poorly known at the time. Taking place on the other side of the globe from the United States, the cruise also exposed students to cultural and personal experiences that shaped their lives and professions. It demonstrated the importance …

Spatial Spread Of The West Africa Ebola Epidemic, Andrew M. Kramer, J. Tomlin Pulliam, Laura W. Alexander, Andrew W. Park, Pejman Rohani, John M. Drake

Integrative Biology Faculty and Staff Publications

Controlling Ebola outbreaks and planning an effective response to future emerging diseases are enhanced by understanding the role of geography in transmission. Here we show how epidemic expansion may be predicted by evaluating the relative probability of alternative epidemic paths. We compared multiple candidate models to characterize the spatial network over which the 2013–2015 West Africa epidemic of Ebola virus spread and estimate the effects of geographical covariates on transmission during peak spread. The best model was a generalized gravity model where the probability of transmission between locations depended on distance, population density and international border closures between Guinea, Liberia …

Ordination Obscures The Influence Of Environment On Plankton Metacommunity Structure, Tad A. Dallas, Andrew M. Kramer, Marcus Zokan, John M. Drake

Integrative Biology Faculty and Staff Publications

The composition of plankton communities in individual habitats is often influenced by environmental conditions like pH or hydroperiod. At larger scales, environmental gradients can influence community structure across interconnected local communities. Detecting the role of environmental and spatial factors on metacommunity structure depends on the ordering of sites and species prior to analysis. We investigated this ordination in two wetland metacommunities; a well-sampled, hyper-diverse zooplankton metacommunity, and a Central American phytoplankton metacommunity. We calculated coherence, turnover, and boundary clumping to classify the structure of the metacommunity, and we propose a statistic that responds to variation in both coherence and turnover. …

Mathematical Models Are A Powerful Method To Understand And Control The Spread Of Huanglongbing, Rachel A. Taylor, Erin Mordecai, Christopher A. Gilligan, Jason R. Rohr, Leah R. Johnson

Integrative Biology Faculty and Staff Publications

Huanglongbing, or citrus greening, is a global citrus disease occurring in almost all citrus growing regions and causing substantial economic burdens to individual growers, citrus industries and governments. Successful management strategies to reduce disease burden are desperately needed but with so many possible interventions and combinations thereof, it is difficult to know which are worthwhile or cost-effective. We review how mathematical models have yielded useful insights into controlling disease spread for other vector-borne plant diseases, and the small number of mathematical models of Huanglongbing. We adapt a malaria model to Huanglongbing, by including temperature-dependent psyllid traits and economic costs, to …

The Pros And Cons Of Ecological Risk Assessment Based On Data From Different Levels Of Biological Organization, Jason R. Rohr, Christopher J. Salice, Roger M. Nisbet

Integrative Biology Faculty and Staff Publications

Ecological risk assessment (ERA) is the process used to evaluate the safety of manufactured chemicals to the environment. Here we review the pros and cons of ERA across levels of biological organization, including suborganismal (e.g., biomarkers), individual, population, community, ecosystem and landscapes levels. Our review revealed that level of biological organization is often related negatively with ease at assessing cause-effect relationships, ease of high-throughput screening of large numbers of chemicals (it is especially easier for suborganismal endpoints), and uncertainty of the ERA because low levels of biological organization tend to have a large distance between their measurement (what is quantified) …