Global Ecology and Conservation 16 (2018) e00441

Contents lists available at ScienceDirect

Global Ecology and Conservation

journal homepage: http://www.elsevier.com/locate/gecco

Review Paper

Identifying management-relevant research priorities for

responding to disease-associated amphibian declines
Evan H. Campbell Grant a, *, Michael J. Adams b, 1, Robert N. Fisher c,
Daniel A. Grear d, Brian J. Halstead e, Blake R. Hossack f, Erin Muths g,
Katherine L.D. Richgels d, Robin E. Russell d, Kelly L. Smalling h,
J. Hardin Waddle i, Susan C. Walls i, C. LeAnn White d
a
U.S. Geological Survey, Patuxent Wildlife Research Center, SO Conte Anadromous Fish Research Lab, 1 Migratory Way, Turners Falls, MA,
01376, USA
b
U.S. Geological Survey, Forest and Rangeland Ecosystem Science Center, Corvallis, OR, 97331, USA
c
U.S. Geological Survey, Western Ecological Research Center, San Diego, CA, 92101, USA
d
U.S. Geological Survey National Wildlife Health Center, 6006 Schroeder Rd, Madison, WI, 53711, USA
e
U.S. Geological Survey, Western Ecological Research Center, Dixon, CA, 95620, USA
f
U.S. Geological Survey, Northern Rocky Mountain Science Center, Missoula, MT, 59801, USA
g
U.S. Geological Survey, Fort Collins Science Center, Fort Collins, CO, 80526, USA
h
U.S. Geological Survey, New Jersey Water Science Center, Lawrenceville, NJ, 08648, USA
i
U.S. Geological Survey, Wetland and Aquatic Research Center, Gainesville, FL, 32653, USA

a r t i c l e i n f o a b s t r a c t

Article history: A research priority can be defined as a knowledge gap that, if resolved, identifies the
Received 5 April 2018 optimal course of conservation action. We (a group of geographically distributed and
Accepted 12 September 2018 multidisciplinary research scientists) used tools from nominal group theory and decision
analysis to collaboratively identify and prioritize information needs within the context of
disease-associated amphibian decline, in order to develop a strategy that would support
US management agency needs. We developed iterated influence diagrams to create and
assess a unified research strategy. We illustrated a transparent process for identifying
specific knowledge gaps in amphibian disease ecology relevant to environmental man-
agement, and then constructed a research plan to address these uncertainties. The
resulting priorities include a need to: (1) understand the drivers of the community-disease
relationship, (2) determine the mechanisms by which exposure to contaminants influence
disease outcomes, (3) identify elements of terrestrial and aquatic habitats that stabilize
host-pathogen dynamics, (4) discuss how metapopulations may be managed to reduce the
speed and intensity of disease outbreaks, and (5) define the relationship between habitat
management and the environmental and host microbiomes. Along with identifying
research priorities for disease management, we present the details of the process used to
develop a consensus plan for addressing disease-related declines in amphibians on
federally managed lands of the United States.
Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).

* Corresponding author.
E-mail address: ehgrant@usgs.gov (E.H. Campbell Grant).
1
after the first author, contributors are listed alphabetically.

https://doi.org/10.1016/j.gecco.2018.e00441
2351-9894/Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
2 E.H. Campbell Grant et al. / Global Ecology and Conservation 16 (2018) e00441

1. Introduction

Emerging diseases of wildlife are increasing globally (Tompkins et al., 2015), making them an important consideration in
ecosystem management. Currently, our ability to manage outbreaks of disease in wildlife is limited (Altizer et al., 2003), and
identifying potential research routes to increase the breadth of options and improve the efficacy of management strategies is
needed. Understanding wildlife host-pathogen relationships is difficult due to many factors, including species-specific dif-
ferences in susceptibility, local conditions that affect both pathogen and host, and the complexity of disease transmission
cycles that often involve multiple hosts (Buhnerkempe et al., 2015; Keesing et al., 2010). While there is a large literature on
host-pathogen ecology, few effective actions have been identified to mitigate disease impacts on populations (Garner et al.,
2016).
Amphibians are among the most threatened groups of wildlife, and disease is a major factor in global amphibian declines
(Collins and Storfer, 2003). Despite a growing body of literature about the effects of diseases on amphibians, effective in-situ
management options for treating disease are difficult to identify (e.g., Canessa et al., 2018). Effectively removing a pathogen
from the environment or treating free-ranging individuals is exceptionally difficult (Oliver et al., 2015). As an alternative,
manipulating the environment to alter the effect of pathogens on host populations may be a potentially effective, yet
understudied, option. Environmental characteristics may affect hosts, pathogens, and host-pathogen interactions differently
(Leite et al., 2015; Roznik et al., 2015), especially if the pathogen has different microclimate and environmental tolerances
than the host. For example, for two pathogens of importance to US amphibians, evidence suggests even small changes in
water temperatures affect prevalence of Batrachochytrium dendrobatidis (Bd) infection (Forrest and Schlaepfer, 2011;
Woodhams et al., 2003), while other studies show ranaviruses may be unable to inoculate hosts after drying (Brunner et al.,
2007; Gray et al, 2009). Alternatively, environmental variables may influence a host's susceptibility to disease, e.g. by inducing
stress that leads to a suppression of immune function. Therefore, the environment plays a crucial role in the health of
amphibian populations, and persistence of the population could depend on several factors, including biotic (e.g., community
composition; Johnson et al., 2015), abiotic (e.g., water quality; Johnson et al., 2007), and/or anthropogenic factors (e.g.,
contaminants; Sparling et al., 2010). However, more research is needed to determine what type of habitat management may
be most effective for reducing disease risk in amphibian populations. Habitat management is expected to span multiple
dimensions, increasing the complexity of necessary information for making science-based decisions.
When research priorities cross disciplines and geographic regions, collaboration is necessary. To encourage consensus
decision making in selecting research directions, a transparent process is required to determine priorities (Huge
and
Mukherjee, 2018; Vennix, 1999). There are currently several approaches commonly used to identify research priorities.
Informal approaches use expert opinion to generate lists of perceived research needs. These rely on observations of patterns
and unexplained phenomena, without an explicit framework for linking observations and research questions (e.g., identifying
research priorities for the causative agent of amphibian chytridiomycosis, Batrachochytrium dendrobatidis (Bd): Leite et al.,
2015). Informal approaches are susceptible to bias, and lack transparency because they rely on individual expertise and
‘mental models’ of a system. They may result in a lack of consensus when individual reasoning is not supported by data or
made explicit (Huge
and Mukherjee, 2018). The most formal approaches require a decision problem to be framed directly
(e.g., through a structured decision making approach; Shea et al., 2014). In this case, research priorities are knowledge gaps
that, when resolved, influence the optimal course of action (i.e., provide the highest expected value of information; Runge
et al., 2011). When a particular decision cannot be framed explicitly, a nominal group theory (NGT) approach may be used,
which can generate research priorities through a process that is both democratic and semi-anonymous, encourages critical
reflection, improves the generation of creative ideas, and facilitates consensus-building (Huge
and Mukherjee, 2018; Tuffrey-
Wijne et al., 2016; Vennix, 1999).
As a research program within the U.S. Department of the Interior, the mission of the Amphibian Research and Monitoring
Initiative (ARMI) is to provide information that U.S. government agencies need to make decisions that directly or indirectly
affect amphibians. We combined tools from nominal group theory (Fink et al., 1984; Huge
and Mukherjee, 2018; Tuffrey-
Wijne et al., 2016) and influence diagrams (Howard and Matheson, 2005) to develop a rigorous and structured research
strategy to identify, address, and prioritize information needs to improve management of U.S. amphibian populations under
threat of disease. Throughout development of this strategy, we drew on our collective experience working in support of U.S.
Department of Interior agencies (Fish and Wildlife Service, National Park Service, Bureau of Land Management) and other
state and federal partners who have ongoing and close collaborative relationships with each author. We use this approach to
identify specific knowledge gaps in amphibian disease ecology relevant to environmental management, and develop research
priorities to address these uncertainties.

2. Materials and methods

Along with knowledge of local amphibian species and regionally varying habitats and threats, authors brought expertise in
hydrology, epidemiology, quantitative ecology, contaminants, amphibian pathogens (particularly Bd and ranavirus), and
forest, wetland, and stream ecology. We used a nominal group theory (NGT) consensus approach (Fink et al., 1984; Huge
and
Mukherjee, 2018) to articulate and organize research needs and identify those that are priorities for developing management
options (e.g., Tuffrey-Wijne et al., 2016) within the context of amphibian diseases affecting populations in the United States.
Application of NGT requires a diversity of expertise and proceeds along 4 major steps: (1) generating ideas, (2) sharing and
 E.H. Campbell Grant et al. / Global Ecology and Conservation 16 (2018) e00441 3

recording ideas, (3) group discussion, and (4) ranking and voting. We employed this approach rather than attempting to be
exhaustive in identifying knowledge gaps or uncertainties of amphibian disease systems, to synthesize information and
eliminate uncertainties that were not relevant to resource management. The nominal group theory approach has been used
successfully in healthcare and medicine (Fink et al., 1984; Tuffrey-Wijne et al., 2016; Wicki et al., 2016), but there are few
applications in wildlife management (Huge
and Mukherjee, 2018).
To encourage creativity, and to isolate the process of idea generation from critical evaluation, we applied our NGT approach
to develop a disease research strategy in two phases. The first was to generate and organize ideas, and the second was to
identify knowledge gaps and prioritize research needs (comprehensive steps of each phase are delineated below). With this
approach, we facilitated divergent and convergent thinking to most efficiently identify priority research needs that were
collaborative (Howard et al., 2008). During the process, we used facilitated discussion and iterated influence diagrams to
generate and organize ideas, that alternated between steps of creative discovery (divergence) and judgement and selection
(convergence). Previous research had indicated that the ability to find creative solutions is improved if multiple modes of
thinking are employed, especially when members of a group have different creative styles (Riding and Cheema, 1991). In
addition to working collaboratively as a large group through focused discussion, we frequently broke out in small groups to
tackle specific tasks. We varied small group membership with each step.

2.1. Phase one: generate and organize ideas

Our goal in phase one (Fig. 1) was to determine specific research questions that would be used to develop system diagrams
and lead to a prioritization of research gaps in phase two. As a starting point, we considered five major topics in amphibian-
pathogen systems. These topics included: host-pathogen dynamics, microbiota, environmental factors (including contami-
nants), mechanisms for spread and exposure, and mitigation and treatment for wild populations and habitats. Each of these
topics has a large body of supporting literature, and rather than conduct a formal synthesis of each, we used our experience
and knowledge to summarize the state of understanding for each topic, identify possible research opportunities, and list
challenges, constraints, and perceived barriers to conducting research under each topic. In this first divergence step, each
author independently enumerated perceived research needs within these topics, and small groups of 4e5 members syn-
thesized each into a ‘scoping’ document. The individual ‘scoping’ documents were then summarized across participants
within each topic. After individually reviewing these summarized documents, each person then articulated an additional 3e5
specific research questions that, if resolved, could improve our ability to implement management actions to increase the
persistence of amphibian populations in the presence of pathogens.
These questions were collated and circulated among all authors prior to a 2 day in-person working group, where authors
were randomly assigned to new small groups, with the task of identifying additional questions across topics (this expansive
list is given in Appendix Table 1). As a convergence exercise, we discussed performance criteria for ranking questions,
including perceived importance, relevance to informing specific management actions, and the ability to carry out research
with available expertise and facilities; small groups then discussed and ranked each question and then refined and

Fig. 1. Schematic of phase one of research strategy development through multiple linked phases of divergent and convergent thinking. From the five main pre-
determined topics, individuals enumerated research ideas. Ideas were grouped and summarized into like-topics and specific research questions were formulated.
Small groups ranked research questions. The top ranked questions relevant to local management were synthesized into the main topics that were analyzed in
phase two.
4 E.H. Campbell Grant et al. / Global Ecology and Conservation 16 (2018) e00441

organized the top-ranking questions (Fig. 1). Because more general questions can appear to have greater importance (as it is
easy to consider how they will maximally meet all performance metrics), the top-ranked questions were not useful as
research priorities, but did identify overarching topics (environmental contaminants, community composition and
structure, climate, habitat) from which more specific research needs could be identified. Groups were next asked to expand
these four topics into narratives with greater detail and specificity, in preparation for a second convergence step involving
organizing ideas using graphical aids.

2.2. Phase two: identify knowledge gaps and refine critical information needs

Our goal in phase two was to use influence diagrams with our four phase-one topics to identify knowledge gaps, which
would in turn enable us to prioritize research needs. The four main topics that phase one identified as factors expected to
influence the relationship between pathogen and host all have considerable support in the literature. Using these factors, we
developed detailed influence diagrams to describe the amphibian-disease system in greater detail. An influence diagram is
represented as a directed acyclic graph, which contains ‘nodes’ that are key stochastic processes, and ‘links’ that describe
functional relationships between two nodes (Howard and Matheson, 2005). Graphs may serve as the basis for quantitative
evaluation using Bayesian belief networks (e.g., Marcot et al., 2006) or as path diagrams in a structural equation modeling
approach (Grace, 2008). Influence diagrams have several uses in decision analysis, including (1) developing a shared un-
derstanding of a system (2) facilitating communication about a system, (3) integrating knowledge from diverse experts, (4)
clarifying thinking about processes and relationships of components of a dynamical system, and (5) identifying uncertainties
by articulating alternative hypotheses as pathways.

2.2.1. Developing influence diagrams to represent hypotheses of pathogen-host-environment relationships

As a first step in phase two, we self-organized (based on expertise) into subgroups that allowed us to explicitly identify
conceptual links important to each of four topics identified in phase 1. We did this by generating influence diagrams
describing the major cofactors in amphibian-disease systems via causal relationships (links) and responses (nodes). These
subgroups met via conference calls and used online collaboration software to modify each diagram in real time while
considering the system from their topical perspectives. All subgroups maintained two terminal nodes: ‘Disease’ and
‘Population Dynamics’, but otherwise developed influence diagrams independently (EHCG facilitated all subgroups).
Groups were asked to consider a series of questions to guide assessment of the influence diagram as they worked (Ap-
pendix Table 2).
While many of the resulting nodes and links were represented in multiple diagrams, the exercise revealed important
pathways only evident when considering each topic separately. We then simplified each topical influence diagram, developed
narratives to identify the major ecological processes, and combined all sub-diagrams into a single influence diagram with 7
connected nodes (Fig. 2).

Table 1
Summary of important links and narrative description of the hypothesized mechanism(s) represented in the influence sub-diagrams (comprising the 9
priority uncertainties), identified through phase 2 influence diagrams.

Sub- Important Link Hypothesized mechanism

diagram(s)
Contaminants Interaction between contaminants and disease Contaminants may affect host-pathogen interactions by weakening the immune system
of amphibians, or causing an inducible response that strengthens the resistance, but
little is known about how these interactions affect wild populations; these interactions
could be very important for population growth.
Contaminants Influence of contaminants on interspecific The effects of contaminants may differ among species, altering community structure.
(community) interactions
Contaminants Influence of contaminants on habitat quality Land use and habitat characteristics jointly influence exposure of amphibians to
contaminants.
Climate Influence of climate on habitat Local habitat characteristics mitigate the effects of climate (via temperature,
precipitation, and relative humidity), leading to different disease and population
outcomes.
Climate Interaction of climate on pathogen exposure Climate conditions may interact with host traits to affect changes in pathogen
and host susceptibility distribution and amphibian breeding phenology, changes in pathogen abundance, or
susceptibility of hosts to pathogens.
Community Outcome of community membership and Attributes of the vertebrate and microbial community (e.g., identity, richness, functional
structure on disease outcomes diversity, density) may change disease outcomes via multiple potential mechanisms.
Habitat/ Pathogen movement across landscape may be Metapopulation dynamics of pathogens interacts with landscape conditions and
Community habitat and community-dependent amphibian and other non-amphibian host metapopulations.
Habitat Habitat influences on amphibian population Habitat characteristics directly influence population dynamics (e.g., by affecting
dynamics developmental rates and the probability of successful metamorphosis).
Habitat Habitat characteristics can influence the Habitat affects abiotic conditions in both terrestrial and aquatic amphibian habitats (e.g.,
diversity of hosts found at a location. temperature and water availability) which affect amphibian and microbial (including
pathogen) species presence and abundance.
 E.H. Campbell Grant et al. / Global Ecology and Conservation 16 (2018) e00441 5

2.2.2. Using the influence diagrams for research prioritization

We met a second time in-person, to develop and use our influence diagrams to identify (1) key pieces of information
needed to mitigate the effect of disease on amphibian populations, and (2) parts of the system diagram considered most
important for influencing population outcomes under disease pressure. By conducting this evaluation in two steps, we were
able to separate uncertainty of a process from influence of the process on disease outcomes, to avoid common ‘psychological
traps’ (Gregory and Keeney, 2003) in developing research priorities.
We again divided into the 4 topical groups, and for each ecological process (represented as links), searched the
literature for evidence to support the hypothesized relationships. The point of this exercise was not to be exhaustive, but
to quickly identify areas where knowledge gaps exist, or where findings were contrary (indicating a need for additional
research). Hypotheses which had good support in the literature, those with limited but consistent findings, or those
where we had confidence in the existing findings were not further considered as knowledge gaps, and therefore not
research priorities.
Using this shared knowledge, each subgroup identified 2e3 links (i.e., ecological processes) that were most important in
each of the topic influence diagrams. This resulted in a list of 9 priority uncertainties across the sub-diagrams (main text Table
1), which were the combination of uncertain and important ecological processes linking disease and amphibian population
persistence. These key uncertainties were the topics that we determined would be most productive for informing man-
agement, and after specifying research plans for each, would comprise our research strategy.

3. Results

By employing tools from nominal group theory (phase one) and using influence diagrams (phase two) to articulate and
organize important ecological processes underlying amphibian-disease systems, we identified nine knowledge gaps (Table 1),

Fig. 2. Simplified influence diagram. Nodes (ovals) represent environmental factors and links (arrows) represent the relationship between nodes, leading to two
focal nodes of principle concern in identifying the causes of amphibian decline: Disease and Population Dynamics (hexagons). Some links are represented
multiple times because different subgroups identified similar links (but hypotheses describing the links differed depending on which subgroup added the link;
arrows are colored according to the subgroup). Every group started with a link between Disease and Population Dynamics (gray link). Each link was associated
with a description of the processes linking two nodes. For example, Contaminants ⋄ Habitat: The kind and concentration of contaminants can influence certain
abiotic conditions in a habitat. Habitat ⋄ Disease: Abiotic variables (including water quality) within a habitat directly affect colonization, growth, and survival of
pathogenic and anti-pathogenic members of a microbial community on a host. Habitat ⋄ Community: Water quality is a result of upland and pond characteristics,
and upland characteristics influence load and growth of pathogen on non-aquatic stages of amphibians (and other vertebrate hosts in the community); these
conditions also influence population dynamics within the community; habitat patches (amphibian and pathogen populations) are connected via host dispersal.
6 E.H. Campbell Grant et al. / Global Ecology and Conservation 16 (2018) e00441

representing priorities for clarifying mechanisms and cofactors driving these systems. We collaboratively selected the five
most immediate priorities for the development of research plans but consider all nine as elements of a long-term research
strategy. Addressing these priorities will help identify management actions to reduce the impact of disease on amphibian
populations on federally managed lands in the US.
Our resulting five research priorities are expanded on here:

3.1. What are the drivers of community-disease relationships?

Currently there is debate in the ecological literature regarding the relationship of community diversity, pathogen diversity,
disease prevalence, and disease intensity. Increasing host diversity can be associated with increased parasite and pathogen
diversity (diversity begets diversity hypothesis, Johnson et al., 2015). However, increasing biodiversity can be associated with
reduced prevalence or intensity of diseases in focal hosts (i.e., the dilution effect, Keesing et al., 2010), but alternatively, may
lead to amplification (Randolph and Dobson, 2012). Strauss et al. (2015) demonstrate how increasing community diversity
can result in a reduction in disease risk, increase disease risk, or have no effect on disease dynamics, indicating that the
composition of the community, as well as the ability of each member to transmit disease, may be as important as the number
of species in the community. In contrast, Johnson et al. (2015) present three hypothetical and non-exclusive mechanisms for
how community diversity may affect disease in a focal host. These hypotheses predict changes in pathogen transmission rates
by changing the density of susceptible hosts in the community (susceptible host reduction or augmentation), the contact rates
of infected and susceptible individuals (encounter reduction or augmentation) or the density of infected hosts (infected host
reduction or augmentation).
Attempts to quantify the relationship between biodiversity and disease in nature include correlational studies that esti-
mate disease risk by relating diversity to the density of infected hosts or force of infection. However, efforts to estimate the
three components of the diversity - disease relationship are needed to be able to determine the driving mechanisms and
relate them to interventions. Priority questions include:

a. What is the effect of amphibian community diversity on pathogen abundance and prevalence?
b. Does the strength and direction of the diversity - disease relationship vary by region, species identity, or host
competency?

3.2. Does exposure to environmentally available chemicals cause immunomodulation in amphibians, resulting in increased disease
risk?

Evaluating sub-lethal effects of disease, contaminants and their synergistic effects on amphibians is an important step in
determining the relationship between contaminants in the environment and disease susceptibility in exposed amphibians.
Metabolomics is the study of all metabolites present in cells, tissues, organs, biological fluids or organisms. This technique
has been used successfully in the human and veterinary medical fields to investigate contaminant exposure, impacts of diet
on health, individual disease states and immune responses and to evaluate risk factors for disease (Voge et al., 2016). For
amphibians, differences in metabolites among cohorts within a population (those exposed and unexposed to combinations
of pathogen and contaminants) are expected to indicate specific processes such as exposure, upregulation or suppression of
the immune system, and may serve as a biomarker of disease risk. Such techniques will increase our understanding of the
potential immunosuppressive effects of several known and emerging contaminants on amphibians. Priority questions
include:

a. Do commonly occurring chemicals cause immunosuppression in amphibians?

b. Does chemical-induced immunosuppression increase probability of disease?

3.3. Which habitat characteristics most influence amphibian disease outcomes?

Habitat characteristics likely affect disease outcomes by structuring pathogen communities and affecting host-pathogen
interactions. In contrast to treatments applied to individuals, environmental manipulations that alter habitat or community
characteristics to change host-pathogen interactions may reduce disease risk (Wobeser, 2002). For example, manipulating
temperatures in amphibian habitats might affect the outcome of host-Bd interactions because of the pathogen's thermal
constraints (Woodhams et al., 2003) or the host's physiological responses to changes in temperature (Andre et al., 2008). In
particular, habitat manipulation is a potential option for managing pathogens that have an environmental reservoir. Specific
questions include:

a. What are important habitat characteristics that mediate the occurrence and prevalence of pathogens?
b. What habitat characteristics correspond with variation in pathogen load on individual hosts?
 E.H. Campbell Grant et al. / Global Ecology and Conservation 16 (2018) e00441 7

3.4. Can host metapopulation structure and dynamics predict the distribution and spread of an amphibian pathogen?

Knowledge of host and pathogen metapopulation dynamics are key for forecasting epidemic potential of diseases and

and Jones, 2010). To understand metapopulation dynamics of both host and
developing disease mitigation strategies (Salathe
pathogen, we need information on the rates and patterns of spread and the environmental factors that facilitate or impede
host and pathogen movement. Host movement affects the distribution of pathogens on a landscape for pathogens that are
transmitted directly. Once a pathogen reaches a new patch, its ability to persist (either on the host or in the environment) and
be transmitted to new susceptible hosts (directly or indirectly), is also influenced by characteristics of the environment and
the host.
A fundamental question is the extent to which describing host metapopulation structure leads to improved predictions
of pathogen distribution and potential for spread. By identifying network structure and movement patterns of host species,
and the degree to which host metapopulation dynamics inform pathogen metapopulation structure, we can improve
predictions on the temporal and spatial spread of disease. This information can be incorporated into disease spread models
to understand if transmission pathways can be interrupted to limit spread of disease by hosts, and to predict which sites are
the most likely to remain disease-free for reintroductions or maintenance of sensitive species. Research questions under
this topic include:

a. How correlated are amphibian host and pathogen metapopulation dynamics?

b. Which transmission pathways are most important to metapopulation-level disease spread and persistence?

3.5. Can habitat management influence the amphibian skin microbiome, improving disease outcomes?

Because the microbial community of amphibian skin (microbiome) can reduce susceptibility to pathogens (Lauer et al.,
2007), determining how local environmental variation shapes microbial communities is an emerging field of significant
importance. The skin microbiome is complex and can vary according to host species, life stage, sex, habitat features, and study
area (Kueneman et al., 2014). Although >2000 microbes with anti-Bd properties have been identified (Woodhams et al.,
2015), most research on the amphibian microbiome has focused on a small number of amphibian species or small study areas.
How environmental characteristics, including the presence of contaminants and other stressors, shape amphibian
microbiomes at both the level of communities (microbial and amphibian) and individuals is still largely unknown. Further,
most studies of the role of the microbiome in infection have occurred in laboratory settings and there remains limited un-
derstanding of how well the microbiome buffers wild animals from infection or disease. Characterizing variation in
environment-host microbial communities, measuring the susceptibility of microbiomes to contaminants, and linking
microbiome sampling with long-term demographic studies at established disease sites is needed to understand the role of the
skin microbiome in disease resistance and to identify microbes that can be used to reduce infection or mortality from in-
fectious disease. Priority questions include:

a. How does the environment affect an individual's skin microbiome (richness and specific microbes)?
b. How does the microbiome affect survival of amphibians in populations with a pathogen?

4. Discussion

Our application of concepts and tools from behavioral science and decision theory was a novel approach to develop a
unified research plan, carried out by our group of geographically distributed and multidisciplinary research scientists. In
contrast to an informal reliance on expert opinion, we used nominal group theory, employing divergent and convergent
thinking to articulate our individual mental models of the amphibian host-pathogen systems (using our regional and indi-
vidual expertise). We combined these individual perspectives and collaboratively identified research priorities once we had a
shared understanding.
Via this process, we identified mechanistic hypotheses with respect to the handful of major factors (Fig. 2) amphibian
ecologists have identified as correlates of declines (Collins and Storfer, 2003) and the emerging importance of community
interactions for disease outbreaks (Johnson et al., 2015), and represented these relationships in an influence diagram
(Fig. 2). This exercise, by design, did not generate a comprehensive review of the state of knowledge for each topic.
Instead, we searched for and evaluated existing knowledge for particular aspects of the system that we considered
important to informing resource management decisions. The resulting five prioritized research needs has enabled us to
move forward on implementing inter-regional and inter-agency collaboration in support of US Department of Interior
agency needs. We found several important benefits to the structured approach we used. Our process encouraged
development of common language and clarity in communication among scientists with different, and complementary,
backgrounds. Most participants had not previously used influence or system diagrams to structure thinking. This novel
approach was challenging but beneficial, as it increased the ability to communicate complex ideas across individual
expertise, and encouraged each person to broaden their perspectives outside of their typical study system. Second, this
8 E.H. Campbell Grant et al. / Global Ecology and Conservation 16 (2018) e00441

approach improved consensus in the development and selection of a collaborative research pursuit, which stemmed from
co-generation of research priorities. This evolved as each person had an opportunity to add ideas, critically evaluate these
ideas, and revise and retain those which were promising after group evaluation. We note that some ideas which were not
retained in early discussions re-emerged at later steps in the process, which is a benefit of employing multiple
convergent-divergent cycles. Ultimately, the development of this research strategy enhanced the opportunity for
everyone to participate in the decision-making process at each step, and resulted in a transparent and well-documented
strategy that can be more easily communicated to partners.
Overall, the outcome of this process identified 5 research priorities that, when addressed, will allow us to identify
management options that may reduce disease risk to amphibian populations. These priorities reflect the current uncer-
tainty regarding the causes and drivers of disease-induced mortality and extinction of amphibian populations, and
encompass multiple scales from the microbiome of the individual to the composition of the amphibian community. All
have support in the literature as potential lines of research; here we developed more specific research questions that
address significant uncertainties within our influence diagrams. These priorities include investigating the drivers of the
community-disease relationship, exploring the role of chemical exposure as a co-factor in disease, determining the rela-
tionship between habitat characteristics and disease outcomes, evaluating the role of metapopulation structure in
amphibian pathogen spread, and finally, exploring the relative importance of the microbiome under different field-relevant
environmental conditions. We believe that research addressing these priority questions will lead to a reduction in un-
certainty regarding factors that influence disease outcomes in amphibians and thus improve our abilities to manage
disease risk in amphibian populations. Currently, there are substantial obstacles for managing amphibian disease,
including uncertainty regarding the drivers of disease and the effectiveness of potential mitigation, as well as limited
resources available for the management of these species. By identifying priorities we can focus these limited resources in a
cost-effective manner.
This novel approach brought challenges. Considering each step in the process separately required sustained effort and
cognitive energy, which was difficult to accomplish in a single in-person meeting. We met via conference call and used online
tools to collaborate, which some participants thought may have been less efficient for creative idea generation than face-to-
face meetings. Furthermore, despite our attempts to increase the breadth of ideas we considered at each step, it is entirely
possible that we may have overlooked other research priorities. There are two possible reasons for this. First, we did not
consider any specific management decision. In a formal decision analysis, the value of information can be used to calculate the
value of addressing a research priority relative to a particular management decision (Runge et al., 2011). Those which are
sound investments address critical uncertainties that would influence the optimal course of action. Instead, we relied on our
combined interactions with resource managers in our service to partner agencies within the US Department of the Interior to
understand the range of potential management strategies, and decision context, which could be considered. This did not
allow us to formally estimate the true costs and benefits of pursuing different priorities (i.e., calculating the value of resolving
the identified research priorities). Second, the success of a divergent-convergent creative process requires carefully balancing
number of participants (and associated topical coverage) with efficiency. We believe that our familiarity with the literature,
experience with different amphibian species and habitats, and range of topical and regional expertise was sufficient for
exploration and evaluation of research priorities.
Our approach allowed us to identify the first steps in a strategy to meet the needs of multiple management agencies
tasked with addressing the complex subject of the management of disease-associated amphibian declines, and to provide
a transparent record of how these priorities were generated. Important outcomes include a common articulation of the
problem and potential approaches, consensus on research priorities relevant to US Department of Interior management
agencies, and a transparent model that can be used to justify future work and can accommodate new information.
Because our objective was to identify information useful to developing effective management actions directly, this
strategy may differ from prioritizations with more academic objectives which have management as a secondary goal. This
focus on environmental management actions was driven by ARMI's mandate to conduct research that informs US public
land management, and may have limited the scope of potential research priorities because of implicit perceptions of
limiting factors on management: cost, feasibility within existing resource constraints, and an implicit understanding of
competing objectives. Overall, amphibian disease research may consider multiple drivers and a combination of collab-
orative and coherent investigations are expected to be most effective at leading to viable management options.

Author contributions

EHCG and MJA conceived the ideas and designed methodology; EHCG led the writing of the manuscript. All authors
contributed critically to the drafts and gave final approval for publication.

Acknowledgements

Riley Bernard helped with facilitation. The development of this research strategy was supported by the USGS Ecosystems
Mission Area. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the
U.S. Government. This manuscript is contribution #666 of the Amphibian Research and Monitoring Initiative (ARMI) of the US
Geological Survey.
 E.H. Campbell Grant et al. / Global Ecology and Conservation 16 (2018) e00441 9

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.gecco.2018.e00441.

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