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Amphibian conservation in the Anthropocene
Biological Conservation 236 (2019) 543–547
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Amphibian conservation in the Anthropocene
T
ARTICLE INFO
ABSTRACT
Keywords: Amphibian decline Conservation dilemma Management response Research priorities
Research is necessary to identify patterns in nature, to understand how a system functions, and to make predictions about the future state of an ecosystem. Applied research in conservation biology can identify effective strategies to maintain biodiversity, though many papers end with the conclusion that more research is needed. However, more research does not necessarily lead to solutions. We use the ongoing global decline of amphibians as a salient example to highlight limitations in current conservation research, and to focus on finding solutions which are directly relevant for conservation. While research has been conducted since declines were first detected in the 1990s, outside a few specific examples, little progress in conservation has been achieved. We suggest that the case of amphibian declines is relevant to conservation science in general, as the current paradigm for conservation is that management is planned after research is completed; research and management are not effectively (and not directly) connected. This disconnect illustrates the knowledge-action divide which has been identified as a serious deficiency in conservation. Accordingly, we use this introductory paper to the Special Issue (Amphibian conservation in the Anthropocene: Progress and challenges) to describe amphibians as a conservation dilemma, and to make the case for a different, more pragmatic, and more solutions-focused view of conservation research.
1. Introduction [Conservation] biology, with its vast informational detail and complexity, is a ‘high-information’ field, where years and decades can easily be wasted on the usual type of ‘low-information’ observations and experiments if one does not think carefully in advance about what the most important and conclusive experiments would be [— those that facilitate management action]. — Paraphrased from Platt 1964 (“Strong inference”, Science 146, 347–353) Though there are exceptions, the current conservation paradigm fails to directly connect research to management (Knight et al., 2008; Cook et al., 2010). This is partly blamed on the knowledge-implementation gap and a divide between conservation science and practice (Arlettaz et al., 2010; Cook et al., 2013; Toomey et al., 2017), and approaches such as translational ecology are proposed as solutions (Schlesinger, 2010; Chapin, 2017). However, even when scientists and managers co-develop research needs, management is typically implemented only after research is completed (Caughley, 1994). Because environmental conditions and socio-political opportunities can shift quickly, there can be a disconnect between research and subsequent management actions. A strategy of waiting for completion of research before action commences may not be the most efficient way to solve immediate and pressing conservation problems. Further, a detailed understanding of a system does not necessarily yield information relevant to management and does not always lead to management action. For example, efforts to mitigate the effects of white nose syndrome in bats has benefitted from a decade of research into biological and
chemical treatments directed at the fungal pathogen responsible for populations declines (e.g., Frick et al., 2016) but we still lack solutions that can be implemented in the field and on a scale necessary to address these declines. Despite ongoing and obvious needs, the science of conservation biology has not fulfilled its original objective of being a “mission-oriented” discipline of both pure and applied science directed at solving problems (Soule and Wilcox, 1980). As scientists working in the branch of ecology that is supposed to offer solutions to declines in biodiversity, we need to more quickly identify and implement conservation actions more efficiently. This means that we need to ensure that we are identifying the questions with the most utility to conservation, and that resulting actions are implemented (i.e., managers can more readily use research results). The global decline of amphibians serves as a pressing example. After an initial phase of debating the existence and quantifying the phenomenon (Pechmann et al., 1991), research turned to the identification of the causes of amphibian declines. Despite nearly three decades of research, declines of both rare and common species continue – both in local population abundance, and at the more important metapopulation scale (e.g., Adams et al., 2013; Grant et al., 2016; Petrovan and Schmidt, 2016). What is missing, and what this special issue provides, is solutions. By identifying and carrying out a specific course of research that is designed to directly inform management and conservation action, we can move solutions from the theoretical to the applied. For example, there are a handful of common causes of amphibian declines. Some, such as climate change and agricultural chemical use, are difficult to remedy at a large scale without changing societal norms, but may be mitigated at a smaller scale. Knowing which drivers of decline are important locally, and how they may interact to affect local populations, remains a pressing research need.
https://doi.org/10.1016/j.biocon.2019.03.003 Received 1 November 2018; Received in revised form 26 February 2019; Accepted 3 March 2019 Available online 13 June 2019 0006-3207/ © 2019 Published by Elsevier Ltd.
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Box 1 Addressing real-world conservation. While the application of conservation biology theory and tools has been described elsewhere (e.g., Sodhi and Ehrlich 2010), it is instructive to review points that are particularly relevant (but not exclusive) to amphibian conservation. 1. Identify local conservation problems and needs (i.e., objectives and tractable questions) via conversations with local managers (Braunisch et al., 2012; Converse and Grant 2019 – this issue). Research priorities of managers may differ substantially from those of researchers (Mason et al. 2017). 2. Provide a synthetic review of what is known with a summary that is informative for both researchers and managers (Pullin and Knight 2009); focus on available evidence and effectiveness (one may start with conservationevidence.com; accesssed 17 October 2018, and add local knowledge). 3. Assess which questions are most likely to change conservation outcomes. This can be accomplished, for example, using value of information analysis, which requires an explicit framing of the management decision. Such an analysis trades generality for specificity, but information with high value of information for multiple specific decisions is often the most important research for conservation gains (Bolam et al. 2019). It is also possible to use nominal group theory and influence diagrams to identify the most relevant research questions, independent of a specific management decision (Grant et al. 2018). 4. Identify the life history stage which has the greatest effect on population viability such that conservation efforts can be focused on this stage (Crouse et al. 1987; Crowder et al. 1994; Sterrett et al., 2019b; Petrovan and Schmidt 2019 – this issue). 5. Learn while doing conservation (i.e., research and conservation actions are not mutually exclusive or necessarily sequential). For example, use an adaptive management approach to improve future decisions (Canessa et al. 2019b– this issue; Keith et al. 2011). The most efficient learning happens when predictions are made for each conservation action, the predictions are formalized as a set of models and the models are assessed in a rigorous way yielding a “best” model (i.e., action). 6. Determine the effectiveness of ongoing or previous management actions through a comparative effectiveness analysis. This and conservationevidence.com can indicate whether ongoing conservation actions are useful, but generally they fall short in identifying why they fail (Schmidt et al. 2019 – this issue). 7. Start new research. Think big and experimental (sensu Semlitsch et al., 2009). Match scale(s) of research to scale(s) of management (Scroggie et al., 2019 – this issue). 8. Publish the results (for science) and implement outreach (for conservation). Talk to local conservationists (again, now with results). Do this in the style of translational ecology (Schlesinger 2010, Chapin, 2017): using common-sense, clear and inclusive dialogue that allows two-way conversations. A simple way to improve outreach may be to translate important research results and management guidelines into different languages as many people involved in conservation on the ground do not read or speak English (Amano et al. 2016). and Grant, 2019 – this issue). Alternatively, scientists and managers in one part of the world may not know what to do, but the solution has been identified elsewhere. This problem represents the skewed view of conservation biology that is promulgated by a bias towards information published in English language journals (Amano et al., 2016) – an overlooked facet of translational ecology. Additionally, combining theory with (even sparse) field data may identify promising avenues for conservation-oriented research (Direnzo and Grant, 2019 – this issue). Second, scientists and managers know what to do but they choose not to act. Doing nothing may be due to a perceived or real lack of sufficient evidence (requiring more research on the effects of an action before it can be implemented Canessa et al., 2019b – this issue, Petrovan and Schmidt, 2019 – this issue); a recognition of trade-offs in other resource management objectives or other constraints (e.g., legal, policy, and funding constraints) that cannot be addressed via more research; or a fear of the unknown [e.g., how an innovative but untested strategy (e.g., Mendelson et al., 2019 – this issue, Lewis et al., 2019 – this issue) might work]. Third, scientists and managers know what to do, implement appropriate actions, but the actions are insufficient (in scale or quantity). For example, increasing the amount of high-quality habitat (Schmidt et al., 2019 – this issue) is successful, but insufficient implementation impedes population recovery at meaningful metapopulation scales. Failure to sufficiently manage the landscape can be driven by a lack of funding, past equivocal results, trade-offs among other objectives that vary spatially, or political or societal constraints. Finally, scientists and managers know what to do but the action is not yet ready for application in the field. For example, Sterrett et al. (2019a – this issue) have a list of possible conservation actions – one is “mitigate contaminants.” While we may know that this is important, it is not known how to precisely implement this strategy. This is made more complex when there are multiple, and potentially interacting, stressors (Smalling et al., 2019 this issue). Constraints underlying each of these reasons may be real (e.g., management actions are only allowed on publicly managed landscapes that include biodiversity objectives), or perceived (e.g., lack of understanding of methods or erroneous beliefs about how a system
The issue of complexity in causes of population declines is not unique to amphibians, and many factors underlying amphibian population declines are shared across taxa (e.g., emerging fungal diseases in bats, snakes, amphibians (Fisher et al., 2016); habitat loss and alteration (Dobson et al., 2006); climate change (Parmesan and Yohe, 2003); invasive predators (Doherty et al., 2016)). Conservation science, in particular amphibian conservation science, needs an improved focus on problem-solving, that is, identifying and testing solutions that are fieldbased and population-oriented. This includes elements of predicting future threats and developing proactive responses to the resulting forecasts. This special issue is timely, given the lack of progress in mitigating amphibian decline and recent criticism of the lack of predictive power in the science of ecology (e.g., Petchey et al., 2015; Houlahan et al., 2017; Pennekamp et al., 2017). Indeed, recently Godet and Devictor (2018) evaluated nearly 13,000 papers in conservation journals and found that only 8.4% proposed solutions to defined conservation problems and only two-thirds of the papers with solutions tested them. This means that a vanishingly small proportion of this large body of work actually trialed the proposed solutions. In research on amphibian declines, Canessa et al. (2019a – this issue) finds the same grim pattern (a preponderance of research, but few field-trialed mitigation measures) for pathogen management – a prominent concern for amphibian populations globally. While theory and conceptual models are vital in ecology for generating expectations and organizing ideas when field data are unavailable, the imbalance between theory and empirical data subverts the intended purpose of conservation research. 2. Owning up to failure There are four fundamental reasons why amphibian conservation may fail. First, scientists and managers don't know what to do – while research may identify a decline, it may not be designed to offer a course of action to halt or reverse the trend. We suggest that this particular inertia can be overcome with clear thinking and directed research, and may be simply a failure in creativity in developing actions (Converse 544
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functions). Discerning the difference between perceived and real uncertainties can be accomplished by framing decisions explicitly (e.g., under a structured decision-making process; Converse and Grant, 2019 – this issue) and a commitment to collaborative efforts between scientists and managers. Once perceived uncertainties have been addressed, real uncertainties can be reduced by targeted research.
(Converse and Grant, 2019 – this issue, Canessa et al., 2019a, 2019b – this issue; Scroggie et al., 2019 – this issue), which will ultimately yield better presentation of policy-relevant science and likely increased implementation (Game et al., 2014), realizing the call for improved ‘translational ecology’ (Enquist et al., 2017). Some challenges span multiple topics; for example, funding is a central and oft-cited problem. However, increased funding does not guarantee that complex problems will be solved (Game et al., 2014). This may be especially true for amphibians since many causes of decline can be addressed at a local (and thereby tractable) scale. Greater creativity in finding solutions is needed. Creative solutions come from having a variety of perspectives represented in the conversation and can be facilitated by increased dialogue among managers, policy makers and scientists. While this requires investment from all groups, the benefit is expected to be more targeted research, better applicability, and increased use of the science by managers (Braunisch et al., 2012; Hernandez-Mocillo et al., 2017; Mason et al., 2017). Communication is a perennial problem across disciplines and across different types of actors in conservation (Schlesinger, 2010; Chapin, 2017) especially when managers may be concerned about a local-scale problem, while a scientist is taking a broader-scale perspective (Mosher et al., 2019). Scale matters and the ability to discuss concepts across scales from a variety of perspectives is necessary (Adams and Muths, 2019 – this issue). Similar to difficulties communicating across scales, the complexity of predictive models can pose challenges to shared understanding. Model development requires close collaboration among modelers, biologists, and managers. Understanding the premise and basic mechanics of the model, as well as the output, is crucial for correct parameterization, trust in the output, and effective use of the results (Mosher et al., 2019). The rarity of field-tested conservation solutions (Godet and Devictor, 2018) is a primary reason for the increasing gap between science and practice. In part, this may be because many implemented solutions are part of mitigation efforts carried out by consultants or conservation programs carried out by managers (Cook et al., 2012). Post-implementation monitoring may not be inherently expected, encouraged or supported. Thus the results of these field tests of solutions may not be scientifically robust enough for publication in peer-reviewed journals and are not widely disseminated. In conservation science there is a shift away from carrying out (and publishing) real-word, local interventions, towards broader-scale conservation challenges, so that solutions-based research and field-testing remains partly ignored or out of reach in helping to guide management decisions (Pullin et al., 2004; Arlettaz et al., 2010; Toomey et al., 2017). In response to this we have assembled in this Special Issue multiple examples where conservation science offers direct, implementable, and practical solutions.
3. When can more research help? For achieving progress in conservation implementation, more research is not necessarily better. Critical research (Box 1) falls into two categories: 1) research that strategizes actions for currently identified conservation problems (e.g., Matos et al., 2019 – this issue; Scheele et al., 2019 – this issue; Scroggie et al., 2019 – this issue), research that has direct applicability to real-world problems [e.g., understanding animal movement relative to disease transfer; Bailey and Muths (2019 – this issue) or adaptive management for reintroductions Canessa et al., 2019b – this issue] and 2) research that addresses future threats. Considering the future allows the identification of emerging problems at an early stage, when proactive management may be most efficient and effective (Sterrett et al., 2019a – this issue). Often, prediction can inform which uncertainties will plague the implementation of conservation actions (Earl, 2019 – this issue), allowing sufficient time to conduct research to address these information needs. Predictive methodologies vary (e.g., horizon scanning, scenario planning, strategic foresight; Schoemaker, 1995, Cook et al., 2014, Sutherland et al., 2014) and their utility varies with the socio-ecological system in question (Hartel et al., 2019 – this issue). Identifying new threats through these predictive methodologies is important but understanding the relative effect of a new threat (e.g., do pesticides matter in temporary wetlands with endemic disease, Smalling et al., 2019 – this issue) is more important. That is, addressing first-order (e.g., local and immediate) problems is more valuable in advancing conservation (Scroggie et al., 2019 – this issue) than the identification of global patterns and drivers. Similarly, identifying, describing and quantifying current and future threats are not sufficient. Predictive science plays an important role in research, perhaps especially in conservation where predictions may be realized in relatively short time frames (e.g., of the threat of the emerging pathogen Batrachochytrium salamandrivorans to European amphibians and its expected threat to US amphibians; Richgels et al., 2016, Canessa et al., 2018). 4. Ongoing challenges and suggestions on how to address them Even with improved research approaches, barriers to effective amphibian conservation will remain and include: 1) understanding the context of management decisions, 2) developing creative solutions, and 3) assessing and communicating successes and failures. Although certainly not exhaustive, the following are examples of these challenges. Successful implementation of conservation actions often hinges on human communication, collaboration and the socio-political environment of the resource managers – that is, the context of management (Calhoun et al., 2014; Hartel et al., 2019 – this issue). Behavioural psychology and decision theory can aid in navigating this landscape
5. Conclusions: the future We are in a new era of amphibian decline. We remain in need of more options; even the relatively few solutions that have been proposed (e.g., Garner et al., 2016) require additional testing. Although progress in amphibian conservation has been slow in terms of consensus conclusions identifying “smoking guns” or “silver bullets”, there have been some conservation successes. Independent of a consideration of cost,
Box 2 A selection of actions that have evidence of success for amphibian conservation. 1. 2. 3. 4. 5. 6.
Create more suitable habitat (e.g., manage hydrology; Schmidt et al., 2015) Supplement populations (captive rearing or facilitated colonization/translocation; Griffiths and Pavajeau, 2008, Muths et al. in press). 3. Reduce the use of pesticides and herbicides in wetland habitat (Lin et al., 2008) Mitigate the effects of roads (e.g., provide culverts underneath, Matos et al., 2017, Smith et al., 2018) Protect habitat (small scale, e.g., exclude or restore grazing at wetlands; Buckley et al., 2014) Remove and control invasive or non-native species (e.g., fish) (Jarchow et al., 2016; Knapp et al., 2016). 545
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trade-offs, and jurisdiction (all real constraints), there is evidence that some kinds of management can be successful (Smith et al., 2018; Box 2). These particular management actions are unlikely to have utility in all places; their efficacy will depend on the local conditions, the target species, and other non-ecological factors (such as the willingness of landowners to accept conservation actions). In cases where inertia simply cannot be overcome, and management actions cannot be initiated for amphibian conservation, there is utility in keeping amphibians in management conversations by formally considering their conservation needs as objectives in management decisions directed at other species. For example, in considering two actions that have similar expected outcomes for a non-amphibian target species, the optimal solution might differ if co-occurring amphibians are considered. Considering amphibians as a (non-target) objective may thus help to avoid unintended consequences for amphibians when managing other aspects of an ecosystem. This involves a formal trade-off and optimization analysis but is easily incorporated in a decision analysis (Converse and Grant, 2019 – this issue). To stem the decline of amphibian diversity, we need to recognize and repair the disconnect between research and subsequent management actions. Throughout papers in this special issue, we remind managers and researchers that conservation biology is “mission-oriented” and directed at solving problems (Soule and Wilcox, 1980). Within this context, the included papers highlight work that specifically addresses the need for management solutions via targeted research. Impediments to action in conservation include a lack of knowledge, an inability to act once that knowledge is achieved, and the insufficient application of conservation actions. Responses include identification of research questions with the most utility to applied conservation, fullscale field trials of promising mitigation actions, and accommodation of the human dimensions (including political climates) that influence the implementation of even proven conservation actions. While the global decline of amphibians illustrates this disconnect, amphibians are not alone in facing an uncertain future unless we are able to collectively improve conservation efforts. We suggest that this is possible by re-tooling approaches and goals in conservation science to emphasize actions at local scales rather than chasing generalities (i.e., focusing on research that will directly inform management), and increasing capacity to test and apply management strategies at appropriate scales. This improved focus on problem-solving that returns fieldbased and population level strategies has the potential to move amphibian conservation and the preservation of biodiversity forward.
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Schulp, C.J.E., Verburg, P.H., Plieninger, T., 2017. Priority questions for the science, policy and practice of cultural landscapes in Europe. Landsc. Ecol. 32, 2083–2096. Houlahan, J.E., McKinney, S.T., Anderson, T.M., McGill, B.J., 2017. The priority of prediction in ecological understanding. Oikos 126, 1–7. Jarchow, C.J., Hossack, B.R., Sigafus, B.H., Schwalbe, C.R., Muths, E., 2016. Modeling habitat connectivity to inform reintroductions: a case study with the Chiricahua leopard frog. J. Herpetol. (1), 63–69. https://doi.org/10.1670/14-172. Keith, D.A., Martin, T.G., McDonald-Madden, E., Walters, C., 2011. Uncertainty and adaptive management for biodiversity conservation. Biol. Conserv. 144, 1175–1178. Knapp, R.A., Fellers, G.M., Kleeman, P.M., Miller, D.A.W., Vredenburg, V.T., Rosenblum, E.B., Briggs, C.J., 2016. Large-scale recovery of an endangered amphibian despite ongoing exposure to multiple stressors. Proc. Natl. Acad. Sci. U. S. A. 113, 11889–11894. Knight, A.T., Cowling, R.M., Rouget, M., Balmford, A., Lombard, A.T., Campbell, B.M., 2008. Knowing but not doing: selecting priority conservation areas and the research–implementation gap. Conserv. Biol. 22, 610–617. Lewis, C., Richards-Zawacki, C.L., Ibáñez, R., Luedtke, J., Voyles, J., Houser, P., Gratwicke, B., 2019. Conserving Panamanian harlequin frogs by integrating captivebreeding and research programs. Biol. Conserv (this issue). Lin, H.-C., Cheng, L.-Y., Chen, P.-C., Chang, M.-H., 2008. Involving local communities in amphibian conservation: Taipei frog Rana taipehensis as an example. Int. Zoo Yearb. 42, 90–98. Mason, J.G., Rudd, M.A., Crowder, L.B., 2017. Ocean research priorities: similarities and differences among scientists, policymakers, and fishermen in the United States. BioScience 67, 418–428. Matos, C., Petrovan, S., Ward, A.I., Wheeler, P., 2017. Facilitating permeability of landscapes impacted by roads for protected amphibians: patterns of movement for the great crested newt. PeerJ 5, e2922. Matos, C., Patrovan, S.O., Wheeler, P., Ward, A.I., 2019. Landscape connectivity and spatial prioritisation in an urbanising world: a network analysis approach for a threatened amphibian. Biol. Conserv (this issue). Mendelson III, J.M., Whitfield, S.M., Sredl, M.J., 2019. A recovery engine strategy for amphibian conservation in the context of disease. Biol. Conserv (this issue). Mosher, B.A., Bernard, R.F., Lorch, J.M., Miller, D.A.W., Richgels, K.L.D., White, C.L., Grant, E.H.C., 2019. Maximizing the utility of molecular methods in ecology and conservation requires communication and diverse research partnerships. Front. Ecol. Environ in press. Muths, E., F.B. Wright, III, and L.L. Bailey. In press. A continuum of risk tolerance: Reintroductions of toads in the Rockies. IN: Walls, S. and K. O'Donnell, Strategies for Conservation Success in Herpetology. Parmesan, C., Yohe, G., 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42. https://doi.org/10.1038/nature01286. Pechmann, J.H.K., Scott, D.E., Semlitsch, R.D., Caldwell, J.P., Vitt, L.J., Gibbons, J.W., 1991. Declining amphibian populations: the problem of separating human impacts from natural fluctuations. Science 253, 892–895. Pennekamp, F., Adamson, M.W., Petchey, O.L., Poggiale, J.-C., Aguiar, M., Kooi, B.W., Botkin, D.B., DeAngelis, D.L., 2017. The practice of prediction: what can ecologists learn from applied, ecology-related fields? Ecol. Complex. 32, 156–167. Petchey, O.L., Pontarp, M., Massie, T.M., Kéfi, S., Ozgul, A., Weilenmann, M., Palamara, G.M., Altermatt, F., Matthews, B., Levine, J.M., Childs, D.Z., 2015. The ecological forecast horizon, and examples of its uses and determinants. Ecol. Lett. 18, 597–611. Petrovan, S.O., Schmidt, B.R., 2016. Volunteer conservation action data reveals largescale and long-term negative population trends of a widespread amphibian, the common toad (Bufo bufo). PLoS One 11, e0161943. https://doi.org/10.1371/journal. pone.0161943. Petrovan, S.O., Schmidt, B.R., 2019. Neglected juveniles; a call for integrating all amphibian life stages in assessments of mitigation success. Biol. Conserv (this issue). Pullin, A.S., Knight, T.M., 2009. Doing more good than harm – building an evidence-base for conservation and environmental management. Biol. Conserv. 142, 931–934. Pullin, A.S., Knight, T.M., Stone, D.A., Charman, K., 2004. Do conservation managers use scientific evidence to support their decision-making? Biol. Conserv. 119, 245–252. Richgels, K.L.D., Russell, R.E., Adams, M.J., White, C.L., Grant, E.H.C., 2016. Spatial variation in risk and consequence of Batrachochytrium salamandrivorans
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Evan H. Campbell Granta, , Erin Muthsb, Benedikt R. Schmidtc,d, Silviu O. Petrovane,f a U.S. Geological Survey, Patuxent Wildlife Research Center, SO Conte Anadromous Fish Research Lab, 1 Migratory Way, Turners Falls, MA 01376, United States of America b U.S. Geological Survey, Fort Collins Science Center, Fort Collins, CO 80523, United States of America c Department of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland d Info Fauna Karch, UniMail, Bâtiment G, Bellevaux 51, 2000 Neuchâtel, Switzerland e Conservation Science Group, Department of Zoology, University of Cambridge, The David Attenborough Building, Cambridge CB2 3QZ, UK f Froglife, 1 Loxley, Werrington, Peterborough PE4 5BW, UK E-mail address: [email protected] (E.H.C. Grant). ⁎
Corresponding author. 547
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Amphibian conservation in the Anthropocene
T
ARTICLE INFO
ABSTRACT
Keywords: Amphibian decline Conservation dilemma Management response Research priorities
Research is necessary to identify patterns in nature, to understand how a system functions, and to make predictions about the future state of an ecosystem. Applied research in conservation biology can identify effective strategies to maintain biodiversity, though many papers end with the conclusion that more research is needed. However, more research does not necessarily lead to solutions. We use the ongoing global decline of amphibians as a salient example to highlight limitations in current conservation research, and to focus on finding solutions which are directly relevant for conservation. While research has been conducted since declines were first detected in the 1990s, outside a few specific examples, little progress in conservation has been achieved. We suggest that the case of amphibian declines is relevant to conservation science in general, as the current paradigm for conservation is that management is planned after research is completed; research and management are not effectively (and not directly) connected. This disconnect illustrates the knowledge-action divide which has been identified as a serious deficiency in conservation. Accordingly, we use this introductory paper to the Special Issue (Amphibian conservation in the Anthropocene: Progress and challenges) to describe amphibians as a conservation dilemma, and to make the case for a different, more pragmatic, and more solutions-focused view of conservation research.
1. Introduction [Conservation] biology, with its vast informational detail and complexity, is a ‘high-information’ field, where years and decades can easily be wasted on the usual type of ‘low-information’ observations and experiments if one does not think carefully in advance about what the most important and conclusive experiments would be [— those that facilitate management action]. — Paraphrased from Platt 1964 (“Strong inference”, Science 146, 347–353) Though there are exceptions, the current conservation paradigm fails to directly connect research to management (Knight et al., 2008; Cook et al., 2010). This is partly blamed on the knowledge-implementation gap and a divide between conservation science and practice (Arlettaz et al., 2010; Cook et al., 2013; Toomey et al., 2017), and approaches such as translational ecology are proposed as solutions (Schlesinger, 2010; Chapin, 2017). However, even when scientists and managers co-develop research needs, management is typically implemented only after research is completed (Caughley, 1994). Because environmental conditions and socio-political opportunities can shift quickly, there can be a disconnect between research and subsequent management actions. A strategy of waiting for completion of research before action commences may not be the most efficient way to solve immediate and pressing conservation problems. Further, a detailed understanding of a system does not necessarily yield information relevant to management and does not always lead to management action. For example, efforts to mitigate the effects of white nose syndrome in bats has benefitted from a decade of research into biological and
chemical treatments directed at the fungal pathogen responsible for populations declines (e.g., Frick et al., 2016) but we still lack solutions that can be implemented in the field and on a scale necessary to address these declines. Despite ongoing and obvious needs, the science of conservation biology has not fulfilled its original objective of being a “mission-oriented” discipline of both pure and applied science directed at solving problems (Soule and Wilcox, 1980). As scientists working in the branch of ecology that is supposed to offer solutions to declines in biodiversity, we need to more quickly identify and implement conservation actions more efficiently. This means that we need to ensure that we are identifying the questions with the most utility to conservation, and that resulting actions are implemented (i.e., managers can more readily use research results). The global decline of amphibians serves as a pressing example. After an initial phase of debating the existence and quantifying the phenomenon (Pechmann et al., 1991), research turned to the identification of the causes of amphibian declines. Despite nearly three decades of research, declines of both rare and common species continue – both in local population abundance, and at the more important metapopulation scale (e.g., Adams et al., 2013; Grant et al., 2016; Petrovan and Schmidt, 2016). What is missing, and what this special issue provides, is solutions. By identifying and carrying out a specific course of research that is designed to directly inform management and conservation action, we can move solutions from the theoretical to the applied. For example, there are a handful of common causes of amphibian declines. Some, such as climate change and agricultural chemical use, are difficult to remedy at a large scale without changing societal norms, but may be mitigated at a smaller scale. Knowing which drivers of decline are important locally, and how they may interact to affect local populations, remains a pressing research need.
https://doi.org/10.1016/j.biocon.2019.03.003 Received 1 November 2018; Received in revised form 26 February 2019; Accepted 3 March 2019 Available online 13 June 2019 0006-3207/ © 2019 Published by Elsevier Ltd.
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Box 1 Addressing real-world conservation. While the application of conservation biology theory and tools has been described elsewhere (e.g., Sodhi and Ehrlich 2010), it is instructive to review points that are particularly relevant (but not exclusive) to amphibian conservation. 1. Identify local conservation problems and needs (i.e., objectives and tractable questions) via conversations with local managers (Braunisch et al., 2012; Converse and Grant 2019 – this issue). Research priorities of managers may differ substantially from those of researchers (Mason et al. 2017). 2. Provide a synthetic review of what is known with a summary that is informative for both researchers and managers (Pullin and Knight 2009); focus on available evidence and effectiveness (one may start with conservationevidence.com; accesssed 17 October 2018, and add local knowledge). 3. Assess which questions are most likely to change conservation outcomes. This can be accomplished, for example, using value of information analysis, which requires an explicit framing of the management decision. Such an analysis trades generality for specificity, but information with high value of information for multiple specific decisions is often the most important research for conservation gains (Bolam et al. 2019). It is also possible to use nominal group theory and influence diagrams to identify the most relevant research questions, independent of a specific management decision (Grant et al. 2018). 4. Identify the life history stage which has the greatest effect on population viability such that conservation efforts can be focused on this stage (Crouse et al. 1987; Crowder et al. 1994; Sterrett et al., 2019b; Petrovan and Schmidt 2019 – this issue). 5. Learn while doing conservation (i.e., research and conservation actions are not mutually exclusive or necessarily sequential). For example, use an adaptive management approach to improve future decisions (Canessa et al. 2019b– this issue; Keith et al. 2011). The most efficient learning happens when predictions are made for each conservation action, the predictions are formalized as a set of models and the models are assessed in a rigorous way yielding a “best” model (i.e., action). 6. Determine the effectiveness of ongoing or previous management actions through a comparative effectiveness analysis. This and conservationevidence.com can indicate whether ongoing conservation actions are useful, but generally they fall short in identifying why they fail (Schmidt et al. 2019 – this issue). 7. Start new research. Think big and experimental (sensu Semlitsch et al., 2009). Match scale(s) of research to scale(s) of management (Scroggie et al., 2019 – this issue). 8. Publish the results (for science) and implement outreach (for conservation). Talk to local conservationists (again, now with results). Do this in the style of translational ecology (Schlesinger 2010, Chapin, 2017): using common-sense, clear and inclusive dialogue that allows two-way conversations. A simple way to improve outreach may be to translate important research results and management guidelines into different languages as many people involved in conservation on the ground do not read or speak English (Amano et al. 2016). and Grant, 2019 – this issue). Alternatively, scientists and managers in one part of the world may not know what to do, but the solution has been identified elsewhere. This problem represents the skewed view of conservation biology that is promulgated by a bias towards information published in English language journals (Amano et al., 2016) – an overlooked facet of translational ecology. Additionally, combining theory with (even sparse) field data may identify promising avenues for conservation-oriented research (Direnzo and Grant, 2019 – this issue). Second, scientists and managers know what to do but they choose not to act. Doing nothing may be due to a perceived or real lack of sufficient evidence (requiring more research on the effects of an action before it can be implemented Canessa et al., 2019b – this issue, Petrovan and Schmidt, 2019 – this issue); a recognition of trade-offs in other resource management objectives or other constraints (e.g., legal, policy, and funding constraints) that cannot be addressed via more research; or a fear of the unknown [e.g., how an innovative but untested strategy (e.g., Mendelson et al., 2019 – this issue, Lewis et al., 2019 – this issue) might work]. Third, scientists and managers know what to do, implement appropriate actions, but the actions are insufficient (in scale or quantity). For example, increasing the amount of high-quality habitat (Schmidt et al., 2019 – this issue) is successful, but insufficient implementation impedes population recovery at meaningful metapopulation scales. Failure to sufficiently manage the landscape can be driven by a lack of funding, past equivocal results, trade-offs among other objectives that vary spatially, or political or societal constraints. Finally, scientists and managers know what to do but the action is not yet ready for application in the field. For example, Sterrett et al. (2019a – this issue) have a list of possible conservation actions – one is “mitigate contaminants.” While we may know that this is important, it is not known how to precisely implement this strategy. This is made more complex when there are multiple, and potentially interacting, stressors (Smalling et al., 2019 this issue). Constraints underlying each of these reasons may be real (e.g., management actions are only allowed on publicly managed landscapes that include biodiversity objectives), or perceived (e.g., lack of understanding of methods or erroneous beliefs about how a system
The issue of complexity in causes of population declines is not unique to amphibians, and many factors underlying amphibian population declines are shared across taxa (e.g., emerging fungal diseases in bats, snakes, amphibians (Fisher et al., 2016); habitat loss and alteration (Dobson et al., 2006); climate change (Parmesan and Yohe, 2003); invasive predators (Doherty et al., 2016)). Conservation science, in particular amphibian conservation science, needs an improved focus on problem-solving, that is, identifying and testing solutions that are fieldbased and population-oriented. This includes elements of predicting future threats and developing proactive responses to the resulting forecasts. This special issue is timely, given the lack of progress in mitigating amphibian decline and recent criticism of the lack of predictive power in the science of ecology (e.g., Petchey et al., 2015; Houlahan et al., 2017; Pennekamp et al., 2017). Indeed, recently Godet and Devictor (2018) evaluated nearly 13,000 papers in conservation journals and found that only 8.4% proposed solutions to defined conservation problems and only two-thirds of the papers with solutions tested them. This means that a vanishingly small proportion of this large body of work actually trialed the proposed solutions. In research on amphibian declines, Canessa et al. (2019a – this issue) finds the same grim pattern (a preponderance of research, but few field-trialed mitigation measures) for pathogen management – a prominent concern for amphibian populations globally. While theory and conceptual models are vital in ecology for generating expectations and organizing ideas when field data are unavailable, the imbalance between theory and empirical data subverts the intended purpose of conservation research. 2. Owning up to failure There are four fundamental reasons why amphibian conservation may fail. First, scientists and managers don't know what to do – while research may identify a decline, it may not be designed to offer a course of action to halt or reverse the trend. We suggest that this particular inertia can be overcome with clear thinking and directed research, and may be simply a failure in creativity in developing actions (Converse 544
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functions). Discerning the difference between perceived and real uncertainties can be accomplished by framing decisions explicitly (e.g., under a structured decision-making process; Converse and Grant, 2019 – this issue) and a commitment to collaborative efforts between scientists and managers. Once perceived uncertainties have been addressed, real uncertainties can be reduced by targeted research.
(Converse and Grant, 2019 – this issue, Canessa et al., 2019a, 2019b – this issue; Scroggie et al., 2019 – this issue), which will ultimately yield better presentation of policy-relevant science and likely increased implementation (Game et al., 2014), realizing the call for improved ‘translational ecology’ (Enquist et al., 2017). Some challenges span multiple topics; for example, funding is a central and oft-cited problem. However, increased funding does not guarantee that complex problems will be solved (Game et al., 2014). This may be especially true for amphibians since many causes of decline can be addressed at a local (and thereby tractable) scale. Greater creativity in finding solutions is needed. Creative solutions come from having a variety of perspectives represented in the conversation and can be facilitated by increased dialogue among managers, policy makers and scientists. While this requires investment from all groups, the benefit is expected to be more targeted research, better applicability, and increased use of the science by managers (Braunisch et al., 2012; Hernandez-Mocillo et al., 2017; Mason et al., 2017). Communication is a perennial problem across disciplines and across different types of actors in conservation (Schlesinger, 2010; Chapin, 2017) especially when managers may be concerned about a local-scale problem, while a scientist is taking a broader-scale perspective (Mosher et al., 2019). Scale matters and the ability to discuss concepts across scales from a variety of perspectives is necessary (Adams and Muths, 2019 – this issue). Similar to difficulties communicating across scales, the complexity of predictive models can pose challenges to shared understanding. Model development requires close collaboration among modelers, biologists, and managers. Understanding the premise and basic mechanics of the model, as well as the output, is crucial for correct parameterization, trust in the output, and effective use of the results (Mosher et al., 2019). The rarity of field-tested conservation solutions (Godet and Devictor, 2018) is a primary reason for the increasing gap between science and practice. In part, this may be because many implemented solutions are part of mitigation efforts carried out by consultants or conservation programs carried out by managers (Cook et al., 2012). Post-implementation monitoring may not be inherently expected, encouraged or supported. Thus the results of these field tests of solutions may not be scientifically robust enough for publication in peer-reviewed journals and are not widely disseminated. In conservation science there is a shift away from carrying out (and publishing) real-word, local interventions, towards broader-scale conservation challenges, so that solutions-based research and field-testing remains partly ignored or out of reach in helping to guide management decisions (Pullin et al., 2004; Arlettaz et al., 2010; Toomey et al., 2017). In response to this we have assembled in this Special Issue multiple examples where conservation science offers direct, implementable, and practical solutions.
3. When can more research help? For achieving progress in conservation implementation, more research is not necessarily better. Critical research (Box 1) falls into two categories: 1) research that strategizes actions for currently identified conservation problems (e.g., Matos et al., 2019 – this issue; Scheele et al., 2019 – this issue; Scroggie et al., 2019 – this issue), research that has direct applicability to real-world problems [e.g., understanding animal movement relative to disease transfer; Bailey and Muths (2019 – this issue) or adaptive management for reintroductions Canessa et al., 2019b – this issue] and 2) research that addresses future threats. Considering the future allows the identification of emerging problems at an early stage, when proactive management may be most efficient and effective (Sterrett et al., 2019a – this issue). Often, prediction can inform which uncertainties will plague the implementation of conservation actions (Earl, 2019 – this issue), allowing sufficient time to conduct research to address these information needs. Predictive methodologies vary (e.g., horizon scanning, scenario planning, strategic foresight; Schoemaker, 1995, Cook et al., 2014, Sutherland et al., 2014) and their utility varies with the socio-ecological system in question (Hartel et al., 2019 – this issue). Identifying new threats through these predictive methodologies is important but understanding the relative effect of a new threat (e.g., do pesticides matter in temporary wetlands with endemic disease, Smalling et al., 2019 – this issue) is more important. That is, addressing first-order (e.g., local and immediate) problems is more valuable in advancing conservation (Scroggie et al., 2019 – this issue) than the identification of global patterns and drivers. Similarly, identifying, describing and quantifying current and future threats are not sufficient. Predictive science plays an important role in research, perhaps especially in conservation where predictions may be realized in relatively short time frames (e.g., of the threat of the emerging pathogen Batrachochytrium salamandrivorans to European amphibians and its expected threat to US amphibians; Richgels et al., 2016, Canessa et al., 2018). 4. Ongoing challenges and suggestions on how to address them Even with improved research approaches, barriers to effective amphibian conservation will remain and include: 1) understanding the context of management decisions, 2) developing creative solutions, and 3) assessing and communicating successes and failures. Although certainly not exhaustive, the following are examples of these challenges. Successful implementation of conservation actions often hinges on human communication, collaboration and the socio-political environment of the resource managers – that is, the context of management (Calhoun et al., 2014; Hartel et al., 2019 – this issue). Behavioural psychology and decision theory can aid in navigating this landscape
5. Conclusions: the future We are in a new era of amphibian decline. We remain in need of more options; even the relatively few solutions that have been proposed (e.g., Garner et al., 2016) require additional testing. Although progress in amphibian conservation has been slow in terms of consensus conclusions identifying “smoking guns” or “silver bullets”, there have been some conservation successes. Independent of a consideration of cost,
Box 2 A selection of actions that have evidence of success for amphibian conservation. 1. 2. 3. 4. 5. 6.
Create more suitable habitat (e.g., manage hydrology; Schmidt et al., 2015) Supplement populations (captive rearing or facilitated colonization/translocation; Griffiths and Pavajeau, 2008, Muths et al. in press). 3. Reduce the use of pesticides and herbicides in wetland habitat (Lin et al., 2008) Mitigate the effects of roads (e.g., provide culverts underneath, Matos et al., 2017, Smith et al., 2018) Protect habitat (small scale, e.g., exclude or restore grazing at wetlands; Buckley et al., 2014) Remove and control invasive or non-native species (e.g., fish) (Jarchow et al., 2016; Knapp et al., 2016). 545
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trade-offs, and jurisdiction (all real constraints), there is evidence that some kinds of management can be successful (Smith et al., 2018; Box 2). These particular management actions are unlikely to have utility in all places; their efficacy will depend on the local conditions, the target species, and other non-ecological factors (such as the willingness of landowners to accept conservation actions). In cases where inertia simply cannot be overcome, and management actions cannot be initiated for amphibian conservation, there is utility in keeping amphibians in management conversations by formally considering their conservation needs as objectives in management decisions directed at other species. For example, in considering two actions that have similar expected outcomes for a non-amphibian target species, the optimal solution might differ if co-occurring amphibians are considered. Considering amphibians as a (non-target) objective may thus help to avoid unintended consequences for amphibians when managing other aspects of an ecosystem. This involves a formal trade-off and optimization analysis but is easily incorporated in a decision analysis (Converse and Grant, 2019 – this issue). To stem the decline of amphibian diversity, we need to recognize and repair the disconnect between research and subsequent management actions. Throughout papers in this special issue, we remind managers and researchers that conservation biology is “mission-oriented” and directed at solving problems (Soule and Wilcox, 1980). Within this context, the included papers highlight work that specifically addresses the need for management solutions via targeted research. Impediments to action in conservation include a lack of knowledge, an inability to act once that knowledge is achieved, and the insufficient application of conservation actions. Responses include identification of research questions with the most utility to applied conservation, fullscale field trials of promising mitigation actions, and accommodation of the human dimensions (including political climates) that influence the implementation of even proven conservation actions. While the global decline of amphibians illustrates this disconnect, amphibians are not alone in facing an uncertain future unless we are able to collectively improve conservation efforts. We suggest that this is possible by re-tooling approaches and goals in conservation science to emphasize actions at local scales rather than chasing generalities (i.e., focusing on research that will directly inform management), and increasing capacity to test and apply management strategies at appropriate scales. This improved focus on problem-solving that returns fieldbased and population level strategies has the potential to move amphibian conservation and the preservation of biodiversity forward.
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Evan H. Campbell Granta, , Erin Muthsb, Benedikt R. Schmidtc,d, Silviu O. Petrovane,f a U.S. Geological Survey, Patuxent Wildlife Research Center, SO Conte Anadromous Fish Research Lab, 1 Migratory Way, Turners Falls, MA 01376, United States of America b U.S. Geological Survey, Fort Collins Science Center, Fort Collins, CO 80523, United States of America c Department of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland d Info Fauna Karch, UniMail, Bâtiment G, Bellevaux 51, 2000 Neuchâtel, Switzerland e Conservation Science Group, Department of Zoology, University of Cambridge, The David Attenborough Building, Cambridge CB2 3QZ, UK f Froglife, 1 Loxley, Werrington, Peterborough PE4 5BW, UK E-mail address: [email protected] (E.H.C. Grant). ⁎
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