Using life history traits to assess climate change vulnerability in understudied species

Abstract

Climate change is a primary threat to biodiversity, but formany species, we still lack information required to assess their relative vulnerability to changes. Climate change vulnerability assessment (CCVA) is a widely used technique to rank relative vulnerability to climate change based on species characteristics, such as their distributions, habitat associations, environmental tolerances, and life-history traits. However, for species that we expect are vulnerable to climate change yet are understudied, like many amphibians, we often lack information required to construct CCVAs using existing methods. We used the CCVA framework to construct trait-based models based on life history theory, using empirical evidence of traits and distributions that reflected sensitivity of amphibians to environmental perturbation.We performed CCVAs for amphibians in 7 states in the northcentral USA, focusing on 31 aquatic-breeding species listed as species of greatest conservation need by at least 1 state. Because detailed information on habitat requirements is unavailable for most amphibian species, we used species distributions and information on traits expected to influence vulnerability to a drying climate (e.g., clutch size and habitat breadth). We scored species vulnerability based on changes projected for midcentury (2040–2069) from 2 climate models representing “least-dry” and “most-dry” scenarios for the region. Species characteristics useful for discriminating vulnerability in our models included small range size, small clutch size, inflexible diel activity patterns, and smaller habitat breadth. When projected climate scenarios included a mix of drier and wetter conditions in the future, the exposure of a species to drying conditions was most important to relative rankings. When the scenario was universally drier, species characteristics were more important to relative rankings. Using information typically available even for understudied species and a range of climate projections, our results highlight the potential of using life history traits as indicators of relative climate vulnerability. The commonalities we identified provide a framework that can be used to assess other understudied species threatened by climate change.

Keywords

amphibian / at-risk / climate change vulnerability assessment / climate models / scenariomodeling / species of greatest conservation need / trait variation

References

[1] Alder,J.R. & Hostetler, S.W. (2021) CMIP5 MACAv2-METDATA monthly water balance model projections 1950-2099 for the contiguous United States. U.S. Geological Survey Data Release. Available from:

[2] Arneth,A., Shin,Y.J., Leadley,P., Rondinini, C., Bukvareva,E., Kolb,M. et al. (2020) Post-2020 biodiversity targets need to embrace climate change. Proceedings of the National Academy of Sciences, 117, 30882-30891.

[3] Association of Fish and Wildlife Agencies. 2022. State Wildlife Action Plans. Washington, D.C. Available from: https://www.fishwildlife.org/afwa-informs/state-wildlife-action-plans

[4] Bartelt,P.E., Klaver,R.W. & Porter,W.P. (2010) Modeling amphibian energetics, habitat suitability, and movements of Western toads, Anaxyrus (=Bufo) boreas, across present and future landscapes. Ecological Modelling, 221, 2675-2686.

[5] Beever,E.A., Hall,L.E., Varner,J., Loosen, A.E., Dunham,J.B., Gahl,M.K. et al. (2017) Behavioral flexibility as a mechanism for coping with climate change. Frontiers in Ecology and the Environment, 15, 299-308.

[6] Beranek,C.T., Sanders, S., Clulow,J. & Mahony,M. (2022) Factors influencing persistence of a threatened amphibian in restored wetlands despite severe population decline during climate change driven weather extremes. Biodiversity and Conservation, 31, 1267-1287.

[7] Bland,L.M., Collen,B., Orme,C.D.L. & Bielby, J. (2015) Predicting the conservation status of data-deficient species. Conservation Biology, 29, 250-259.

[8] Borgelt,J., Dorber,M., Høiberg,M.A. & Verones,F. (2022) More than half of data deficient species predicted to be threatened by extinction. Communications Biology, 5, 679.

[9] Brandon,R.A. (1971) Correlation of seasonal abundance with feeding and reproductive activity in the grotto salamander (Typhlotriton spelaeus). American Midland Naturalist, 86, 93.

[10] Brown,C., Nowakowski, A.J., Keung,N.C., Lawler,S.P. & Todd, B.D. (2021) Untangling multi-scale habitat relationships of an endangered frog in streams to inform reintroduction programs. Ecosphere, 12, 1-21.

[11] Caro,T., Rowe,Z., Berger,J., Wholey, P. & Dobson,A. (2022) An inconvenient misconception: climate change is not the principal driver of biodiversity loss. Conservation Letters, 15, e12868.

[12] Case,M.J., Lawler,J.J. & Tomasevic,J.A. (2015) Relative sensitivity to climate change of species in northwestern North America. Biological Conservation, 187, 127-133.

[13] Cayuela,H., Lemaître, J.-F., Muths,E., McCaffery,R.M., Frétey, T., Le Garff,B. et al. (2021) Thermal conditions predict intraspecific variation in senescence rate in frogs and toads. Proceedings of the National Academy of Sciences, 118, e2112235118.

[14] Cody,M.L. (1966) A general theory of clutch size. Evolution, 20, 174.

[15] Crawford,B.A., Maerz,J.C., Terrell,V.C.K. & Moore,C.T. (2022) Population viability analysis for a pond-breeding amphibian under future drought scenarios in the southeastern United States. Global Ecology and Conservation, 36, e02119.

[16] Culp,L.A., Cohen,E.B., Scarpignato,A.L., Thogmartin,W.E. & Marra, P.P. (2017) Full annual cycle climate change vulnerability assessment for migratory birds. Ecosphere, 8, 1-22.

[17] Davenport,J.M. & Hossack, B.R. (2016) Reevaluating geographic variation in life-history traits of a widespread nearctic amphibian. Journal of Zoology, 299, 304-310.

[18] Davidson,A., Dunn,L., Gergely,K., McKerrow, A., Williams,S. & Case,M. (2021) Refining the coarse filter approach: using habitat-based species models to identify rarity and vulnerabilities in the protection of U.S. biodiversity. Global Ecology and Conservation, 28, e01598.

[19] Dawson,T.P., Jackson, S.T., House,J.I., Prentice,I.C. & Mace, G.M. (2011) Beyond predictions: biodiversity conservation in a changing climate. Science, 332, 53-58.

[20] DeMarche,M.L., Doak,D.F. & Morris,W.F. (2019) Incorporating local adaptation into forecasts of species’ distribution and abundance under climate change. Global Change Biology, 25, 775-793.

[21] Deser,C., Knutti,R., Solomon,S. & Phillips, A.S. (2012) Communication of the role of natural variability in future North American climate. Nature Climate Change, 2, 775-779.

[22] Dickinson,M.G., Orme,C.D.L., Suttle,K.B. & Mace, G.M. (2014) Separating sensitivity from exposure in assessing extinction risk from climate change. Scientific Reports, 4, 6898.

[23] Dodd Jr.C.K. (2013) Frogs of the United States and Canada, 2-vol set. Baltimore, MD: Johns Hopkins University Press.

[24] Finn,C., Grattarola, F. & Pincheira-Donoso,D. (2023) More losers than winners: investigating anthropocene defaunation through the diversity of population trends. Biological Reviews, 4, 1732-1748.

[25] Foden,W.B., Butchart, S.H.M., Stuart,S.N., ViéJ.C., Akçakaya, H.R., Angulo,A. et al. (2013) Identifying the world’s most climate change vulnerable species: a systematic trait-based assessment of all birds, amphibians and corals. PLoS One, 8, e65427.

[26] Foden,W.B., Young,B.E., Akçakaya,H.R., Garcia,R.A., Hoffmann, A.A., Stein,B.A. et al. (2019) Climate change vulnerability assessment of species. WIREs Climate Change, 10, 1-36.

[27] Füssel,H.M. & Klein, R.J.T. (2006) Climate change vulnerability assessments: an evolution of conceptual thinking. Climatic Change, 75, 301-329.

[28] Grant,E.H.C., Miller,D.A.W., Schmidt,B.R., Adams,M.J., Amburgey, S.M., Chambert,T. et al. (2016) Quantitative evidence for the effects of multiple drivers on continental-scale amphibian declines. Scientific Reports, 6, 25625.

[29] Griffith,B., Scott,J.M., Adamcik,R., Ashe, D., Czech,B., Fischman,R. et al. (2009) Climate change adaptation for the US National Wildlife Refuge system. Environmental Management, 44, 1043-1052.

[30] Glick,P., Stein, B.A. & Edelson, N.A. (Eds.). (2011) Scanning the Conservation Horizon: a guide to climate change vulnerability assessment. Washington, D.C: National Wildlife Federation.

[31] Haelewaters,D., Matthews, T.J., Wayman,J.P., Cazabonne,J., Heyman,F., Quandt,C.A. et al. (2024) Biological knowledge shortfalls impede conservation efforts in poorly studied taxa-a case study of laboulbeniomycetes. Journal of Biogeography, 51, 29-39.

[32] Hammerson,G.A. (1999) Amphibians and Reptiles in Colorado, 2nd Ed. Niwot, CO: University Press in Colorado.

[33] Harper,J.R.M., van Wilgen, N.J., Turner,A.A., Tolley,K.A., Maritz,B., Clusella-Trullas,S. et al. (2022) Application of a trait-based climate change vulnerability assessment to determine management priorities at protected area scale. Conservation Science and Practice, 4, 1-18.

[34] Hausfather,Z. & Peters, G.P. (2020) Emissions - the “business as usual” story is misleading. Nature, 577, 618-620.

[35] Her,Y., Yoo,S.H., Cho,J., Hwang, S., Jeong,J. & Seong,C. (2019) Uncertainty in hydrological analysis of climate change: multi-parameter vs. multi-GCM ensemble predictions. Scientific Reports, 9, 4974.

[36] Hinderer,R.K. (2024) Climate Change Vulnerability Assessment for Amphibians in the North Central United States, U.S. Geological Survey Data Release. Available from:

[37] Hinderer,R.K., Litt,A.R. & McCaffery,M. (2021) Habitat selection by a threatened desert amphibian. Ecology and Evolution, 11, 536-546.

[38] Hoffmann,A.A. & Sgrò C.M. (2011) Climate change and evolutionary adaptation. Nature, 470, 479-485.

[39] Hossack,B.R., Adams,M.J., Pearl,C.A., Wilson, K.W., Bull,E.L., Lohr,K. et al. (2013a) Roles of patch characteristics, drought frequency, and restoration in long-term trends of a widespread amphibian. Conservation Biology, 27, 1410-1420.

[40] Hossack,B.R., Honeycutt, R.K., Sigafus,B.H., Muths,E., Crawford, C.L., Jones,T.R. et al. (2017) Informing recovery in a human-transformed landscape: drought-mediated coexistence alters population trends of an imperiled salamander and invasive predators. Biological Conservation, 209, 377-394.

[41] Hossack,B.R., Lowe,W.H., Webb,M.A.H., Talbott,M.J., Kappenman, K.M. & Corn,P.S. (2013b) Population-level thermal performance of a cold-water ectotherm is linked to ontogeny and local environmental heterogeneity. Freshwater Biology, 58, 2215-2225.

[42] Howard,S.D. & Bickford, D.P. (2014) Amphibians over the edge: silent extinction risk of data deficient species. Diversity and Distributions, 20, 837-846.

[43] Huntley,B., Foden,W.B., Smith,A., Platts, P., Watson,J. & Garcia,R.A. (2016) Using CCVAs and interpreting their results. In: W.B. Foden & B.E. Young, (Eds.) IUCN SSC guidelines for assessing species’ vulnerability to climate change. Cambridge, UK, and Gland, Switzerland: IUCN. pp. 33-48.

[44] Inman,R.D., Esque,T.C. & Nussear,K.E. (2023) Dispersal limitations increase vulnerability under climate change for reptiles and amphibians in the southwestern United States. Journal of Wildlife Management, 87, 1-24.

[45] Intergovernmental Panel on Climate Change. (2022) Climate Change 2022 - Mitigation of Climate Change - Summary for Policymakers (SPM).

[46] Isbell,F., Balvanera, P., Mori,A.S., He,J.S., Bullock, J.M., Regmi,G.R. et al. (2023) Expert perspectives on global biodiversity loss and its drivers and impacts on people. Frontiers in Ecology and the Environment, 21, 94-103.

[47] IUCN. (2021) The IUCN Redlist of Threatened Species. Version 2021-3. Available from: https://www.iucnredlist.org

[48] IUCN. (2024) The IUCN Red List of Threatened Species. Version 2024-1. Available from: www.iucnredlist.org

[49] Jamwal,P.S., Di Febbraro, M., Carranza,M.L., Savage,M. & Loy, A. (2022) Global change on the roof of the world: vulnerability of Himalayan otter species to land use and climate alterations. Diversity and Distributions, 28, 1635-1649.

[50] Kingsolver,J.G., Pfennig, D.W., Kingsolver,J.G. & Pfennig,D.W. (2004) Individual-level selection as a cause of cope’s rule of phyletic size increase. Evolution, 58, 1608-1612.

[51] M. Lannoo (Ed.) (2005) Amphibian Declines: The Conservation Status of United States Species. Berkeley and Los Angeles, California: University of California Press.

[52] LeDee,O.E., Handler, S.D., Hoving,C.L., Swanston,C.W. & Zuckerberg, B. (2021) Preparing wildlife for climate change: how far have we come? Journal of Wildlife Management, 85, 7-16.

[53] Leung,J.Y.S., Russell, B.D., Coleman,M.A., Kelaher,B.P. & Connell, S.D. (2021) Long-term thermal acclimation drives adaptive physiological adjustments of a marine gastropod to reduce sensitivity to climate change. Science of the Total Environment, 771, 145208.

[54] Liebezeit,J., Rowland, E., Cross,M. & Zack,S. 2012. Assessing climate change vulnerability of breeding birds in arctic alaska. A report prepared for the Arctic Landscape Conservation Cooperative. Bozeman, MT.

[55] Luedtke,J.A., Chanson, J., Neam,K., Hobin,L., Maciel,A.O., Catenazzi,A. et al. (2023) Ongoing declines for the world’s amphibians in the face of emerging threats. Nature, 622, 308-314.

[56] Martin,T.G., Kehoe,L., Mantyka-Pringle,C., Chades,I., Wilson,S., Bloom,R.G. et al. (2018) Prioritizing recovery funding to maximize conservation of endangered species. Conservation Letters, 11, 1-9.

[57] Mawdsley,J.R., O’Malley, R. & Ojima,D.S. (2009) A review of climate-change adaptation strategies for wildlife management and biodiversity conservation. Conservation Biology, 23, 1080-1089.

[58] McKinney,M.L. (1997) Extinction vulnerability and selectivity: combining ecological and paleontological views. Annual Review of Ecology and Systematics, 28, 495-516.

[59] McKinney,M.L. (1999) High rates of extinction and threat in poorly studied taxa. Conservation Biology, 13, 1273-1281.

[60] McMahon,G., Gregonis, S.M., Waltman,S.W., Omernik,J.M., Thorson, T.D., Freeouf,J.A. et al. (2001) Developing a spatial framework of common ecological regions for the conterminous United States. Environmental Management, 28, 293-316.

[61] Miller,D.A.W., Grant,E.H.C., Muths,E., Amburgey, S.M., Adams,M.J. Joseph,M.B. et al. (2018) Quantifying climate sensitivity and climate-driven change in North American amphibian communities. Nature Communications, 9, 3926.

[62] Mills,L.S., Bragina, E.V., Kumar,A.V., Zimova,M., Lafferty, D.J.R., Feltner,J. et al. (2018) Winter color polymorphisms identify global hot spots for evolutionary rescue from climate change. Science, 359, 1033-1036.

[63] Moore,C.E., Helmann, J.S., Chen,Y., Amour,S.M.S.t, Hallmark, M.A. Hughes,L.E. et al. (2020) Anuran traits of the United States (ATraiU): a database for anuran traits-based conservation, management, and research. Ecology, 102, 3261.

[64] Nowakowski,A.J., Frishkoff, L.O., Agha,M., Todd, B.D. & Scheffers,B.R. (2018) Changing thermal landscapes: merging climate science and landscape ecology through thermal biology. Current Landscape Ecology Reports, 3, 57-72.

[65] Oliveira,B.F., São-Pedro, V.A., Santos-Barrera,G., Penone,C. & Costa, G.C. (2017) AmphiBIO, a global database for amphibian ecological traits. Scientific Data, 4, 170123.

[66] Pacifici,M., Foden,W.B., Visconti,P., Watson,J.E.M., Butchart, S.H.M., Kovacs,K.M. et al. (2015) Assessing species vulnerability to climate change. Nature Climate Change, 5, 215-224.

[67] Parmesan,C., Morecroft, M.D., Trisurat,Y., Adrian,R., Anshari, G.Z., Arneth,A. et al. (2022) Terrestrial and Freshwater Ecosystems and their Services. In: H.-O. Portner, D.C. Roberts, M. Tignor, E.S. Poloczanska, K. Mintenbeck, A. Alegria et al. (Eds.) Climate change 2022: impacts, adaptation, and vulnerability. contribution of Working Group II to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK and New York, NY, USA: Cambridge University Press, pp. 197-377.

[68] Pearson,R.G., Stanton, J.C., Shoemaker,K.T., Aiello-Lammens,M.E., Ersts, P.J., Horning,N. et al. (2014) Life history and spatial traits predict extinction risk due to climate change. Nature Climate Change, 4, 217-221.

[69] Petranka,J.W. (1998) Salamanders of the United States and Canada. Washington, D.C.: Smithsonian Institution Press.

[70] Pettus,D. & Angleton, G.M. (1967) Comparative reproductive biology of montane and Piedmont chorus frogs. Evolution, 21, 500.

[71] Price,S.J., Leung,W.T.M., Owen,C.J., Puschendorf, R., Sergeant,C., Cunningham,A.A. et al. (2019) Effects of historic and projected climate change on the range and impacts of an emerging wildlife disease. Global Change Biology, 25, 2648-2660.

[72] Rangwala,I., Moss,W., Wolken,J., Rondeau, R., Newlon,K., Guinotte,J. et al. (2021) Uncertainty, complexity and constraints: how do we robustly assess biological responses under a rapidly changing climate? Climate, 9, 177.

[73] Ray,A.M., Gould,W.R., Hossack,B.R., Sepulveda,A.J., Thoma,D.P., Patla,D.A. et al. (2016) Influence of climate drivers on colonization and extinction dynamics of wetland-dependent species. Ecosphere, 7, 1-21.

[74] Roberts,L.J., Burnett, R., Tietz,J. & Veloz,S. (2019) Recent drought and tree mortality effects on the avian community in southern Sierra Nevada: a glimpse of the future? Ecological Applications, 29, e01848.

[75] Sæther,B.-E., Ringsby, T.H., Røskaft,E., Saether,B.-E. & Roskaft, E. (1996) Life history variation, population processes and priorities in species conservation: towards a reunion of research paradigms. Oikos, 77, 217.

[76] Schwalm,C.R., Glendon, S. & Duffy,P.B. (2020) RCP8.5 tracks cumulative CO2 emissions. Proceedings of the National Academy of Sciences, 117, 19656-19657.

[77] Stearns,S.C. (1992) The evolution of life histories. New York: Oxford University Press.

[78] Steel,Z.L., Wilkerson, M., Grof-Tisza,P. & Sulzner,K. 2011. Assessing species and area vulnerability to climate change for the Oregon Conservation Strategy: Willamette Valley Ecoregion. Davis, CA.

[79] Stephenson,N. (1998) Actual evapotranspiration and deficit: biologically meaningful correlates of vegetation distribution across spatial scales. Journal of Biogeography, 25, 855-870.

[80] Szcodronski,K.E., Bannister, I.T., Hossack,B.R. & Wade,A.A. (2022) Integrating climate-informed planning into State Wildlife Action Plans in the north central United States. Cooperator Report. U.S. Geological Survey North Central Climate Adaptation Science Center, 1, 1-41.

[81] Szcodronski,K.E., Wade, A.A., Burton,S.E. & Hossack,B.R. (2024) Incorporating projected climate conditions to map future riparian refugia. Conservation Science and Practice, 6, e13183.

[82] Teixeira,J.C. & Huber, C.D. (2021) The inflated significance of neutral genetic diversity in conservation genetics. Proceedings of the National Academy of Sciences, 118, 1-10.

[83] Thurman,L.L., Stein,B.A., Beever,E.A., Foden,W., Geange,S.R., Green,N. et al. (2020) Persist in place or shift in space? Evaluating the adaptive capacity of species to climate change. Frontiers in Ecology and the Environment, 18, 520-528.

[84] Torda,G., Donelson, J.M., Aranda,M., Barshis,D.J., Bay,L., Berumen,M.L. et al. (2017) Rapid adaptive responses to climate change in corals. Nature Climate Change, 7, 627-636.

[85] Tuberville,T.D., Andrews, K.M., Sperry,J.H. & Grosse,A.M. (2015) Use of the NatureServe climate change vulnerability index as an assessment tool for reptiles and amphibians: lessons learned. Environmental Management, 56, 822-834.

[86] U.S. Environmental Protection Agency. (2013) Level III ecoregions of the continental United States. Corvallis, Oregon, USA.

[87] U.S. Environmental Protection Agency. (2017) Integrated Climate and Land Use Scenarios (ICLUS) Version 2. Washington, D.C.

[88] Wade,A.A., Hand,B.K., Kovach,R.P., Luikart,G., Whited,D.C. & Muhlfeld,C.C. (2017) Accounting for adaptive capacity and uncertainty in assessments of species’ climate-change vulnerability. Conservation Biology, 31, 136-149.

[89] Walls,S., Barichivich, W. & Brown,M. (2013) Drought, deluge and declines: the impact of precipitation extremes on amphibians in a changing climate. Biology, 2, 399-418.

[90] Wintle,B.A., Bekessy, S.A., Keith,D.A., Van Wilgen,B.W., Cabeza, M., Schröder,B. et al. (2011) Ecological-economic optimization of biodiversity conservation under climate change. Nature Climate Change, 1, 355-359.

[91] Womack,M.C., Steigerwald, E., Blackburn,D.C., Cannatella,D.C., Catenazzi, A., Che,J. et al. (2022) State of the amphibia 2020: a review of five years of amphibian research and existing resources. Ichthyology & Herpetology, 110, 638-661.

[92] Young,B.E., Dubois,N.S. & Rowland,E.L. (2015) Using the climate change vulnerability index to inform adaptation planning: lessons, innovations, and next steps. Wildlife Society Bulletin, 39, 174-181.

RIGHTS & PERMISSIONS

Published 2024. This article is a U.S. Government work and is in the public domain in the USA. Integrative Conservation published by John Wiley & Sons Australia, Ltd on behalf of Xishuangbanna Tropical Botanical Garden (XTBG).