Abstract
Biotic interactions and environmental factors influence a species’ occurrence. Facilitative interactions have the potential to expand species occupancy and mitigate abiotic stress, but are often not considered. The Great Basin clade of the Columbia spotted frog (Rana luteiventris) is an aquatic amphibian found in the arid and semi-arid Great Basin, USA. Aquatic resources in this system are limited and likely to change under future climate scenarios. American beavers (Castor canadensis) are ecosystem engineers that impact the surrounding landscape by increasing water availability. Consequently, beaver-created habitat can facilitate the presence of other species by providing the aquatic resources required by many aquatic and riparian animals. Our objective was to understand patterns of co-occurrence between Columbia spotted frogs and beavers across environmental gradients in the Great Basin, USA. We used environmental DNA detections to quantify the co-occurrence of Columbia spotted frog and beaver using a two-species occupancy framework. At the lowest annual precipitation (202 mm), Columbia spotted frogs were 3× (95% CI 2.35, 3.96) more likely to occur with beavers than without; however, they were less likely to occur with beavers once precipitation was > 380 mm. Thus, beaver activity may increase aquatic resources for Columbia spotted frogs in the Great Basin that may mitigate changing precipitation patterns under climate change. Facilitative interactions likely extend to other aquatic species in arid systems and highlight an important consideration for ecologists when evaluating a species’ response to climate change, and may promote the formation of refugia for species with strict abiotic tolerances and dispersal limitations.
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Data availability statement
Dataset used in this study is available on the Figshare repository. Figshare, dataset, https://doi.org/10.6084/m9.figshare.18282185.v1.
References
Afkhami ME, McIntyre PJ, Strauss SY (2014) Mutualist-mediated effects on species’ range limits across large geographic scales. Ecol Lett 17:1265–1273
Albert S, Trimble T (2000) Beavers are partners in riparian restoration on the Zuni Indian reservation. Ecol Restor 18:87–92
Aragón P, Carrascal LM, Palomino D (2018) Macro-spatial structure of biotic interactions in the distribution of a raptor species. J Biogeogr 45:1859–1871
Arkle RS, Pilliod DS (2015) Persistence at distributional edges: Columbia spotted frog habitat in the arid Great Basin, USA. Ecol Evol 5:3704–3724
Arnhold TR, Penha J, Peoples BK, Mateus LAF (2019) Positive co-occurrence between feeding-associative savannah fishes depends on species and habitat. Freshw Biol 64:1029–1039
Ashcroft MB (2010) Identifying refugia from climate change. J Biogeogr 37:1407–1413
Baker BW, Ducharme HC, Mitchell DCS, Stanley TR, Peinetti HR (2005) Interaction of beaver and elk herbivory reduces standing crop of willow. Ecol Appl 15:110–118
Barnes MA, Turner CR, Jerde CL, Renshaw MA, Chadderton WL, Lodge DM (2014) Environmental conditions influence eDNA persistence in aquatic systems. Environ Sci Technol 48:1819–1827
Barrile GM, Walters A, Webster M, Chalfoun AD (2021) Informed breeding dispersal following stochastic changes to patch quality in a pond-breeding amphibian. J Anim Ecol 90:1878–1890
Beier P, Barrett RH (1987) Beaver habitat use and impact in Truckee river basin, California. J Wildl Manag 51:794–799
Brown JH (1971) Mechanisms of competitive exclusion between two species of chipmunks. Ecology 52:305–311
Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125
Bull EL (2005) Ecology of the Columbia spotted frog in northeastern Oregon. Gen. Tech. Rep. PNW-GTR-640. Portland, OR: U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station. 46
Cayan DR, Das T, Pierce DW, Barnett TP, Tyree M, Gershunov A (2010) Future dryness in the southwest US and the hydrology of the early 21st century drought. Proc Natl Acad Sci USA 107:21271–21276
Cubashi U, Meehl GA, Boer GJ (2001) Projections of future climate change. In: Houghton JT (eds.) Climate Change 2001: The Scientific Basis. Cambridge University Press, Cambridge, pp 525–582
Cunningham JM, Calhoun AJK, Glanz WE (2007) Pond-Breeding Amphibian Species Richness and Habitat Selection in a Beaver-Modified Landscape. J Wildl Manag 71:2517–2526
Davis AJ, Jenkinson LS, Lawton JH, Shorrocks B, Wood S (1998) Making mistakes when predicting shifts in species range in response to global warming. Nature 391:783–786
DeVries P, Fetherston KL, Vitale A, Madsen S (2012) Emulating Riverine Landscape Controls of Beaver in Stream Restoration Emulating Riverine Landscape Controls of Beaver in Stream Restoration. Fisheries 37:246–255
Engelhardt EK, Neuschulz EL, Hof C (2020) Ignoring biotic interactions overestimates climate change effects: the potential response of the spotted nutcracker to changes in climate and resource plants. J Biogeogr 47:143–154
Gibson PP, Olden JD (2014) Ecology, management, and conservation implications of North American beaver (Castor canadensis) in dryland streams. Aquat Conserv Mar Freshwat Ecosyst 24:391–409
Goldberg CS, Pilliod DS, Arkle RS, Waits LP (2011) Molecular detection of vertebrates in stream water: a demonstration using rocky mountain tailed frogs and Idaho Giant Salamanders. PLoS ONE 6:e22746
Goldberg CS, Turner CR, Deiner K, Klymus KE, Thomsen PF, Murphy MA, Spear SF, McKee A, Oyler-McCance SJ, Cornman RS, Laramie MB, Mahon AR, Lance RF, Pilliod DS, Strickler KM, Waits LP, Fremier AK, Takahara T, Herder JE, Taberlet P, Gilbert M (2016) Critical considerations for the application of environmental DNA methods to detect aquatic species. Methods Ecol Evol 7:1299–1307
Guisan A, Thuiller W (2005) Predicting species distribution: offering more than simple habitat models. Ecol Lett 8:993–1009
Hay KG (2010) Succession of beaver ponds in Colorado 50 years after beaver removal. J Wildl Manag 74(8):1732–1736. https://doi.org/10.2193/2009-055
Haynes TB, Schmutz JA, Lindberg MS, Wright KG, Uher-Koch BD, Rosenberger AE (2014) Occupancy of yellow-billed and Pacific loons: evidence for interspecific competition and habitat mediated co-occurrence. J Avian Biol 45:296–304
Hossack BR, Gould WR, Patla DA, Muths E (2015) Trends in Rocky Mountain amphibians and the role of beaver as a keystone species. Biol Cons 187:260–269
Hurd B, Leafy N, Jones R, Smith J (1999) Relative regional vulnerability of water resources to climate change. J Am Water Resour Assoc 35:1399–1409
Hurvich CM, Tsai CL (1989) Regression and time series model selection in small samples. Biometrika 76:297–307
Karraker NE, Gibbs JP (2009) Amphibian production in forested landscapes in relation to wetland hydroperiod: a case study of vernal pools and beaver ponds. Biol Cons 142:2293–2302
Keppel G, Van Niel KP, Wardell-Johnson GW, Yates CJ, Byrne M, Mucina L, Schut AGT, Hopper SD, Franklin SE (2012) Refugia: identifying and understanding safe havens for biodiversity under climate change. Glob Ecol Biogeogr 21:393–404
Keppel G, Mokany K, Wardell-Johnson GW, Phillips BL, Welbergen JA, Reside AE (2015) The capacity of refugia for conservation planning under climate change. Front Ecol Environ 13:106–112
Larkin MA, Blackshields G, Brown NP, Chenna R, Mcgettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640
Loarie SR, Carter BE, Hayhoe K, McMahon S, Moe R, Knight CA, Ackerly DD (2008) Climate change and the future of California’s endemic flora. PLoS ONE 3:e2502
Mackenzie DI, Bailey LL, Nichols JD (2004) Investigating species co-occurrence patterns when species are detected imperfectly. J Anim Ecol 73:546–555
Majerova M, Neilson BT, Schmadel NM, Wheaton JM, Snow CJ (2015) Impacts of beaver dams on hydrologic and temperature regimes in a mountain stream. Hydrol Earth Syst Sci 19:3541–3556
Müller-Schwarze D, Schulte BA (1999) Behavorial and ecological characteristics of a “climax” population of beaver (Castor canadensis). In: Busher PE, Dzieclolowski RM (eds) Beaver protection, management, and utilization in Europe and North America. Kluwer Academic/Plenum Press, New York, pp 161–177
Oja EB, Swartz LK, Muths E, Hossack BR (2021) Amphibian population responses to mitigation: Relative importance of wetland age and design. Ecol Indic 131
Peoples BK, Frimpong EA (2016) Biotic interactions and habitat drive positive co-occurrence between facilitating and beneficiary stream fishes. J Biogeogr 43:923–931
Petranka JW, Harp EM, Holbrook CT, Hamel JA (2007) Long-term persistence of amphibian populations in a restored wetland complex. Biol Cons 138:371–380
Pilliod DS, Peterson CR, Ritson PI (2002) Seasonal migration of Columbia spotted frogs (Rana luteiventris) among complementary resources in a high mountain basin. Can J Zool 80:1849–1862
Pilliod DS, Arkle RS, Robertson JM, Murphy MA, Funk WC (2015) Effects of changing climate on aquatic habitat and connectivity for remnant populations of a wide-ranging frog species in an arid landscape. Ecol Evol 5:3979–3994
Pilliod DS, Rohde AT, Charnley S, Davee RR, Dunham JB, Gosnell H, Grant GE, Hausner MB, Huntington JL, Nash C (2018) Survey of beaver-related restoration practices in rangeland streams of the western USA. Environ Manag 61:58–68
Pilliod DS, Hausner MB, Scherer RD (2021) From satellites to frogs: quantifying ecohydrological change, drought mitigation, and population demography in desert meadows. Sci Total Environ 758:143632
Pollock MM, Beechie TJ, Wheaton JM, Jordan CE, Bouwes N, Weber N, Volk C (2014) Using beaver dams to restore incised stream ecosystems. Bioscience 64:279–290
Popescu VD, Gibbs JP (2009) Interactions between climate, beaver activity, and pond occupancy by the cold-adapted mink frog in New York State, USA. Biol Cons 142:2059–2068
Richmond OMW, Hines JE, Beissinger SR (2010) Two-species occupancy models: a new parameterization applied to co-occurrence of secretive rails. Ecol Appl 20:2036–2046
Ritter TD, Gower CN, McNew LB (2020) Habitat conditions at beaver settlement sites: implications for beaver restoration projects. Restor Ecol 28:196–205
Robinson QH, Bustos D, Roemer GW (2014) The application of occupancy modeling to evaluate intraguild predation in a model carnivore system. Ecology 95:3112–3123
Rosenzweig C, Karoly D, Vicarelli M et al (2008) Attributing physical and biological impacts to anthropogenic climate change. Nature 453:353–357. https://doi.org/10.1038/nature06937
Rota CT, Ferreira MAR, Kays RW, Forrester TD, Kalies EL, McShea WJ, Parsons AW, Millspaugh JJ (2016) A multispecies occupancy model for two or more interacting species. Methods Ecol Evol 7:1164–1173
Serrano PK (2011) Molecular phylogeography of the American beaver (Castor canadensis): Implications for management and conservation. The University of Arizona, Dissertation
Sherry TW, Holmes RT (1988) Habitat selection by breeding American Redstarts in response to a dominant competitor the Least Flycatcher. Auk 105(2):350–364. https://doi.org/10.2307/4087501
Smith MM, Goldberg CS (2020) Occupancy in dynamic systems: accounting for multiple scales and false positives using environmental DNA to inform monitoring. Ecography 43:376–386
Steen DA, Mcclure CJW, Brock JC, Craig Rudolph D, Pierce JB, Lee JR, Jeffrey Humphries W, Gregory BB, Sutton WB, Smith LL, Baxley DL, Stevenson DJ, Guyer C (2014) Snake co-occurrence patterns are best explained by habitat and hypothesized effects of interspecific interactions. J Anim Ecol 83:286–295
Strickler KM, Fremier AK, Goldberg CS (2015) Quantifying effects of UV-B, temperature, and pH on eDNA degradation in aquatic microcosms. Biol Cons 183:85–92
White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:S120–S138
White SM, Rahel FJ, Ahel FRJR, White SM, Rahel FJ (2008) Complementation of habitats for Bonneville cutthroat trout in watersheds influenced by beavers, livestock, and drought. Trans Am Fish Soc 137:881–894
Willems EP, Hill RA (2009) Predator-specific landscapes of fear and resource distribution: effects on spatial range use. Ecology 90:546–555
Wisz MS, Pottier J, Kissling WD, Pellissier L, Lenoir J, Damgaard CF, Dormann CF, Forchhammer MC, Grytnes JA, Guisan A, Heikkinen RK, Høye TT, Kühn I, Luoto M, Maiorano L, Nilsson MC, Normand S, Öckinger E, Schmidt NM, Termansen M, Timmermann A, Wardle DA, Aastrup P, Svenning JC (2013) The role of biotic interactions in shaping distributions and realised assemblages of species: Implications for species distribution modelling. Biol Rev 88:15–30
Xue T, Tang G, Sun L, Wu Y, Liu Y, Dou Y (2017) Long-term trends in precipitation and precitpitaiton extremes and underlying mechanisms in the U.S. Great Basin during 1951–2013. J Geophys Res Atmos 122:6152–6169
Yackulic CB, Reid J, Nichols JD, Hines JE, Davis R, Forsman E (2014) The roles of competition and habitat in the dynamics of populations and species distributions. Ecology 95:265–279
Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinform 13:134
Zero VH, Murphy MA (2016) An amphibian species of concern prefers breeding in active beaver ponds. Ecosphere 7:1–13
Acknowledgements
We thank David Pilliod for initiating the pilot study for eDNA sampling of this species and providing valuable advice on initial sampling design. Mitch Czerwinski and Caleb Klima provided field support and Robert Arkle provided information on previous modeling efforts. We thank Kelli Van Norman, Chad Mellison, Jeff Petersen, Teri Slatauski, Paul Makela, and Jeremy Bisson for their support and valuable knowledge of Columbia spotted frogs in the Great Basin. We thank Daniel Thornton and Rod Saylor for reviewing study design and providing feedback on results and conclusions of this study.
Funding
Funding for this project was provided by the Bureau of Land Management and U.S. Fish and Wildlife Service. The views and conclusions contained in this document are those of the authors and should not be interpreted as representing the opinions or policies of the U.S. Government. Mention of trade names or commercial products does not constitute their endorsement by the U.S. Government.
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MMS and CSG conceived idea and developed the methodology. MMS conducted fieldwork, performed molecular analysis, and analyzed the data. MMS and CSG wrote the manuscript.
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We demonstrate how facilitative interactions can promote occupancy in a semi-arid system; predicted to become warmer and drier. We used eDNA at regional scales to advance methodology and conservation.
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Communicated by Mathew Samuel Crowther.
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Smith, M.M., Goldberg, C.S. Facilitative interaction promotes occupancy of a desert amphibian across a climate gradient. Oecologia 198, 815–823 (2022). https://doi.org/10.1007/s00442-022-05127-6
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DOI: https://doi.org/10.1007/s00442-022-05127-6