Abstract
Environmental niche models (ENMs) are commonly used to inform management of invasive species, but invasive species often violate two key assumptions of ENMs which assert that species’ ecological niches are stable in space and time, and that organisms are in equilibrium with their environment. The American bullfrog (Rana catesbeiana) invasion in California provides an excellent opportunity to use ENM approaches recommended for overcoming these assumption violations to inform management of a harmful invader. In the current study, we used dynamic ENM approaches and explicit comparisons between native and invaded niches to: (1) examine how environmental drivers of occurrence in California shifted during the invasion process, and (2) investigate the potential for continued bullfrog expansion by explicitly assessing their environmental equilibrium. Since their initial introduction to metropolitan areas of California in the late 1800s, bullfrogs have spread throughout the state with the most notable recent expansions in coastal regions, the Central Valley, and the mountains of northern California. Bullfrog occurrence in California was consistently associated with human activity and higher winter temperature. Small pockets of high human activity have sustained bullfrog populations in otherwise unsuitable areas. The areas in California with the highest predicted risk of increased bullfrog abundance and future bullfrog expansion include the southern Central Valley, the coast of northern California, and mid elevations in the mountains of northern California. Continued bullfrog invasion in these areas is likely to impact sensitive native amphibian populations.
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Availability of data and material
This study relies on previously published datasets that are available from the following public domain resources: https://www.gbif.org/; https://bison.usgs.gov/#home; https://nas.er.usgs.gov/viewer/omap.aspx?; https://prism.oregonstate.edu/; https://apps.nationalmap.gov/downloader/#/; https://themasites.pbl.nl/tridion/en/themasites/hyde/download/index-2.html; https://datadryad.org/stash/dataset/doi:10.5061/dryad.052q5
Code availability
The code used for all analyses in this manuscript can be provided by the corresponding author upon request.
References
Adams A (2017) Decline and localized extirpation of the foothill yellow-legged frog (Rana boylii) in the presence of the fungal pathogen, Batrachochytrium dendrobatidis: Contemporary and historical perspectives. PhD Thesis, UC Santa Barbara
Allen CR, Nemec KT, Wardwell DA et al (2013) Predictors of regional establishment success and spread of introduced non-indigenous vertebrates. Glob Ecol Biogeogr 22:889–899. https://doi.org/10.1111/geb.12054
Arim M, Abades SR, Neill PE et al (2006) Spread dynamics of invasive species. Proc Natl Acad Sci 103:374–378. https://doi.org/10.1073/pnas.0504272102
Barbet-Massin M, Rome Q, Villemant C, Courchamp F (2018) Can species distribution models really predict the expansion of invasive species? PLoS ONE. https://doi.org/10.1371/journal.pone.0193085
Beale CM, Lennon JJ (2012) Incorporating uncertainty in predictive species distribution modelling. Philos Trans R Soc B 367:247–258. https://doi.org/10.1098/rstb.2011.0178
BISON.usgs.gov (2021) BISON occurrence download
Bissattini AM, Vignoli L (2017) Let’s eat out, there’s crayfish for dinner: American bullfrog niche shifts inside and outside native ranges and the effect of introduced crayfish. Biol Invasions 19:2633–2646. https://doi.org/10.1007/s10530-017-1473-6
Broennimann O, Guisan A (2008) Predicting current and future biological invasions: both native and invaded ranges matter. Biol Lett 4:585–589. https://doi.org/10.1098/rsbl.2008.0254
Brown C, Hayes MP, Green G, et al (2015) Yosemite toad conservation assessment. USDA Forest Service, CA Department of Fish and Wildlife, National Park Service, US Fish and Wildlife Service
Brown C, Hayes MP, Green G, Macfarlane D (2014) Mountain yellow-legged frog conservation assessment for the Sierra Nevada mountains of California, USA. USDA Forest Service, CA Department of Fish and Wildlife, National Park Service, US Fish and Wildlife Service
Bury RB, Whelan JA (1984) Ecology and management of the bullfrog. US Fish and Wildlife Service, Denver Wildlife Research Center
Conant R, Collins JP (1991) A field guide to reptiles and amphibians: Eastern/Central North America. Houghton Mifflin, Boston
D’Amore A, Hemingway V, Wasson K (2009) Do a threatened native amphibian and its invasive congener differ in response to human alteration of the landscape? Biol Invasions 12:145. https://doi.org/10.1007/s10530-009-9438-z
Didham RK, Tylianakis JM, Gemmell NJ et al (2007) Interactive effects of habitat modification and species invasion on native species decline. Trends Ecol Evol 22:489–496. https://doi.org/10.1016/j.tree.2007.07.001
Doubledee RA, Muller EB, Nisbet RM (2003) Bullfrogs, disturbance regimes, and the persistence of California red-legged frogs. J Wildl Manag 67:424–438. https://doi.org/10.2307/3802783
Ehrlich P (1989) Attributes of invaders and the invading processes vertebrates. Biol Invasions Glob Perspect pp 315–328
Elith J, Kearney M, Phillips S (2010) The art of modelling range-shifting species. Methods Ecol Evol 1:330–342. https://doi.org/10.1111/j.2041-210X.2010.00036.x
Fernandez M, Hamilton H (2015) Ecological niche transferability using invasive species as a case study. PLoS ONE. https://doi.org/10.1371/journal.pone.0119891
Ficetola GF, Maiorano L, Falcucci A et al (2010) Knowing the past to predict the future: land-use change and the distribution of invasive bullfrogs. Glob Change Biol 16:528–537. https://doi.org/10.1111/j.1365-2486.2009.01957.x
Ficetola GF, Thuiller W, Miaud C (2007) Prediction and validation of the potential global distribution of a problematic alien invasive species — the American bullfrog. Divers Distrib 13:476–485. https://doi.org/10.1111/j.1472-4642.2007.00377.x
Fourcade Y, Engler JO, Rödder D, Secondi J (2014) Mapping species distributions with MAXENT using a geographically biased sample of presence data: a performance assessment of methods for correcting sampling bias. PLoS ONE. https://doi.org/10.1371/journal.pone.0097122
Gahl MK, Calhoun AJK, Graves R (2009) Facultative use of seasonal pools by American bullfrogs (Rana catesbeiana). Wetlands 29:697–703. https://doi.org/10.1672/08-56.1
Gallien L, Douzet R, Pratte S et al (2012) Invasive species distribution models – how violating the equilibrium assumption can create new insights. Glob Ecol Biogeogr 21:1126–1136. https://doi.org/10.1111/j.1466-8238.2012.00768.x
Garcia TS, Rowe JC, Doyle JB (2015) A tad too high: Sensitivity to UV-B radiation may limit invasion potential of American bullfrogs (Lithobates catesbeianus) in the Pacific Northwest invasion range. Aquat Invasions 10:237–247. https://doi.org/10.3391/ai.2015.10.2.12
GBIF (2020) GBIF occurrence download - Amphibia. Accessed 20 Oct 2020
Goldewijk KK, Beusen A, de Vos M, van Drecht G (2011) The HYDE 3.1 spatially explicit database of human induced land use change over the past 12,000 years. Glob Ecol Biogeogr 20:73–86
Guisan A, Thuiller W (2005) Predicting species distribution: offering more than simple habitat models. Ecol Lett 8:993–1009
Hartley S, Harris R, Lester PJ (2006) Quantifying uncertainty in the potential distribution of an invasive species: climate and the Argentine ant. Ecol Lett 9:1068–1079. https://doi.org/10.1111/j.1461-0248.2006.00954.x
Hattab T, Garzon-Lopez CX, Ewald M et al (2017) A unified framework to model the potential and realized distributions of invasive species within the invaded range. Divers Distrib 23:806–819. https://doi.org/10.1111/ddi.12566
Herrel A, van der Meijden A (2014) An analysis of the live reptile and amphibian trade in the USA compared to the global trade in endangered species. Herpetol J 24:103–110
Hijmans RJ, Phillips AS, Leathwick JR, Elith J (2011) Package “dismo.” http://cran.r-project.org/web/packages/dismo/index.html
Hijmans RJ, van Etten J (2012) raster: Geographic analysis and modeling with raster data. R Package Version 20–12
IUCN (2020) Lithobates catesbeianus. In: IUCN Red List Threat. Species
Jennings MR, Hayes MP (1985) Pre-1900 overharvest of California red-legged frogs (Rana aurora draytonii): The inducement for bullfrog (Rana catesbeiana) introduction. Herpetologica 41:94–103
Jiménez-Valverde A, Peterson AT, Soberón J et al (2011) Use of niche models in invasive species risk assessments. Biol Invasions 13:2785–2797. https://doi.org/10.1007/s10530-011-9963-4
Johovic I, Gama M, Banha F et al (2020) A potential threat to amphibians in the European Natura 2000 network: Forecasting the distribution of the American bullfrog Lithobates catesbeianus. Biol Conserv 245:108551. https://doi.org/10.1016/j.biocon.2020.108551
Kupferberg SJ (1997) Bullfrog (Rana catesbeiana) invasion of a California river: the role of larval competition. Ecology 78:1736–1751. https://doi.org/10.1890/0012-9658(1997)078[1736:BRCIOA]2.0.CO;2
Lawler SP, Dritz D, Strange T, Holyoak M (1999) Effects of introduced mosquitofish and bullfrogs on the threatened California red-legged frog. Conserv Biol 13:613–622. https://doi.org/10.1046/j.1523-1739.1999.98075.x
Leutner B, Horning N, Schwalb-Willmann J, Hijmans RJ (2019) Tools for remote sensing data analysis. In: CRAN
Lobo JM, Jiménez-Valverde A, Real R (2008) AUC: a misleading measure of the performance of predictive distribution models. Glob Ecol Biogeogr 17:145–151. https://doi.org/10.1111/j.1466-8238.2007.00358.x
Lowe S, Browne M, Boudjelas S, de Poorter M (2000) 100 of the world’s worst invasive alien species: a selection from the Global Invasive Species Database. The Invasive Species Specialist Group
McKercher L, Gregoire DR (2021) Lithobates catesbeianus (Shaw, 1802). In: US Geol. Surv. Nonindigenous Aquat. Species Database
Miaud C, Dejean T, Savard K et al (2016) Invasive North American bullfrogs transmit lethal fungus Batrachochytrium dendrobatidis infections to native amphibian host species. Biol Invasions 18:2299–2308. https://doi.org/10.1007/s10530-016-1161-y
Morey S (1988) American bullfrog (Lithobates catesbeianus). California Department of Fish and Wildlife California Interagency Wildlife Task Group, Sacramento, California
Moyle PB (1973) Effects of introduced bullfrogs, Rana catesbeiana, on the native frogs of the San Joaquin Valley, California. Copeia 1973:18–22. https://doi.org/10.2307/1442351
Murray RG, Popescu VD, Palen WJ, Govindarajulu P (2015) Relative performance of ecological niche and occupancy models for predicting invasions by patchily-distributed species. Biol Invasions 17:2691–2706. https://doi.org/10.1007/s10530-015-0906-3
Naimi B, Araujo MB (2016) sdm: a reproducible and extensible R platform for species distribution modelling. Ecography 39:368–375. https://doi.org/10.1111/ecog.01881
Newman M, Alexander MA, Ault TR et al (2016) The pacific decadal oscillation, revisited. J Clim 29:4399–4427. https://doi.org/10.1175/JCLI-D-15-0508.1
Nori J, Akmentins MS, Ghirardi R et al (2011) American bullfrog invasion in Argentina: where should we take urgent measures? Biodivers Conserv 20:1125–1132. https://doi.org/10.1007/s10531-011-0014-3
Palen WJ, Schindler DE (2010) Water clarity, maternal behavior, and physiology combine to eliminate UV radiation risk to amphibians in a montane landscape. Proc Natl Acad Sci 107:9701–9706. https://doi.org/10.1073/pnas.0912970107
Perry H (2020) Bullfrog CA locations (compiled from publicly available online datasets). California Department of Fish and Wildlife, West Sacramento, CA
Peterson AC, McKenzie VJ (2014) Investigating differences across host species and scales to explain the distribution of the amphibian pathogen Batrachochytrium dendrobatidis. PLoS ONE. https://doi.org/10.1371/journal.pone.0107441
Peterson AC, Richgels KLD, Johnson PTJ, McKenzie VJ (2013) Investigating the dispersal routes used by an invasive amphibian, Lithobates catesbeianus, in human-dominated landscapes. Biol Invasions 15:2179–2191. https://doi.org/10.1007/s10530-013-0442-y
Petitpierre B, Kueffer C, Broennimann O et al (2012) Climatic niche shifts are rare among terrestrial plant invaders. Science 335:1344–1348. https://doi.org/10.1126/science.1215933
Pope K, Brown C, Hayes M, et al (2014) Cascades frog conservation assessment. USDA Forest Serivice, Pacific Southwest Reserach Station
PRISM Climate Group (2020). In: Northwest Alliance Comput. Sci. Eng. Or. State Univ. http://prism.oregonstate.edu
Rhoades AM, Huang X, Ullrich PA, Zarzycki CM (2016) Characterizing Sierra Nevada snowpack using variable-resolution CESM. J Appl Meteorol Climatol 55:173–196. https://doi.org/10.1175/JAMC-D-15-0156.1
Runquist RDB, Lake T, Tiffin P, Moeller DA (2019) Species distribution models throughout the invasion history of Palmer amaranth predict regions at risk of future invasion and reveal challenges with modeling rapidly shifting geographic ranges. Sci Rep. https://doi.org/10.1038/s41598-018-38054-9
Sepulveda AJ, Layhee M (2015) Description of fall and winter movements of the introduced American bullfrog (Lithobates catesbeianus) in a Montana, USA, pond. Herpetol Conserv Biol 10:978–984
Soberón J (2007) Grinnellian and Eltonian niches and geographic distributions of species. Ecol Lett 10:1115–1123. https://doi.org/10.1111/j.1461-0248.2007.01107.x
Soberón J, Peterson AT (2005) Interpretation of models of fundamental ecological niches and species’ distributional areas
Srivastava V, Lafond V, Griess VC (2019) Species distribution models (SDM): applications, benefits and challenges in invasive species management. CAB Rev 14:1–13
Stebbins RC (2003) A field guide to western reptiles and amphibians, 3rd edn. Houghton Mifflin Company, Boston
Stewart ER, Reese SA, Ultsch GR (2004) The physiology of hibernation in Canadian leopard frogs (Rana pipiens) and bullfrogs (Rana catesbeiana). Physiol Biochem Zool 77:65–73. https://doi.org/10.1086/378921
Thornton DH, Peers MJL (2019) Species distribution modeling. In: Population ecology in practice: underused, misused and abused methods. Wiley-Blackwell, London
Thuiller W, Lafourcade B, Engler R, Araújo MB (2009) BIOMOD – a platform for ensemble forecasting of species distributions. Ecography 32:369–373. https://doi.org/10.1111/j.1600-0587.2008.05742.x
USGS (2004) National Hydrography Dataset. In: US Dep. Inter. US Geol Surv
Václavík T, Meentemeyer RK (2012) Equilibrium or not? Modelling potential distribution of invasive species in different stages of invasion. Divers Distrib 18:73–83. https://doi.org/10.1111/j.1472-4642.2011.00854.x
Van Buskirk J, Jansen van Rensburg A (2020) Relative importance of isolation-by-environment and other determinants of gene flow in an alpine amphibian. Evolution 74:962–978. https://doi.org/10.1111/evo.13955
Venter O, Sanderson EW, Magrach A, et al (2016) Data from: Global terrestrial Human Footprint maps for 1993 and 2009, v2, Dryad. Dataset
Whitney KD, Gabler CA (2008) Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Divers Distrib 14:569–580. https://doi.org/10.1111/j.1472-4642.2008.00473.x
Willis YL, Moyle DL, Baskett TS (1956) Emergence, breeding, hibernation, movements and transformation of the bullfrog, Rana catesbeiana, in Missouri. Copeia 1956:30–41. https://doi.org/10.2307/1439241
With KA (2002) The landscape ecology of invasive spread. Conserv Biol 16:1192–1203. https://doi.org/10.1046/j.1523-1739.2002.01064.x
Yalcin S, Leroux SJ, Jonathan B (2017) Diversity and suitability of existing methods and metrics for quantifying species range shifts. Glob Ecol Biogeogr 26:609–624. https://doi.org/10.1111/geb.12579
Yap TA, Koo MS, Ambrose RF, Vredenburg V (2018) Introduced bullfrog facilitates pathogen invasion in the western United States. PLoS ONE 13:e0188384
Acknowledgements
MS committee members Leslie New, Caren Goldberg, and Daniel Thornton provided guidance, feedback, and support throughout the duration of this study. Bullfrog occurrence records in California were provided by Laura Patterson and Heather Perry (California Department of Fish and Wildlife). Sky Button provided guidance on environmental niche modeling, and Babak Naimi (University of Helsinki) provided guidance on use of the sdm R package. The Scientific Writing Association for Graduate Students (SWAGS) and members of the Piovia-Scott lab at Washington State University gave feedback on writing.
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This material is based upon work supported by the National Science Foundation Graduate Research Fellowship Program under Grant No. 1842493.
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Both authors contributed to the study conception and design. NN obtained and prepared data, selected statistical analyses to be used in the study, ran statistical analyses, and produced figures and tables. NN wrote the first draft of the manuscript; JP-S contributed substantially to revisions of the manuscript. Both authors read and approved the final manuscript.
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Nelson, N., Piovia-Scott, J. Using environmental niche models to elucidate drivers of the American bullfrog invasion in California. Biol Invasions 24, 1767–1783 (2022). https://doi.org/10.1007/s10530-022-02744-3
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DOI: https://doi.org/10.1007/s10530-022-02744-3