[en] Climate change and invasive species are two major drivers of biodiversity loss and their interaction may lead to unprecedented further loss. Invasive ectotherms can be expected to tolerate temperature variation because of a broad thermal tolerance and may even benefit from warmer temperatures in their new ranges that better match their thermal preference. Multi-trait studies provide a valuable approach to elucidate the influence of temperature on the invasion process and offer insights into how climatic factors may facilitate or hinder the spread of invasive ectotherms.
We here used marsh frogs, Pelophylax ridibundus, a species that is invading large areas of Western Europe but whose invasive potential has been underestimated. We measured the maximal and minimal temperatures to sustain physical activity, the preferred temperature, and the thermal dependence of their stamina and jumping performance in relation to the environmental temperatures observed in their invasive range.
Our results showed that marsh frogs can withstand body temperatures that cover 100% of the annual temperature variation in the pond they live in and 77% of the observed current annual air temperature variation. Their preferred body temperature and performance optima were higher than the average temperature in their pond and the average air temperature experienced under the shade.
These data suggest that invasive marsh frogs may benefit from a warmer climate. Broad thermal tolerances, combined with high thermal preferences and traits maximized at high temperatures, may allow this species to expand their activity period and colonize underexploited shaded habitat, thereby promoting their invasion success.
Research center :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Padilla, Pablo ; Université de Liège - ULiège > Freshwater and OCeanic science Unit of reSearch (FOCUS) ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Laboratoire d'Écologie et de Conservation des Amphibiens (LECA)
Herrel, Anthony; MNHN - Muséum National d'Histoire Naturelle [FR]
Denoël, Mathieu ; Université de Liège - ULiège > Freshwater and OCeanic science Unit of reSearch (FOCUS) ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Laboratoire d'Écologie et de Conservation des Amphibiens (LECA)
Language :
English
Title :
May future climate change promote the invasion of the marsh frog? An integrative thermo-physiological study
Publication date :
June 2023
Journal title :
Oecologia
ISSN :
0029-8549
eISSN :
1432-1939
Publisher :
Springer, Germany
Volume :
202
Issue :
2
Pages :
227-238
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE] FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture [BE]
Ali E, Cramer W, Carnicer J et al (2022) Cross-chapter paper 4: Mediterranean region. In: Pörtner HO, Roberts DC, Tignor M, Poloczanska ES, Mintenbeck K, Alegría A, Craig M, Langsdorf S, Löschke S, Möller V, Okem A, Rama B (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 University Press, Cambridge, pp 2233–2272
Allen WL, Street SE, Capellini I (2017) Fast life history traits promote invasion success in amphibians and reptiles. Ecol Lett 20:222–230. 10.1111/ele.12728 DOI: 10.1111/ele.12728
Andersen D, Borzée A, Jang Y (2021) Predicting global climatic suitability for the four most invasive anuran species using ecological niche factor analysis. Glob Ecol Conserv 25:e01433. 10.1016/j.gecco.2020.e01433 DOI: 10.1016/j.gecco.2020.e01433
Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, Oxford. 10.1093/acprof:oso/9780198570875.001.1 DOI: 10.1093/acprof:oso/9780198570875.001.1
Angilletta MJ, Hill T, Robson MA (2002) Is physiological performance optimized by thermoregulatory behavior?: a case study of the eastern fence lizard, Sceloporus undulatus. J Therm Biol 27:199–204. 10.1016/S0306-4565(01)00084-5 DOI: 10.1016/S0306-4565(01)00084-5
Araspin L, Martinez AS, Wagener C et al (2020) Rapid shifts in the temperature dependence of locomotor performance in an invasive frog, Xenopus laevis, implications for conservation. Integr Comp Biol 60:456–466. 10.1093/icb/icaa010 DOI: 10.1093/icb/icaa010
Araújo MB, Thuiller W, Pearson RG (2006) Climate warming and the decline of amphibians and reptiles in Europe. J Biogeogr 33:1712–1728. 10.1111/j.1365-2699.2006.01482.x DOI: 10.1111/j.1365-2699.2006.01482.x
Batty RS, Blaxter JHS (1992) The effect of temperature on the burst swimming performance of fish larvae. J Exp Biol 170:187–201. 10.1242/jeb.170.1.187 DOI: 10.1242/jeb.170.1.187
Bennett AF (1984) Thermal dependence of muscle function. Am J Physiol 247:R217–R229
Bennett AF (1987) Evolution of the control of body temperature: is warmer better? In: Dejours P, Bolis L, Taylor CR, Weibel ER (eds) Comparative physiology: life in water and on land. Liviana Press, Padova, pp 421–431
Bennett AF (1990) Thermal dependence of locomotor capacity. Am J Physiol 259:R253–R258
Blaustein AR, Walls SC, Bancroft BA et al (2010) Direct and indirect effects of climate change on amphibian populations. Diversity 2:281–313. 10.3390/d2020281 DOI: 10.3390/d2020281
Bodensteiner BL, Agudelo-Cantero GA, Arietta AZA et al (2021) Thermal adaptation revisited: How conserved are thermal traits of reptiles and amphibians? J Exp Zool Part A Ecol Integr Physiol 335:173–194. 10.1002/jez.2414 DOI: 10.1002/jez.2414
Bulté G, Blouin-Demers G (2006) Cautionary notes on the descriptive analysis of performance curves in reptiles. J Therm Biol 31:287–291. 10.1016/j.jtherbio.2005.11.030 DOI: 10.1016/j.jtherbio.2005.11.030
Cattiaux J, Douville H, Schoetter R et al (2015) Projected increase in diurnal and interdiurnal variations of European summer temperatures. Geophys Res Lett 42:899–907. 10.1002/2014GL062531 DOI: 10.1002/2014GL062531
Cecchetto NR, Medina SM, Ibargüengoytía NR (2020) Running performance with emphasis on low temperatures in a Patagonian lizard, Liolaemus lineomaculatus. Sci Rep 10:1–13. 10.1038/s41598-020-71617-3 DOI: 10.1038/s41598-020-71617-3
Christy MT (1996) The efficacy of using passive integrated transponder (PIT) tags without anaesthetic in free-living frogs. Aust Zool 30:139–142. 10.7882/AZ.1996.004 DOI: 10.7882/AZ.1996.004
Cossins AR, Bowler K (1987) Temperature biology of animals. Chapman and Hall, London DOI: 10.1007/978-94-009-3127-5
Denoël M (2006) Seasonal variation of morph ratio in facultatively paedomorphic populations of the palmate newt Triturus helveticus. Acta Oecologica 29:165–170. 10.1016/j.actao.2005.09.003 DOI: 10.1016/j.actao.2005.09.003
Denoël M, Duret C, Lorrain-Soligon L et al (2022) High habitat invasibility unveils the invasiveness potential of water frogs. Biol Invasions 24:3447–3459. 10.1007/s10530-022-02849-9 DOI: 10.1007/s10530-022-02849-9
Deutsch CA, Tewksbury JJ, Huey RB et al (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci USA 105:6668–6672. 10.1073/pnas.0709472105 DOI: 10.1073/pnas.0709472105
Dillon ME, Woods HA, Wang G et al (2016) Life in the frequency domain: the biological impacts of changes in climate variability at multiple time scales. Integr Comp Biol 56:14–30. 10.1093/icb/icw024 DOI: 10.1093/icb/icw024
Doniol-Valcroze P, Mazepa G, Grimal F et al (2021) Discovery of a Pelophylax saharicus (Anura, Ranidae) population in Southern France: a new potentially invasive species of water frogs in Europe. Amphib Reptil 8:427–442. 10.1163/15685381-bja10066 DOI: 10.1163/15685381-bja10066
Dubey S, Leuenberger J, Perrin N (2014) Multiple origins of invasive and “native” water frogs (Pelophylax spp.) in Switzerland. Biol J Linn Soc 112:442–449. 10.1111/bij.12283 DOI: 10.1111/bij.12283
Dufresnes C, Mazepa G (2020) Hybridogenesis in water frogs. eLS 1:718–726. 10.1002/9780470015902.a0029090 DOI: 10.1002/9780470015902.a0029090
Dufresnes C, Denoël M, Di Santo L, Dubey S (2017a) Multiple uprising invasions of Pelophylax water frogs, potentially inducing a new hybridogenetic complex. Sci Rep 7:6506. 10.1038/s41598-017-06655-5 DOI: 10.1038/s41598-017-06655-5
Dufresnes C, Di Santo L, Leuenberger J et al (2017b) Cryptic invasion of Italian pool frogs (Pelophylax bergeri) across Western Europe unraveled by multilocus phylogeography. Biol Invasions 19:1407–1420. 10.1007/s10530-016-1359-z DOI: 10.1007/s10530-016-1359-z
Duret C, Pille F, Denoël M (2022) Efficiency of aquatic PIT-tag telemetry, a powerful tool to improve monitoring and detection of marked individuals in pond environments. Hydrobiologia 849:2609–2619. 10.1007/s10750-022-04888-8 DOI: 10.1007/s10750-022-04888-8
Galloy V, Denoël M (2010) Detrimental effect of temperature increase on the fitness of an amphibian (Lissotriton helveticus). Acta Oecologica 36:179–183. 10.1016/j.actao.2009.12.002 DOI: 10.1016/j.actao.2009.12.002
Gatten RE (1974) Effect of nutritional status on the preferred body temperature of the turtles Pseudemys scripta and Terrapene ornata. Copeia 1974:912–917 DOI: 10.2307/1442590
Ginal P, Kruger N, Wagener C et al (2023) More time for aliens? Performance shifts lead to increased activity time budgets propelling invasion success. Biol Invasions 25:267–283. 10.1007/s10530-022-02903-6 DOI: 10.1007/s10530-022-02903-6
Hellmann JJ, Byers JE, Bierwagen BG, Dukes JS (2008) Five potential consequences of climate change for invasive species. Conserv Biol 22:534–543. 10.1111/j.1523-1739.2008.00951.x DOI: 10.1111/j.1523-1739.2008.00951.x
Herrel A, Bonneaud C (2012a) Temperature dependence of locomotor performance in the tropical clawed frog, Xenopus tropicalis. J Exp Biol 215:2465–2470. 10.1242/jeb.069765 DOI: 10.1242/jeb.069765
Herrel A, Bonneaud C (2012b) Trade-offs between burst performance and maximal exertion capacity in a wild amphibian, Xenopus tropicalis. J Exp Biol 215:3106–3111. 10.1242/jeb.072090 DOI: 10.1242/jeb.072090
Herrel A, Vasilopoulou-Kampitsi M, Bonneaud C (2014) Jumping performance in the highly aquatic frog, Xenopus tropicalis: sex-specific relationships between morphology and performance. PeerJ 2:e661. 10.7717/peerj.661 DOI: 10.7717/peerj.661
Holsbeek G, Jooris R (2010) Potential impact of genome exclusion by alien species in the hybridogenetic water frogs (Pelophylax esculentus complex). Biol Invasions 12:1–13. 10.1007/s10530-009-9427-2 DOI: 10.1007/s10530-009-9427-2
Huang D, Haack RA, Zhang R (2011) Does global warming increase establishment rates of invasive alien species? a centurial time series analysis. PLoS One 6:e24733. 10.1371/journal.pone.0024733 DOI: 10.1371/journal.pone.0024733
Huey RB, Kingsolver JG (1989) Evolution of thermal sensitivity of ectotherm performance. Trends Ecol Evol 4:131–135. 10.1016/0169-5347(89)90211-5 DOI: 10.1016/0169-5347(89)90211-5
IPCC (2022) Climate change 2022: impacts, adaptation, and vulnerability. Contribution of working group ii to the sixth assessment report of the intergovernmental panel on climate change [H.-O. Pörtner, D.C. Roberts, M. Tignor, E.S. Poloczanska, K. Mintenbeck, A. Alegría, M. Craig, S. Langsdorf, S. Löschke, V. Möller, A. Okem, B. Rama (eds.)]. Cambridge University Press. Cambridge University Press
IUCN SSC Amphibian Specialist Group (2015) Lithobates catesbeianus. IUCN Red List Threat Species. 10.2305/IUCN.UK.2022-1.RLTS.T58565A193396825.en DOI: 10.2305/IUCN.UK.2022-1.RLTS.T58565A193396825.en
IUCN Ssc Amphibian Specialist Group (2020) Xenopus laevis. IUCN Red List Threat Species. 10.2305/IUCN.UK.2020-3.RLTS.T110466172A3066881.en DOI: 10.2305/IUCN.UK.2020-3.RLTS.T110466172A3066881.en
IUCN (2022) The IUCN red list of threatened species. Version 2022–2. https://www.iucnredlist.org. Accessed 16 Jan 2023
James RS, Tallis J, Herrel A, Bonneaud C (2012) Warmer is better: thermal sensitivity of both maximal and sustained power output in the iliotibialis muscle isolated from adult Xenopus tropicalis. J Exp Biol 215:552–558. 10.1242/jeb.063396 DOI: 10.1242/jeb.063396
Johnson CR (1972) Thermal relations and daily variation in the thermal tolerance in Bufo marinus. J Herpetol 6:35. 10.2307/1563091 DOI: 10.2307/1563091
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. 10.1016/j.biocon.2020.108551 DOI: 10.1016/j.biocon.2020.108551
Kellermann V, Chown SL, Schou MF et al (2019) Comparing thermal performance curves across traits: how consistent are they? J Exp Biol 222:jeb193433. 10.1242/jeb.193433 DOI: 10.1242/jeb.193433
Kelley AL (2014) The role thermal physiology plays in species invasion. Conserv Physiol 2:1–14. 10.1093/conphys/cou045 DOI: 10.1093/conphys/cou045
Kjellström E, Nikulin G, Strandberg G et al (2018) European climate change at global mean temperature increases of 1.5 and 2°C above pre-industrial conditions as simulated by the EURO-CORDEX regional climate models. Earth Syst Dyn 9:459–478. 10.5194/esd-9-459-2018 DOI: 10.5194/esd-9-459-2018
Larvor G, Berthomier L, Chabot V, Le Pape B, Pradel B, Perez L (2020) MeteoNet, an open reference weather dataset by METEO FRANCE. https://meteonet.umr-cnrm.fr. Accessed on 2022
Lotshaw DP (1977) Temperature adaptation and effects of thermal acclimation in Rana sylvatica and Rana catesbeiana. Comp Biochem Physiol Part A Physiol 56:287–294. 10.1016/0300-9629(77)90239-0 DOI: 10.1016/0300-9629(77)90239-0
Lotze HK, Tittensor DP, Bryndum-Buchholz A et al (2019) Global ensemble projections reveal trophic amplification of ocean biomass declines with climate change. Proc Natl Acad Sci USA 116:12907–12912. 10.1073/pnas.1900194116 DOI: 10.1073/pnas.1900194116
Lutterschmidt WI, Hutchison VH (1997) The critical thermal maximum: data to support the onset of spasms as the definitive end point. Can J Zool 75:1553–1560. 10.1139/z97-782 DOI: 10.1139/z97-782
Lymberakis P, Poulakakis N, Manthalou G et al (2007) Mitochondrial phylogeography of Rana (Pelophylax) populations in the Eastern Mediterranean region. Mol Phylogenet Evol 44:115–125. 10.1016/j.ympev.2007.03.009 DOI: 10.1016/j.ympev.2007.03.009
Mainka SA, Howard GW (2010) Climate change and invasive species: double jeopardy. Integr Zool 5:102–111. 10.1111/j.1749-4877.2010.00193.x DOI: 10.1111/j.1749-4877.2010.00193.x
McMenamin SK, Hadly EA, Wright CK (2008) Climatic change and wetland desiccation cause amphibian decline in Yellowstone National Park. Proc Natl Acad Sci USA 105:16988–16993. 10.1073/pnas.0809090105 DOI: 10.1073/pnas.0809090105
Mittan CS, Zamudio KR (2019) Rapid adaptation to cold in the invasive cane toad Rhinella marina. Conserv Physiol 7:1–12. 10.1093/conphys/coy075 DOI: 10.1093/conphys/coy075
Olyarnik SV, Bracken MES, Byrnes JE, Hughes AR, Hultgren KM, Stachowicz JJ (2009) Ecological factors affecting community invisibility. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 215–238 DOI: 10.1007/978-3-540-79236-9_12
Paaijmans KP, Heinig RL, Seliga RA et al (2013) Temperature variation makes ectotherms more sensitive to climate change. Glob Chang Biol 19:2373–2380. 10.1111/gcb.12240 DOI: 10.1111/gcb.12240
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42. 10.1038/nature01286 DOI: 10.1038/nature01286
Pille F, Pinto L, Denoël M (2021) Predation pressure of invasive marsh frogs: a threat to native amphibians? Diversity 13:595. 10.3390/D13110595 DOI: 10.3390/D13110595
Pinch FC, Claussen DL (2003) Effects of temperature and slope on the sprint speed and stamina of the eastern fence lizard, Sceloporus undulatus. J Herpetol 37:671–679. 10.1670/183-02 DOI: 10.1670/183-02
Pounds JA, Bustamante MR, Coloma LA et al (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161–167. 10.1038/nature04246 DOI: 10.1038/nature04246
R Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rahel FJ, Olden JD (2008) Assessing the effects of climate change on aquatic invasive species. Conserv Biol 22:521–533. 10.1111/j.1523-1739.2008.00950.x DOI: 10.1111/j.1523-1739.2008.00950.x
Rödder D, Ihlow F, Courant J et al (2017) Global realized niche divergence in the African clawed frog Xenopus laevis. Ecol Evol 7:4044–4058 DOI: 10.1002/ece3.3010
Ryan LM, Gunderson AR (2021) Competing native and invasive Anolis lizards exhibit thermal preference plasticity in opposite directions. J Exp Zool Part A Ecol Integr Physiol 335:118–125 DOI: 10.1002/jez.2420
Sakai AK, Allendorf FW, Holt JS et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332. 10.1146/annurev.ecolsys.32.081501.114037 DOI: 10.1146/annurev.ecolsys.32.081501.114037
Sánchez-Bayo F, Wyckhuys KAG (2019) Worldwide decline of the entomofauna: a review of its drivers. Biol Conserv 232:8–27. 10.1016/j.biocon.2019.01.020 DOI: 10.1016/j.biocon.2019.01.020
Sheridan JA, Caruso NM, Apodaca JJ, Rissler LJ (2018) Shifts in frog size and phenology: Testing predictions of climate change on a widespread anuran using data from prior to rapid climate warming. Ecol Evol 8:1316–1327. 10.1002/ece3.3636 DOI: 10.1002/ece3.3636
Simmons AJ, Berrisford P, Dee DP et al (2017) A reassessment of temperature variations and trends from global reanalyses and monthly surface climatological datasets. QJR Meteorol Soc 143:101–119. 10.1002/qj.2949 DOI: 10.1002/qj.2949
Sinclair BJ, Marshall KE, Sewell MA et al (2016) Can we predict ectotherm responses to climate change using thermal performance curves and body temperatures? Ecol Lett 19:1372–1385. 10.1111/ele.12686 DOI: 10.1111/ele.12686
Spellerberg IF (1972) Temperature tolerances of Southeast Australian reptiles examined in relation to reptile thermoregulatory behaviour and distribution. Oecologia 9:23–46. 10.1007/BF00345241 DOI: 10.1007/BF00345241
Stuart SN, Chanson JS, Cox NA et al (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786 DOI: 10.1126/science.1103538
Tattersall GJ, Sinclair BJ, Withers PC et al (2012) Coping with thermal challenges: physiological adaptations to environmental temperatures. Compr Physiol 2:2151–2202. 10.1002/cphy.c110055 DOI: 10.1002/cphy.c110055
Taylor EN, Diele-Viegas LM, Gangloff EJ et al (2021) The thermal ecology and physiology of reptiles and amphibians: a user’s guide. J Exp Zool Part A Ecol Integr Physiol 335:13–44. 10.1002/jez.2396 DOI: 10.1002/jez.2396
Tingley R, Vallinoto M, Sequeira F et al (2014) Realized niche shift during a global biological invasion. Proc Natl Acad Sci 111:10233–10238. 10.1073/pnas.1405766111 DOI: 10.1073/pnas.1405766111
van Damme R, Bauwens D, Verheyen RF (1991) The thermal dependence of feeding behaviour, food consumption and gut-passage time in the lizard Lacerta vivipara Jacquin. Funct Ecol 5:507–517. 10.2307/2389633 DOI: 10.2307/2389633
Vasseur DA, DeLong JP, Gilbert B et al (2014) Increased temperature variation poses a greater risk to species than climate warming. Proc R Soc B Biol Sci 281:20132612. 10.1098/rspb.2013.2612 DOI: 10.1098/rspb.2013.2612
Vickers MJ, Aubret F, Coulon A (2017) Using GAMM to examine inter-individual heterogeneity in thermal performance curves for Natrix natrix indicates bet hedging strategy by mothers. J Therm Biol 63:16–23. 10.1016/j.jtherbio.2016.11.003 DOI: 10.1016/j.jtherbio.2016.11.003
Vimercati G, Davies SJ, Measey J (2018) Rapid adaptive response to a Mediterranean environment reduces phenotypic mismatch in a recent amphibian invader. J Exp Biol 221:jeb174797. 10.1242/jeb.174797 DOI: 10.1242/jeb.174797
Wake DB, Vredenburg VT (2008) Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc Natl Acad Sci 105:11466–11473. 10.1073/pnas.0801921105 DOI: 10.1073/pnas.0801921105
Warren R, Price J, Graham E, Forstenhaeusler N, Van der Wal J (2018) The projected effect on insects, vertebrates, and plants of limiting global warming to 1.5°C rather than 2°C. Science 360:791–795. 10.1126/science.aar3646 DOI: 10.1126/science.aar3646
Wood SN (2006) Generalized additive models: an Introduction with R. Chapman & Hall/CRC, Boca Raton DOI: 10.1201/9781420010404
Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J R Stat Soc Ser B 73:3–36. 10.1111/j.1467-9868.2010.00749.x DOI: 10.1111/j.1467-9868.2010.00749.x
Young A, Anderson RO, Naimo A et al (2022) How do the physiological traits of a lizard change during its invasion of an oceanic island? Oecologia 198:567–578 DOI: 10.1007/s00442-021-05054-y
Zerebecki RA, Sorte CJB (2011) Temperature tolerance and stress proteins as mechanisms of invasive species success. PLoS One 6:e14806. 10.1371/journal.pone.0014806 DOI: 10.1371/journal.pone.0014806
Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York DOI: 10.1007/978-0-387-87458-6
