Amphibian; Dispersal syndrome; Global warming; Habitat fragmentation; Microclimate; Geography, Planning and Development; Ecology; Nature and Landscape Conservation
Abstract :
[en] Context: Climate change and habitat fragmentation exert considerable pressures on biodiversity. The spatial distribution of microclimatic refuges in the landscape can influence species responses to warming climates. Objectives: Using a semi-natural experiment, we investigated the potential synergetic effects of climate warming and habitat connectivity on a single amphibian species. Methods: We monitored populations of the palmate newt, Lissotriton helveticus, under two climate treatments, a warmer climate (+ ~ 2 °C) or a present-day climate, in mesocosms either isolated or connected to the other climatic conditions. We assessed the abundance and phenotype (snout-vent length, body condition and skin coloration: darkness and redness) of juvenile and adult newts, and the dispersal propensity of juveniles. Results: Over the 4 years of climatic manipulation, populations tended to increase more in the present-day than in the warmer climate. Warmer climates decreased the abundance of adult newts and altered the phenotypic composition of populations with darker and less red newts. However, connectivity between the two climates cancelled out the effect of a warmer climate on abundance and reversed the effects on phenotype composition. We further found that juvenile newts from the present-day climate treatment tended to emigrate more from warmer conditions during our laboratory dispersal assay and that population isolation disrupted a common covariation between emigration propensity and body size, leg length and skin darkness. Conclusions: Our results point to a synergetic effect of climate warming and fragmentation on the demography of newt populations and emigration decisions of juveniles, suggesting that microclimate refuges and their accessibility play a key role in buffering the impacts of climate warming, with potential implications for amphibian diversity at a regional scale.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Winandy, Laurane ; Université de Liège - ULiège > Freshwater and OCeanic science Unit of reSearch (FOCUS) ; Laboratoire Évolution and Diversité Biologique (EDB), UMR5174, CNRS, IRD, Université Toulouse III Paul Sabatier, Toulouse, France
Pellerin, Félix ; Laboratoire Évolution and Diversité Biologique (EDB), UMR5174, CNRS, IRD, Université Toulouse III Paul Sabatier, Toulouse, France
Di Gesu, Lucie; Laboratoire Évolution and Diversité Biologique (EDB), UMR5174, CNRS, IRD, Université Toulouse III Paul Sabatier, Toulouse, France
Legrand, Delphine; Station d’Écologie Théorique et Expérimentale (SETE), UAR2029, CNRS, Moulis, France
Cote, Julien ; Laboratoire Évolution and Diversité Biologique (EDB), UMR5174, CNRS, IRD, Université Toulouse III Paul Sabatier, Toulouse, France
Language :
English
Title :
Influence of landscape connectivity on newt’s response to a warmer climate
EU - European Union Labex TULIP - Laboratoire d'Excellence TULIP ANR - Agence Nationale de la Recherche Fondation Fyssen F.R.S.-FNRS - Fonds de la Recherche Scientifique
Funding text :
This work was supported by funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (Grant Agreement No. 817779 to JC), by the French Laboratory of Excellence project ‘TULIP’ (Grant Nos. ANR-10-LABX-41 and ANR-11-IDEX-0002-02) and by an ‘Investissements d’avenir’ program from the Agence Nationale de la Recherche (grant no. ANR-11-INBS-0001AnaEE-Services). LW was supported by the Fyssen Foundation Post-Doctoral Fellowship and is currently a postdoctoral researcher at the Fonds de la recherche scientifique (F.R.S.-FNRS).
Balogová M, Gvoždík L (2015) Can newts cope with the heat? Disparate thermoregulatory strategies of two sympatric species in water. PLoS ONE 10(5):e0128155 DOI: 10.1371/journal.pone.0128155
Bates D, Mächler M, Bolker B, Walker S (2008) Fitting mixed-effects models using the lme4 package in R. In: International Meeting of the Psychometric Society
Bestion E, Clobert J, Cote J (2015a) Dispersal response to climate change: scaling down to intraspecific variation. Ecol Lett 18:1226–1233 DOI: 10.1111/ele.12502
Bestion E, Teyssier A, Richard M et al (2015b) Live fast, die young: experimental evidence of population extinction risk due to climate change. PLoS Biol 13:e1002281 DOI: 10.1371/journal.pbio.1002281
Blaustein AR, Walls SC, Bancroft BA et al (2010) Direct and indirect effects of climate change on amphibian populations. Diversity 2:281–313 DOI: 10.3390/d2020281
Burraco P, Orizaola G, Monaghan P, Metcalfe NB (2020) Climate change and ageing in ectotherms. Glob Change Biol 26:5371–5381 DOI: 10.1111/gcb.15305
Cayuela H, Arsovski D, Bonnaire E et al (2016) The impact of severe drought on survival, fecundity, and population persistence in an endangered amphibian. Ecosphere 7:e01246 DOI: 10.1002/ecs2.1246
Cayuela H, Grolet O, Joly P (2018) Context-dependent dispersal, public information, and heterospecific attraction in newts. Oecologia 188:1069–1080 DOI: 10.1007/s00442-018-4267-3
Chukwuka CO, Mello RS, Cree A, Monks JM (2021) Thermal heterogeneity of selected retreats in cool-temperate viviparous lizards suggests a potential benefit of future climate warming. J Therm Biol 97:102869 DOI: 10.1016/j.jtherbio.2021.102869
Clobert J, Le Galliard J-F, Cote J et al (2009) Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol Lett 12:197–209 DOI: 10.1111/j.1461-0248.2008.01267.x
Cote J, Bestion E, Jacob S, Travis J, Legrand D, Baguette M (2017) Evolution of dispersal strategies and dispersal syndromes in fragmented landscapes. Ecography 40:56–73 DOI: 10.1111/ecog.02538
Cote J, Dahirel M, Altermatt F et al (2022) Dispersal syndromes in challenging environments: a cross-species experiment. Ecol Lett 25:2675–2687 DOI: 10.1111/ele.14124
Denoël M (2006) Seasonal variation of morph ratio in facultatively paedomorphic populations of the palmate newt Triturus helveticus. Acta Oecologica 29:165–170 DOI: 10.1016/j.actao.2005.09.003
Denoël M, Dalleur S, Langrand E et al (2018) Dispersal and alternative breeding site fidelity strategies in an amphibian. Ecography 41:1543–1555 DOI: 10.1111/ecog.03296
Díaz SM, Settele J, Brondízio E et al (2019) The global assessment report on biodiversity and ecosystem services: summary for policy makers
Enriquez-Urzelai U, Bernardo N, Moreno-Rueda G et al (2019) Are amphibians tracking their climatic niches in response to climate warming? A test with Iberian amphibians. Clim Change 154:289–301 DOI: 10.1007/s10584-019-02422-9
Fan XL, Lin ZH, Scheffers BR (2021) Physiological, developmental, and behavioral plasticity in response to thermal acclimation. J Therm Biol 97:102866 DOI: 10.1016/j.jtherbio.2021.102866
Frey SJ, Hadley AS, Johnson SL et al (2016) Spatial models reveal the microclimatic buffering capacity of old-growth forests. Sci Adv 2:e1501392 DOI: 10.1126/sciadv.1501392
Fronhofer EA, Legrand D, Altermatt F et al (2018) Bottom-up and top-down control of dispersal across major organismal groups. Nat Ecol Evol 2:1859–1863 DOI: 10.1038/s41559-018-0686-0
Garcia TS, Stacy J, Sih A (2004) Larval salamander response to UV radiation and predation risk: color change and microhabitat use. Ecol Appl 14:1055–1064 DOI: 10.1890/02-5288
Gunderson AR, Stillman JH (2015) Plasticity in thermal tolerance has limited potential to buffer ectotherms from global warming. Proc R Soc B 282:20150401 DOI: 10.1098/rspb.2015.0401
Gvoždík L (2015) Mismatch between ectotherm thermal preferenda and optima for swimming: a test of the evolutionary pace hypothesis. Evol Biol 42:137–145 DOI: 10.1007/s11692-015-9305-z
Gvoždík L (2022) Thermoregulatory opportunity and competition act independently on life‐history traits in aquatic ectotherms. Funct Ecol 36:2520–2530
Gvoždík L, Puky M, Šugerková M (2007) Acclimation is beneficial at extreme test temperatures in the Danube crested newt, Triturus dobrogicus (Caudata, Salamandridae). Biol J Linn Soc 90:627–636 DOI: 10.1111/j.1095-8312.2006.00752.x
Huey RB, Kearney MR, Krockenberger A et al (2012) Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philos Trans R Soc B 367:1665–1679 DOI: 10.1098/rstb.2012.0005
Joly P, Miaud C (1989) Fidelity to the breeding site in the alpine newt Triturus alpestris. Behav Proc 19:47–56 DOI: 10.1016/0376-6357(89)90030-2
Kristín P, Gvoždík L (2014) Aquatic-to-terrestrial habitat shift reduces energy expenditure in newts. J Exp Zool A 321:183–188 DOI: 10.1002/jez.1849
Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18 DOI: 10.18637/jss.v025.i01
Legrand D, Guillaume O, Baguette M et al (2012) The Metatron: an experimental system to study dispersal and metaecosystems for terrestrial organisms. Nat Methods 9:828–833 DOI: 10.1038/nmeth.2104
Legrand D, Trochet A, Moulherat S et al (2015) Ranking the ecological causes of dispersal in a butterfly. Ecography 38:822–831 DOI: 10.1111/ecog.01283
Lenoir J, Svenning J-C (2015) Climate-related range shifts–a global multidimensional synthesis and new research directions. Ecography 38:15–28 DOI: 10.1111/ecog.00967
Li Y, Cohen JM, Rohr JR (2013) Review and synthesis of the effects of climate change on amphibians. Integr Zool 8:145–161 DOI: 10.1111/1749-4877.12001
Lüdecke D, Lüdecke MD (2019) Package ‘sjstats.’ Statistical functions for Regression Models, Version 0.17, 3
Lüdecke D, Ben-Shachar MS, Patil I et al (2021) performance: an R package for assessment, comparison and testing of statistical models. J Open Source Softw 6:3139 DOI: 10.21105/joss.03139
Mafli A, Wakamatsu K, Roulin A (2011) Melanin-based coloration predicts aggressiveness and boldness in captive eastern Hermann’s tortoises. Anim Behav 81:859–863 DOI: 10.1016/j.anbehav.2011.01.025
Masson-Delmotte V, Zhai P, Pirani A, Connors SL, Péan C, Berger S et al (2021) Climate change 2021: the physical science basis. Contribution of working group I to the sixth assessment report of the intergovernmental panel on climate change, 2
McGaughran A, Laver R, Fraser C (2021) Evolutionary responses to warming. Trends Ecol Evol 36:591–600 DOI: 10.1016/j.tree.2021.02.014
Merilä J, Hendry AP (2014) Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evol Appl 7:1–14 DOI: 10.1111/eva.12137
Milling CR, Rachlow JL, Olsoy PJ et al (2018) Habitat structure modifies microclimate: an approach for mapping fine-scale thermal refuge. Methods Ecol Evol 9:1648–1657 DOI: 10.1111/2041-210X.13008
Mochida K, Kitada M, Ikeda K et al (2013) Spatial and temporal instability of local biotic community mediate a form of aposematic defense in newts, consisting of carotenoid-based coloration and tetrodotoxin. J Chem Ecol 39:1186–1192 DOI: 10.1007/s10886-013-0342-8
Nilsson Sköld H, Aspengren S, Wallin M (2013) Rapid color change in fish and amphibians–function, regulation, and emerging applications. Pigment Cell Melanoma Res 26:29–38 DOI: 10.1111/pcmr.12040
Ogilvy V, Preziosi RF (2012) Can carotenoids mediate the potentially harmful effects of ultraviolet light in Silurana (Xenopus) tropicalis larvae? J Anim Physiol Anim Nutr 96:693–699 DOI: 10.1111/j.1439-0396.2011.01197.x
Ogilvy V, Preziosi RF, Fidgett AL (2012) A brighter future for frogs? The influence of carotenoids on the health, development and reproductive success of the red-eye tree frog. Anim Conserv 15:480–488 DOI: 10.1111/j.1469-1795.2012.00536.x
Opdam P, Wascher D (2004) Climate change meets habitat fragmentation: linking landscape and biogeographical scale levels in research and conservation. Biol Conserv 117:285–297 DOI: 10.1016/j.biocon.2003.12.008
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42 DOI: 10.1038/nature01286
Pellerin F, Cote J, Bestion E, Aguilée R (2019) Matching habitat choice promotes species persistence under climate change. Oikos 128:221–234 DOI: 10.1111/oik.05309
Pellerin F, Bestion E, Winandy L et al (2022) Connectivity among thermal habitats buffers the effects of warm climate on life-history traits and population dynamics. J Anim Ecol 91:2301–2313 DOI: 10.1111/1365-2656.13814
Pittman SE, Osbourn MS, Semlitsch RD (2014) Movement ecology of amphibians: a missing component for understanding population declines. Biol Conserv 169:44–53 DOI: 10.1016/j.biocon.2013.10.020
Reading CJ (2007) Linking global warming to amphibian declines through its effects on female body condition and survivorship. Oecologia 151:125–131 DOI: 10.1007/s00442-006-0558-1
Román-Palacios C, Wiens JJ (2020) Recent responses to climate change reveal the drivers of species extinction and survival. Proc Natl Acad Sci 117:4211–4217 DOI: 10.1073/pnas.1913007117
Roulin A (2014) Melanin-based colour polymorphism responding to climate change. Glob Change Biol 20:3344–3350 DOI: 10.1111/gcb.12594
Saino N, Romano M, Scandolara C et al (2014) Brownish, small and lousy barn swallows have greater natal dispersal propensity. Anim Behav 87:137–146 DOI: 10.1016/j.anbehav.2013.10.022
Scalercio S, Russo M, Dapporto L (2009) Wetlands are refuge areas that delay global warming-induced range shift of Lepidoptera. In: Handbook of nature conservation: global, environmental and economic issues. Nova Publishers, New York, pp 393–406
Scheffers BR, Phillips BL, Laurance WF et al (2013) Increasing arboreality with altitude: a novel biogeographic dimension. Proc R Soc B 280:20131581 DOI: 10.1098/rspb.2013.1581
Seebacher F, Beaman J, Little AG (2014) Regulation of thermal acclimation varies between generations of the short-lived mosquitofish that developed in different environmental conditions. Funct Ecol 28:137–148 DOI: 10.1111/1365-2435.12156
Sillero N (2021) Climate change in action: local elevational shifts on Iberian amphibians and reptiles. Reg Environ Change 21:1–13 DOI: 10.1007/s10113-021-01831-w
Suggitt AJ, Wilson RJ, Isaac NJ et al (2018) Extinction risk from climate change is reduced by microclimatic buffering. Nat Clim Chang 8:713–717 DOI: 10.1038/s41558-018-0231-9
Thompson RM, Beardall J, Beringer J et al (2013) Means and extremes: building variability into community-level climate change experiments. Ecol Lett 16:799–806 DOI: 10.1111/ele.12095
Tryjanowski P, Sparks T, Rybacki M, Berger L (2006) Is body size of the water frog Rana esculenta complex responding to climate change? Naturwissenschaften 93:110–113 DOI: 10.1007/s00114-006-0085-2
Urban MC (2015) Accelerating extinction risk from climate change. Science 348:571–573 DOI: 10.1126/science.aaa4984
Urban MC, Richardson JL, Freidenfelds NA (2014) Plasticity and genetic adaptation mediate amphibian and reptile responses to climate change. Evol Appl 7:88–103 DOI: 10.1111/eva.12114
Verell PA (1987) The directionality of migrations of amphibians to and from a pond in southern England, with particular reference to the smooth newt, Triturus vulgaris. Amphib-Reptil 8:93–100 DOI: 10.1163/156853887X00360
Weinbach A, Cayuela H, Grolet O et al (2018) Resilience to climate variation in a spatially structured amphibian population. Sci Rep 8:1–9 DOI: 10.1038/s41598-018-33111-9
Winandy L, Cote J, Di Gesu L et al (2019) Local predation risk and matrix permeability interact to shape movement strategy. Oikos 128:1402–1412 DOI: 10.1111/oik.06403
Winterová B, Gvoždík L (2021) Individual variation in seasonal acclimation by sympatric amphibians: a climate change perspective. Funct Ecol 35:117–126