High interannual variability of a climate-driven amphibian community in a seasonal rainforest

  • Nicolas DubosEmail author
  • Loïs Morel
  • Angelica Crottini
  • Karen Freeman
  • Jean Honoré
  • Honoré Lava
  • Jean Noël
  • Ingrid Porton
  • Georges Rendrirendry
  • Gonçalo M. Rosa
  • Franco Andreone
Original Paper


Seasonality exerts strong pressures on biodiversity patterns. Yet, temporal beta-diversity is poorly studied in tropical systems, and the drivers of variability in amphibian activity and seasonality remain largely unknown. We quantified intra- and interannual variation in temporal beta-diversity relying on a nine-year, year-round survey (51 species, n > 23,000) performed in a protected area (Betampona, Madagascar). We assessed the dependence on climate of beta-diversity and abundance using a distance-based redundancy analysis and generalised linear mixed models, respectively. Despite the majority of species being preferentially active during one specific period, beta-diversity and abundance were more variable between years than within years. Temporal variation in beta-diversity was best explained by temperature (but climate accounted for only 2% of variation). Species abundance was best explained by temperature (for 32% of the tested species), monthly humidity (30%) and monthly rainfall (24%). We found no climatic dependence for 24% of the species. Our results suggest that studies focusing on species phenology can be misleading when based on single-year surveys even in seasonal systems. The high interannual variability in diversity may be due to an adaptive responses to an important regime of stochastic events. Given the direction of the relationships between weather and abundances, we predict that a large proportion of amphibians would suffer from climate change in Madagascar. We emphasise the need to account for multiple temporal scales in studies of tropical species composition and abundance to better understand species phenology and their response to climate change, and make targeted conservation actions more effective.


Madagascar Phenology Rainforest anurans Reserve Naturelle Intégrale de Betampona Temporal beta-diversity Weather 



We are thankful to the Madagascar Fauna and Flora Group for allowing us to use the data and to Cel and Honoré Alex, who participated in the data collection. Our thanks also to Juliana Rasoma, MFG, for help verifying the meteorological data. We thank Boris Leroy for his continued help. The field survey was carried out with the collaboration of Departement de Biologie Animale (University of Antananarivo), Parc Botanique et Zoologique de Tsimbazaza (Antananarivo) and the Madagascar Fauna and Flora Group. Finally, we wish to thank A. Bollen, A. Katz, G. Kett and C. Welch for their continuous encouragement and support; the porters in the field, the cooks, our driver and all the people from Rendrirendry for their unconditional help, without whom this project would not have been possible. This research project was partially financially supported by Saint Louis Zoo’s Wildcare Institute, Museo Regionale di Scienze Naturali, and Gondwana Conservation and Research. The work of AC is supported by the Portuguese National Funds through FCT—Foundation for Science and Technology—under the IF/00209/2014/CP1256/CT0011 Exploratory Research Project and the Investigador FCT (IF) Grant (IF/00209/2014).

Supplementary material

10531_2019_1916_MOESM1_ESM.docx (2.7 mb)
Electronic supplementary material 1 (FILE 2801 kb)
10531_2019_1916_MOESM2_ESM.docx (1 mb)
Electronic supplementary material 2 (DOCX 1055 kb)


  1. Allnutt TF, Ferrier S, Manion G et al (2008) A method for quantifying biodiversity loss and its application to a 50-year record of deforestation across Madagascar. Conserv Lett 1:173–181. CrossRefGoogle Scholar
  2. Andreone F (1994) The amphibians of Ranomafana rain forest, Madagascar—preliminary community analysis and conservation considerations. Oryx 28:207–214. CrossRefGoogle Scholar
  3. Andreone F (1996) Seasonal variations of the amphibian communities in two rainforests of Madagascar. Biogéographie de Madagascar 1996:397–402Google Scholar
  4. Andreone F, Randriamahazo H (2008) Sahonagasy Action Plan. Conservation Programs for the Amphibians of Madagascar. Museo Regionale di Scienze Naturali, Conservation International, IUCN/Amphibian Specialist Group, BogotàGoogle Scholar
  5. Andreone F, Vences M, Guarino FM et al (2002) Natural history and larval morphology of Boophis occidentalis (Anura: Mantellidae: Boophinae) provide new insights into the phylogeny and adaptive radiation of endemic Malagasy frogs. J Zool 257:425–438. CrossRefGoogle Scholar
  6. Andreone F, Rosa GM, Noël J et al (2010) Living within fallen palm leaves: the discovery of an unknown Blommersia (Mantellidae: Anura) reveals a new reproductive strategy in the amphibians of Madagascar. Naturwissenschaften 97:525–543. CrossRefPubMedGoogle Scholar
  7. Andreone F, Dawson J, Rabemananjara F et al (2016) New Sahonagasy action plan 2016–2020. Amphibian Specialist Group, TorinoGoogle Scholar
  8. Barton K (2018) MuMIn: multi-model inference. R package.
  9. Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Glob Ecol Biogeogr 19:134–143. CrossRefGoogle Scholar
  10. Baselga A, Orme DL (2012) Betapart: an R package for the study of beta diversity. Methods Ecol Evol 3:808–812. CrossRefGoogle Scholar
  11. Baselga A, Bonthoux S, Balent G (2015) Temporal beta biversity of bird assemblages in agricultural landscapes: land cover change vs. stochastic processes. PLoS ONE. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–51. CrossRefGoogle Scholar
  13. Bellard C, Bertelsmeier C, Leadley P et al (2012) Impacts of climate change on the future of biodiversity. Ecol Lett 15:365–377. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Bellati A, Scherz MD, Megson S et al (2018) Resurrection and re-description of Plethodontohyla laevis (Boettger, 1913) and transfer of Rhombophryne alluaudi (Mocquard, 1901) to the genus Plethodontohyla (Amphibia, Microhylidae, Cophylinae). Zoosystematics Evol 94:109–135. CrossRefGoogle Scholar
  15. Benard MF (2015) Warmer winters reduce frog fecundity and shift breeding phenology, which consequently alters larval development and metamorphic timing. Glob Change Biol 21:1058–1065. CrossRefGoogle Scholar
  16. Bernal-bautista MH, Turriago-gonzález JL, Villa-navarro FA (2017) Impact of daily variable temperatures in life-history traits of tropical anurans. Rev Biol Trop 65:55–63CrossRefGoogle Scholar
  17. Bertoluci J, Rodrigues MT (2002) Seasonal patterns of breeding activity of Atlantic Rainforest anurans at Boracéia, Southeastern Brazil. Amphibia-Reptilia 23:161–167. CrossRefGoogle Scholar
  18. Bevier CR (1997) Breeding activity and chorus tenure of two neotropical hylid frogs. Herpetologica 53:297–311Google Scholar
  19. Bletz MC, Rosa GM, Andreone F et al (2015) Widespread presence of the pathogenic fungus Batrachochytrium dendrobatidis in wild amphibian communities in Madagascar. Sci Rep 5:1–10. CrossRefGoogle Scholar
  20. Brown JL, Sillero N, Glaw F et al (2016) Spatial biodiversity patterns of madagascar’ s amphibians and reptiles. PLoS ONE 11:1–26. CrossRefGoogle Scholar
  21. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer S, New YorkGoogle Scholar
  22. Canale C, Henry P (2010) Adaptive phenotypic plasticity and resilience of vertebrates to increasing climatic unpredictability. Clim Res 43:135–147. CrossRefGoogle Scholar
  23. Carey C, Alexander MA (2003) Climate change and amphibian declines: is there a link? Divers Distrib 9:111–121. CrossRefGoogle Scholar
  24. Crump M (1974) Reproductive strategies in a tropical anuran community. Misc Publ Kansas Univ 61:1–68. CrossRefGoogle Scholar
  25. da Vasconcelos TS, dos Santos TG, de Rossa-Feres D, Haddad CFB (2011) Spatial and temporal distribution of tadpole assemblages (Amphibia, Anura) in a seasonal dry tropical forest of southeastern Brazil. Hydrobiologia 673:93–104. CrossRefGoogle Scholar
  26. Daszak P, Scott DE, Kilpatrick AM et al (2005) Amphibian population declines at Savannah River Site are linked to climate, not chytridiomycosis. Ecology 86:3232–3237CrossRefGoogle Scholar
  27. dos Santos TG, da Vasconcelos TS, de Rossa-Feres DC, Haddad CFB (2009) Anurans of a seasonally dry tropical forest: Morro do Diabo State Park, São Paulo state, Brazil. J Nat Hist 43:973–993. CrossRefGoogle Scholar
  28. Dubos N (2013) New locality record for Phelsuma grandis (Sauria: Gekkonidae) in Reunion, in sympatry with the critically endangered Phelsuma inexpectata. Herpetol Notes 6:309–311Google Scholar
  29. Dubos N, Piludu N, Andriantsimanarilafy RR et al (2014) New findings of Phelsuma grandis and P. laticauda (Sauria: Gekkonidae) at the southern edge of the range of the endangered Phelsuma serraticauda in eastern Madagascar. Herpetol Notes 7:21–23Google Scholar
  30. Duellman WE (1995) Temporal fluctuations in abundances of anuran amphibians in a seasonal Amazonian rainforest. J Herpetol 29:13–21CrossRefGoogle Scholar
  31. Duellman WE, Trueb L (1994) Biology of Amphibians. The Johns Hopkins University Press, LondonGoogle Scholar
  32. Frederiksen M, Daunt F, Harris MP, Wanless S (2008) The demographic impact of extreme events: stochastic weather drives survival and population dynamics in a long-lived seabird. J Anim Ecol 78:1020–1029. CrossRefGoogle Scholar
  33. Gardner T, Fitzherbert E, Drewes R, Howell K (2007) Spatial and temporal patterns of abundance and diversity of an East African leaf litter amphibian fauna. Biotropica 39:105–113CrossRefGoogle Scholar
  34. Ghulam A (2014) Monitoring tropical forest degradation in Betampona Nature Reserve, Madagascar using multisource remote sensing data fusion. IEEE J Sel Top Appl Earth Obs Remote Sens 7:4960–4971. CrossRefGoogle Scholar
  35. Glaw F, Vences M (1996) Bemerkungen zur fortpflanzung des waldskinks Amphiglossus melanopleura aus Madagaskar (Sauria: Scincidae), mit einer übersicht über die fortpflanzungsperioden madagassischer reptilien. Salamandra 32:211–216Google Scholar
  36. Glaw F, Vences M (2007) A field guide to the amphibians and reptiles of Madagascar, 3rd edn. Vences & Glaw Verlags, KölnGoogle Scholar
  37. Glos J (2003) The amphibian fauna of the Kirindy dry forest in western Madagascar. Salamandra 39:75–90Google Scholar
  38. Gómez-Rodríguez C, Díaz-Paniagua C, Bustamante J et al (2010) Inter-annual variability in amphibian assemblages: implications for diversity assessment and conservation. Aquat Conserv Mar Freshw Ecosyst 20:668–677. CrossRefGoogle Scholar
  39. Goodman SM, Raselimanana AP, Andriniaina HA et al (2017) The distribution and ecology of invasive alien vertebrate species in the greater Toamasina region, central eastern Madagascar. Malagasy Nat 12:95–109Google Scholar
  40. Gottsberger B, Gruber E (2004) Temporal partitioning of reproductive activity in a neotropical anuran community. J Trop Ecol 20:271–280. CrossRefGoogle Scholar
  41. Grant RA, Chadwick EA, Halliday T (2009) The lunar cycle: a cue for amphibian reproductive phenology? Anim Behav 78:349–357. CrossRefGoogle Scholar
  42. Green GM, Sussman RW (1990) Deforestation history of the eastern rain forests of Madagascar from satellite images. Science 80-(248):212–215. CrossRefGoogle Scholar
  43. Gross J (2019) AmphibiaWeb. Accessed 15 Feb 2019
  44. Grueber CE, Nakagawa S, Laws RJ, Jamieson IG (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711. CrossRefPubMedGoogle Scholar
  45. Harper GJ, Steininger MK, Tucker CJ et al (2007) Fifty years of deforestation and forest fragmentation in Madagascar. Environ Conserv 34:325–333. CrossRefGoogle Scholar
  46. Heinermann J, Rodríguez A, Segev O et al (2015) Year-round activity patterns in a hyperdiverse community of rainforest amphibians in Madagascar. J Nat Hist 49:2213–2231. CrossRefGoogle Scholar
  47. Hero J-M, Gascon C, Magnusson WE (1998) Direct and indirect effects of predation on tadpole community structure in the Amazon rainforest. Austral Ecol 23:474–482. CrossRefGoogle Scholar
  48. Ho C-H, Kim J-H, Jeong J-H et al (2006) Variation of tropical cyclone activity in the South Indian Ocean: El Niño-Southern Oscillation and Madden-Julian Oscillation effects. J Geophys Res 111:D22101. CrossRefGoogle Scholar
  49. Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108. CrossRefPubMedGoogle Scholar
  50. Köhler J, Jansen M, Rodríguez A et al (2017) The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice. Zootaxa 4251:1–124CrossRefGoogle Scholar
  51. Kupfer A, Nabhitabhata J, Himstedt W (2005) Life history of amphibians in the seasonal tropics: habitat, community and population ecology of a caecilian (genus Ichthyophis). J Zool 266:237–247. CrossRefGoogle Scholar
  52. Leprieur F, Oikonomou A (2013) The need for richness- independent measures of turnover when delineating biogeographical regions. J Biogeogr 41:417–420. CrossRefGoogle Scholar
  53. Licata F, Ficetola GF, Freeman K et al (2019) Abundance, distribution and spread of the invasive Asian toad Duttaphrynus melanostictus in eastern Madagascar. Biol Invasions 21:1615–1626. CrossRefGoogle Scholar
  54. Lopez JA, Scarabotti PA, Ghirardi R (2011) Seasonal patterns of abundance and recruitment in an amphibian assemblage from the Parana River floodplain. Interciencia 36:538–544Google Scholar
  55. Marques O, Eterovic A, Endo W (2001) Seasonal activity of snakes in the Atlantic forest in southeastern Brazil. Amphib Reptil 22:103–111. CrossRefGoogle Scholar
  56. McClelland P, Reardon JT, Kraus F et al (2015) Toad eradication feasibility report for Madagascar. Te Anau, New ZealandGoogle Scholar
  57. McConnell W, Viña A, Kull C, Batko C (2015) Forest transition in Madagascar’s highlands: initial evidence and implications. Land 4:1155–1181. CrossRefGoogle Scholar
  58. Moussus J, Jiguet F, Clavel J, Julliard R (2009) A method to estimate phenological variation using data from large scale abundance monitoring programmes. Bird Study 56:198–212. CrossRefGoogle Scholar
  59. Oksanen AJ, Blanchet FG, Kindt R, et al (2015) Community Ecology Package ‘vegan’. R version 2.3-1.
  60. Pearson RG (2015) Asian common toads in Madagascar: an urgent effort to inform surveys and eradication efforts. Glob Change Biol 21:9. CrossRefGoogle Scholar
  61. Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci Discuss 4:439–473. CrossRefGoogle Scholar
  62. Piludu N, Dubos N, Razafimanahaka JH et al (2015) Distribution, threats and conservation of a critically endangered amphibian (Mantella aurantiaca) in eastern Madagascar. Herpetol Notes 8:119–123Google Scholar
  63. Prado C, Uetanabaro M, Haddad C (2005) Breeding activity patterns, reproductive modes, and habitat use by anurans (Amphibia) in a seasonal environment in the Pantanal, Brazil. Amphib Reptil 26:211–221. CrossRefGoogle Scholar
  64. R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical ComputingGoogle Scholar
  65. Riemann JC, Ndriantsoa SH, Rödel MO, Glos J (2017) Functional diversity in a fragmented landscape—Habitat alterations affect functional trait composition of frog assemblages in Madagascar. Glob Ecol Conserv 10:173–183. CrossRefGoogle Scholar
  66. Rosa GM, Noël J, Andreone F (2011) Confirming a new population of the endangered Paroedura masobe (Squamata: Gekkonidae) in the relict Betampona low elevation rainforest, eastern Madagascar. Herpetol Notes 4:405–407Google Scholar
  67. Rosa GM, Andreone F, Crottini A et al (2012) The amphibians of the relict Betampona low-elevation rainforest, eastern Madagascar: an application of the integrative taxonomy approach to biodiversity assessments. Biodivers Conserv 21:1531–1559. CrossRefGoogle Scholar
  68. Rosa GM, Crottini A, Noël J et al (2014) A new phytotelmic species of Platypelis (Microhylidae: Cophylinae) from the Betampona Reserve, eastern Madagascar. Salamandra 50:201–214Google Scholar
  69. Saenz D, Fitzgerald LA, Baum KA (2006) Abiotic correlates of anuran calling phenology: the importance of rain, temperature, and season. Herpetol Monogr 20:64.;2 CrossRefGoogle Scholar
  70. Schalk CM, Saenz D (2016) Environmental drivers of anuran calling phenology in a seasonal neotropical ecosystem. Austral Ecol 41:16–27. CrossRefGoogle Scholar
  71. Segev O, Andreone F, Pala R et al (2012) Reproductive phenology of the Dyscophus antongili, in an urban pond of Madagascar’ s east coast. Acta Herp 7(2):331–340Google Scholar
  72. Shoemaker VH (1992) Exchange of water, ions, and respiratory gases in terrestrial amphibians. In: Feder ME, Burggren WW (eds) Environmental physiology of the amphibians. University of Chicago Press, Chicago, pp 125–150Google Scholar
  73. Socolar JB, Gilroy JJ, Kunin WE, Edwards DP (2016) How should beta-diversity inform biodiversity conservation? Trends Ecol Evol 31:67–80. CrossRefPubMedGoogle Scholar
  74. Sparks T, Carey P (1995) The responses of species to climate over two centuries: an analysis of the Marsham phenological record, 1736–1947. J Ecol 83:321–329CrossRefGoogle Scholar
  75. Strauß A, Guilhaumon F, Randrianiaina RD et al (2016) Opposing patterns of seasonal change in functional and phylogenetic diversity of tadpole assemblages. PLoS ONE 11:e0151744. CrossRefPubMedPubMedCentralGoogle Scholar
  76. Thurman LL, Garcia TS (2017) Differential plasticity in response to simulated climate warming in a high-elevation amphibian assemblage. J Herpetol 51:232–239. CrossRefGoogle Scholar
  77. Tökölyi J, McNamara JM, Houston AI, Barta Z (2012) Timing of avian reproduction in unpredictable environments. Evol Ecol 26:25–42. CrossRefGoogle Scholar
  78. Tonkin JD, Bogan MT, Bonada N et al (2017) Seasonality and predictability shape temporal species diversity. Ecology 98:1201–1216. CrossRefPubMedGoogle Scholar
  79. Vallan D (2000) Influence of forest fragmentation on amphibian diversity in the nature reserve of Ambohitantely, highland Madagascar. Biol Conserv 96:31–43. CrossRefGoogle Scholar
  80. van de Pol M, Cockburn A (2011) Identifying the critical climatic time window that affects trait expression. Am Nat 177:698–707. CrossRefPubMedGoogle Scholar
  81. Vieilledent G, Grinand C, Rakotomalala FA et al (2018) Combining global tree cover loss data with historical national forest cover maps to look at six decades of deforestation and forest fragmentation in Madagascar. Biol Conserv 222:189–197. CrossRefGoogle Scholar
  82. Vieites DR, Wollenberg KC, Andreone F et al (2009) Vast underestimation of Madagascar’s biodiversity evidenced by an integrative amphibian inventory. Proc Natl Acad Sci USA 106:8267–8272. CrossRefPubMedGoogle Scholar
  83. Vignoli L, D’Amen M, Della Rocca F et al (2014) Contrasted influences of moon phases on the reproduction and movement patterns of four amphibian species inhabiting different habitats in central Italy. Amphib Reptil 35:247–254CrossRefGoogle Scholar
  84. Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc Biol Sci 272:2561–2569. CrossRefPubMedPubMedCentralGoogle Scholar
  85. Wells KD (1977) The social behaviour of anuran amphibians. Anim Behav 25:666–693. CrossRefGoogle Scholar
  86. Wells KD (2010) The ecology and behavior of amphibians. University of Chicago Press, Chicago and LondonGoogle Scholar
  87. Whiteman HH, Wissinger SA (2005) Amphibian population cycles and long-term data sets. Amphibian Declines: The Conservation Status of United States Species, University of Chicago Press, Chicago p. 177–184Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Nicolas Dubos
    • 1
    • 2
    Email author
  • Loïs Morel
    • 3
  • Angelica Crottini
    • 4
  • Karen Freeman
    • 5
  • Jean Honoré
    • 5
  • Honoré Lava
    • 5
  • Jean Noël
    • 5
  • Ingrid Porton
    • 5
  • Georges Rendrirendry
    • 5
  • Gonçalo M. Rosa
    • 6
    • 7
  • Franco Andreone
    • 2
  1. 1.Centre d’Ecologie et des Sciences de la Conservation (CESCO UMR 7204), Sorbonne Universités, MNHN, CNRSParisFrance
  2. 2.Museo Regionale di Scienze NaturaliTurinItaly
  3. 3.Géoarchitecture: Territoires Urbanisation, Biodiversité, Environnement (EA 7462 G‑TUBE)Université de Rennes 1, Université de Bretagne Occidentale, Campus de BeaulieuRennesFrance
  4. 4.CIBIO, Research Centre in Biodiversity and Genetic Resources, InBIO, Universidade do Porto, Campus Agrário de VairãoVairãoPortugal
  5. 5.Madagascar Fauna and Flora GroupToamasinaMadagascar
  6. 6.Institute of Zoology, Zoological Society of London, Regent’s ParkLondonUK
  7. 7.Centre for Ecology, Evolution and Environmental Changes (CE3C), Faculdade de Ciências da Universidade de LisboaLisbonPortugal

Personalised recommendations