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Desiccation resistance explains amphibian distributions in a fragmented tropical forest landscape

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Abstract

Context

Although amphibian distributions are associated with environmental moisture at global and local scales, less is known about how desiccation tolerance influences landscape distributions of amphibians.

Objectives

We evaluated two hypotheses linking amphibian distributions in a fragmented tropical forest landscape to desiccation risk. The patch quality hypothesis predicts that desiccation-prone species are absent on small forest patches, which are generally warmer and drier than large patches. Alternatively, the matrix effects hypothesis suggests that desiccation-prone species are absent on isolated forest patches surrounded by open savanna because they will be unable to traverse the matrix in which patches occur.

Methods

We quantified interspecific variation in desiccation proneness using field-based desiccation trials, and tested for associations between desiccation proneness and distributions of amphibians in fragmented forest in northeastern Bolivia.

Results

Rates of evaporative water loss were negatively associated with an index of dispersal limitation, but unrelated to species’ area requirements.

Conclusions

By demonstrating that desiccation-prone species do not occur on isolated forest patches, we provide clear support for the matrix effects hypothesis. We suggest that desiccation proneness is a key trait that may determine amphibian responses to a range of global change drivers, including habitat loss and fragmentation, invasive species, and climate change.

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References

  • Barbosa O, Marquet PA, Bacilgalupe LD, Christie DA, del-Val E, Gutierrez AG, Jones CG, Weather KC, Amesto JJ (2010) Interactions among patch area, forest structure and water fluxes in a fog-inundated forest ecosystem in semi-arid Chile. Funct Ecol 24:909–917

    Article  Google Scholar 

  • Bates D, Bolker B, Haubo R, Walker S (2015) Package ‘lme4’, Linear mixed-effects models using Eigen and S4. https://github.com/lme4/lme4/

  • Beaumont LJ, Pitman A, Perkin S, Zimmermann NE, Yoccoz NG, Thuiller W (2011) Impacts of climate change on the world’s most exceptional ecoregions. Proc Natl Acad Sci USA 108:2306–2311

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Belmaker J, Jetz W (2011) Cross-scale variation in species richness-environment associations. Glob Ecol Biogeogr 20:464–474

    Article  Google Scholar 

  • Beuchat CA, Pough FH, Stewart MM (1984) Response to simultaneous dehydration and thermal stress in three species of Puerto Rican frogs. J Comp Physiol B 154:579–585

    Article  Google Scholar 

  • Bickford D, Sodhi NS, Diemos AC, Lee TM, Koh LP, Brook BW, Sekercioglu CH (2008) Forgetting habitat loss in amphibian extinctions-missing the forest for the disease. Response to: Lips KR, Diffendorfer J, Mendelson JR III et al (2008) Riding the wave: reconciling the roles of disease and climate change in amphibian declines. PLOS Biol 6:e72

    Article  Google Scholar 

  • Brook BW, Sodhi NS, Bradshaw CJA (2008) Synergies among extinction drivers under global change. Trends Ecol Evol 23:453–460

    Article  PubMed  Google Scholar 

  • Brown JH, Kodric-Brown A (1977) Turnover rates in insular biogeography: effects of immigration on extinction. Ecology 58:445–449

    Article  Google Scholar 

  • Calosi P, Bilton DT, Spicer JI (2008) Thermal tolerance, acclamatory capacity and vulnerability to global climate change. Biol Lett 23:99–102

    Article  Google Scholar 

  • Cline BB, Hunter ML Jr (2014) Different open-canopy vegetation types affect matrix permeability for a dispersing forest amphibian. J Appl Ecol 51:319–329

    Article  Google Scholar 

  • Corn PS (1994) Straight-line drift fences and pitfall traps. In: Heyer WR, Donnelly MA, McDiarmid RW, Hayek LC, Foster MS (eds) Measuring and monitoring biological diversity. Standard methods for amphibians. Smithsonian Institution Press, Washington DC, pp 109–117

    Google Scholar 

  • Cosentino BJ, Schooley RL, Phillips CA (2011) Connectivity of agroecosystems: dispersal costs can vary among crops. Landscape Ecol 26:371–379

    Article  Google Scholar 

  • Cox PM, Betts RA, Collins M, Harris PP, Huntingford C, Jones CD (2004) Amazonian forest dieback under climate-carbon cycle projections for the 21st century. Theoret Appl Climatol 78:137–156

    Article  Google Scholar 

  • Crawley MJ (2012) The R book. Wiley, Chichester

    Book  Google Scholar 

  • Da Silva FR, Almeida-Neto M, Mendonça do Prado VH, Haddad CFB, de Cerqueira Rossa‐Feres D (2013) Humidity levels drive reproductive modes and phylogenetic diversity of amphibians in the Brazilian Atlantic Forest. J Biogeogr 39:1720–1732

    Article  Google Scholar 

  • Didham RK, Tylianakis JM, Gemmell NJ, Rand TA, Ewers RM (2007) Interactive effects of habitat modification and species invasion on native species decline. Trends Ecol Evol 22:489–496

    Article  PubMed  Google Scholar 

  • Duarte H, Tejedo M, Katzenberger M, Marangoni F, Baldo D, Beltrán J, Andrea Martí D, Richter-Boix A, Gonzalez-Voyer A (2012) Can amphibians take the heat? Vulnerability to climate warming in subtropical and temperate larval amphibian communities. Glob Change Biol 18:412–421

    Article  Google Scholar 

  • Duellman WE (1999) Global distribution of amphibians: patterns, conservation and future challenges. In: Duellman WE (ed) Patterns of distribution of amphibians a global perspective. The Johns Hopkins University Press, Baltimore, pp 1–30

    Google Scholar 

  • Duellman WE, Trueb L (1994) Biology of amphibians. McGraw-Hill, New York

    Google Scholar 

  • Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 42:59–80

    Article  Google Scholar 

  • Ewers RM, Thorpe S, Didham RK (2007) Synergistic interactions between edge and area effects in a heavily fragmented landscape. Ecology 88:96–106

    Article  PubMed  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515

    Article  Google Scholar 

  • Fletcher RJ Jr (2005) Multiple edge effects and their implications in fragmented landscapes. J Anim Ecol 74:342–352

    Article  Google Scholar 

  • Fraser LH, Carlyle CN (2011) Is spotted knapweed (Centaurea stoebe L.) patch size related to the effect on soil and vegetation properties? Plant Ecol 212:975–983

    Article  Google Scholar 

  • Gascon C, Lovejoy TE, Jr Bierregaard RO, Malcolm JR, Stouffer PC, Vasconcelos HL, Borges S (1999) Matrix habitat and species richness in tropical forest remnants. Biol Conserv 91:223–229

    Article  Google Scholar 

  • Hastings A, Harrison S (1994) Metapopulation dynamics and genetics. Annu Rev Ecol Evol Syst 25:167–188

    Article  Google Scholar 

  • Hedges SB, Duellman WE, Heinicke MP (2008) New World direct-developing frogs (Anura: Terrarana): molecular phylogeny, classification, biogeography, and conservation. Zootaxa 1737:1–82

    Google Scholar 

  • Henle K, Davies KF, Kleyer M, Margules C, Settele J (2004) Predictors of species sensitivity to fragmentation. Biodivers Conserv 13:207–251

    Article  Google Scholar 

  • Hillman SS, Drewes RC, Hedrick MS, Hancock TV (2014) Physiological vagility: correlations with dispersal and population genetic structure of amphibians. Physiol Biochem Zool 87:105–112

    Article  PubMed  Google Scholar 

  • Joseph GS, Cumming GS, Cumming DHM, Mahlangu Z, Altwegg R, Seymour CL (2011) Large termitaria act as refugia for tall trees, deadwood and cavity-using birds in a miombo woodland. Landscape Ecol 26:439–448

    Article  Google Scholar 

  • Jupp TE, Cox PM, Ramming A, Thonicke K, Lucht W, Cramer W (2010) Development of probability density functions for future South American rainfall. New Phytol 187:682–693

    Article  PubMed  Google Scholar 

  • Kolozsvary MB, Swihart RK (1999) Habitat fragmentation and the distribution of amphibians: patch and landscape correlates in farmland. Can J Zool 77:1288–1299

    Article  Google Scholar 

  • Laurance WF, Lovejoy TE, Vasconcelos HL, Bruna EM, Didham R, Stouffer PC (2002) Ecosystem decay of Amazonian forest fragments: a 22-year investigation. Conserv Biol 16:605–618

    Article  Google Scholar 

  • Lavergne S, Mouquet N, Thuiller W, Thuiller W, Ronce O (2010) Biodiversity and climate change: integrating evolutionary and ecological responses of species and communities. Annu Rev Ecol Evol Syst 41:321–350

    Article  Google Scholar 

  • Le Maitre DC, van Wilgen BW, Genderblom CM, Bailey C, Chapman R, Nel JA (2002) Invasive alien trees and water resources in South Africa: case studies of the costs and benefits of management. For Ecol Manage 160:143–159

    Article  Google Scholar 

  • Lee-Yaw JA, Sechley TH, Irwin DE (2015) Conflicting effects of microhabitats on Long-toed Salamander (Ambystoma macrodactylum) movement: implications for landscape connectivity. Can J Zool 93:1–7

    Article  Google Scholar 

  • Martin KL, Carter AL (2013) Brave new propagules: terrestrial embryos in amniotic eggs. Integr Comp Biol. doi:10.1093/icb/ict018

    Google Scholar 

  • Matlack GR (1993) Microenvironment variation within and among forest edge sites in the eastern United States. Biol Conserv 66:185–194

    Article  Google Scholar 

  • Mayle FE, Langstroth RP, Fisher RA, Meir P (2007) Long-term forest-savannah dynamics in the Bolivian Amazon: implications for conservation. Philos Trans R Soc B 362:291–307

    Article  Google Scholar 

  • Mazerolle MJ, Desrochers A (2005) Landscape resistance to frog movements. Can J Zool 83:455–464

    Article  Google Scholar 

  • Nepstad DC, Stickler CM, Soares-Filho B, Merry F (2008) Interactions among Amazon land use, forests and climate: prospects for a near-term forest tipping point. Philos Trans R Soc B Biol Sci 363:1737–1746

    Article  Google Scholar 

  • Nowakowski AJ, Jiménez BO, Allen M, Diaz-Escobar M, Donnelly MA (2013) Landscape resistance to movement of the poison frog, Oophaga pumilio, in the lowlands of northeastern Costa Rica. Anim Conserv 16:188–197

    Article  Google Scholar 

  • Peterman WE, Semlitsch RD (2014) Spatial variation in water loss predicts terrestrial salamander distribution and population dynamics. Oecologia 176:357–369

    Article  PubMed  CAS  Google Scholar 

  • Peterman WE, Locke JL, Semlitsch RD (2013) Spatial and temporal patterns of water loss in heterogeneous landscapes: using plaster models as amphibian analogues. Can J Zool 91:135–140

    Article  Google Scholar 

  • Peterman WE, Connette GM, Semlitsch RD, Eggert LS (2014) Ecological resistance surfaces predict fine-scale genetic differentiation in a terrestrial woodland salamander. Mol Ecol 23:2402–2413

    Article  PubMed  Google Scholar 

  • Pough FH, Stewart MM, Thomas RG (1977) Physiological basis of habitat partitioning in Jamaican Eleutherodactylus. Oecologia 27:285–293

    Article  Google Scholar 

  • R Development Core Team (2014) R: A language and environment for statistical computing, reference index version 3.1.1. R Foundation for Statistical Computing, Vienna, www.R-project.org

  • Reid AM, Lortie CJ (2012) Cushion plants are foundation species with positive effects extending to higher trophic levels. Ecosphere 3:art96

    Article  Google Scholar 

  • Rittenhouse TAG, Harper EB, Rehard LR, Semlitsch RD (2008) The role of microhabitats in the desiccation and survival of anurans in recently harvested Oak-Hickory forest. Copeia 2008:807–814

    Article  Google Scholar 

  • Rollins-Smith LA, Ramsey JP, Pask JD, Reinert LK, Woodhams D (2011) Amphibian immune defense against chytridiomycosis: impacts of changing environments. Integr Comp Biol 51:552–562

    Article  PubMed  CAS  Google Scholar 

  • Rosenberg DK, Noon BJ, Megahan JW, Meslow EC (1998) Compensatory behavior of Ensatina eschscholtzii in biological corridors: a field experiment. Can J Zool 76:117–133

    Article  Google Scholar 

  • Rothermel BB, Luring TM (2005) Burrow availability and desiccation risk of mole salamanders (Ambystoma talpoideum) in harvested versus unharvested forest stands. J Herpetol 39:619–626

    Article  Google Scholar 

  • Rothermel BB, Semlitsch RD (2002) An experimental investigation of landscape resistance of forest versus old-field habitats to emigrating juvenile amphibians. Conserv Biol 16:1324–1332

    Article  Google Scholar 

  • Salazar LF, Nobre CA, Oyama MD (2007) Climate change consequences on the biome distribution in tropical South America. Geophys Res Lett 34:L09708

    Article  Google Scholar 

  • Sinsch U (1997) Postmetamorphic dispersal and recruitment of first breeders in a Bufo calamita metapopulation. Oecologia 112:42–47

    Article  Google Scholar 

  • Smith MA, Green DM (2005) Dispersal and the metapopulation paradigm in amphibian ecology and conservation: are all amphibian populations metapopulations? Ecography 28:110–128

    Article  Google Scholar 

  • Sodhi NS, Bickford D, Diesmos AC, Lee TM, Koh LP, Brook BW, Bradshaw CJ (2008) Measuring the meltdown: drivers of global amphibian extinction and decline. PLoS One 3:e1636

    Article  PubMed  PubMed Central  Google Scholar 

  • Spight TM (1968) The water economy of salamanders: evaporative water loss. Physiol Zool 41:195–203

    Google Scholar 

  • Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues AS, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786

    Article  PubMed  CAS  Google Scholar 

  • Toledo RC, Jared C (1993) Cutaneous adaptations to water-balance in amphibians. Comp Biochem Physiol 105:593–608

    Article  Google Scholar 

  • Warton DI, Hui FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10

    Article  PubMed  Google Scholar 

  • Watling JI, Donnelly MA (2006) Fragments as islands: a synthesis of faunal responses to habitat patchiness. Conserv Biol 20:1016–1025

    Article  PubMed  Google Scholar 

  • Watling JI, Donnelly MA (2007) Multivariate correlates of extinction proneness in a naturally fragmented landscape. Divers Distrib 13:372–378

    Article  Google Scholar 

  • Watling JI, Donnelly MA (2008) Species richness and composition of amphibians and reptiles in a fragmented forest landscape in northeastern Bolivia. Basic Appl Ecol 9:523–532

    Article  Google Scholar 

  • Watling JI, Gerow K, Donnelly MA (2009) Isolation and nested species subsets of amphibians and reptiles on Neotropical forest islands. Anim Conserv 12:467–476

    Article  Google Scholar 

  • Withers PC, Hilman SS, Drewes RC (1984) Evaporative water loss and skin lipids of anuran amphibians. J Exp Zool 232:11–17

    Article  Google Scholar 

  • Wygoda ML (1984) Low cutaneous evaporative water loss in arboreal frogs. Physiol Zool 57:329–337

    Google Scholar 

  • Wygoda ML (1992) Exchange of water, ions, and respiratory gases in terrestrial amphibians. In: Feder FE, Burggren WW (eds) Environmental physiology of the amphibians. University of Chicago Press, Chicago, pp 125–150

    Google Scholar 

  • Young JE, Christian KA, Donnellan S, Tracy CR, Parry D (2005) Comparative analysis of cutaneous evaporative water loss in frogs demonstrates correlation with ecological habits. Physiol Biochem Zool 78:847–856

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank the Weeden Foundation for financial support of our research, and Kathia Rivero of the Museo de Historia Natural Noel Kempff Mercado for arranging research permits. Logistical support in the field was provided by Ian Phillips, Paulo Olivas and Reynaldo Choré. This work was done under University of Florida non-regulatory animal research permit 001-12FTL.

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  1. James I. Watling

    Present address: Department of Biology, John Carroll University, University Heights, OH, 44118, USA

Authors and Affiliations

  1. Ft Lauderdale Research and Education Center, University of Florida, 3205 College Avenue, Fort Lauderdale, FL, 33314, USA

    James I. Watling

  2. Museo de Historia Natural Noel Kempff Mercado, Avenida Irala 565, Santa Cruz De La Sierra, Bolivia

    Lorenzo Braga

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  1. James I. Watling
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  2. Lorenzo Braga
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Correspondence to James I. Watling.

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Watling, J.I., Braga, L. Desiccation resistance explains amphibian distributions in a fragmented tropical forest landscape. Landscape Ecol 30, 1449–1459 (2015). https://doi.org/10.1007/s10980-015-0198-0

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