Species' traits drive amphibian tolerance to anthropogenic habitat modification
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
Australian Government
PubMed
33939215
DOI
10.1111/gcb.15623
Knihovny.cz E-zdroje
- Klíčová slova
- amphibian declines, anthropogenic, biodiversity, citizen science, conservation, habitat modification, life history, species traits,
- MeSH
- biodiverzita * MeSH
- ekosystém * MeSH
- lidé MeSH
- žáby MeSH
- zachování přírodních zdrojů MeSH
- zemědělství MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Austrálie MeSH
Anthropogenic habitat modification is accelerating, threatening the world's biodiversity. Understanding species' responses to anthropogenic modification is vital for halting species' declines. However, this information is lacking for globally threatened amphibians, informed primarily by small community-level studies. We integrated >126,000 verified citizen science observations of frogs, with a global continuous measure of anthropogenic habitat modification for a continental scale analysis of the effects of habitat modification on frogs. We derived a modification tolerance index-accounting for anthropogenic stressors such as human habitation, agriculture, transport and energy production-for 87 species (36% of all Australian frog species). We used this index to quantify and rank each species' tolerance of anthropogenic habitat modification, then compiled traits of all the frog species and assessed how well these equipped species to tolerate modified habitats. Most of Australia's frog species examined were adversely affected by habitat modification. Habitat specialists and species with large geographic range sizes were the least tolerant of habitat modification. Call dominant frequency, body size, clutch type and calling position (i.e. from vegetation) were also related to tolerance of habitat modification. There is an urgent need for improved consideration of anthropogenic impacts and improved conservation measures to ensure the long-term persistence of frog populations, particularly focused on specialists and species identified as intolerant of modified habitats.
Australian Museum Research Institute Australian Museum Sydney NSW Australia
Faculty of Environmental Sciences Czech University of Life Sciences Prague Prague Czech Republic
Zobrazit více v PubMed
Alberti, M. (2015). Eco-evolutionary dynamics in an urbanizing planet. Trends in Ecology & Evolution, 30(2), 114-126. https://doi.org/10.1016/j.tree.2014.11.007
Anderson, R. B. (2019). Human traffic and habitat complexity are strong predictors for the distribution of a declining amphibian. PLoS One, 14(3), e0213426. https://doi.org/10.1371/journal.pone.0213426
Anstis, M. (2017). Tadpoles and frogs of Australia (2nd ed.). New Holland Publishers Pty Ltd.
Aronson, M. F. J., Nilon, C. H., Lepczyk, C. A., Parker, T. S., Warren, P. S., Cilliers, S. S., Goddard, M. A., Hahs, A. K., Herzog, C., Katti, M., La Sorte, F. A., Williams, N. S. G., & Zipperer, W. (2016). Hierarchical filters determine community assembly of urban species pools. Ecology, 97(11), 2952-2963. https://doi.org/10.1002/ecy.1535
Barton, K. (2019). MuMIn: Multi-model inference. R package version 1.43.15. Retrieved from https://CRAN.R-project.org/package=MuMIn
Bielby, J., Cooper, N., Cunningham, A., Garner, T., & Purvis, A. (2008). Predicting susceptibility to future declines in the world's frogs. Conservation Letters, 1(2), 82-90. https://doi.org/10.1111/j.1755-263X.2008.00015.x
Bioacoustics Research Program. (2017). Raven Pro: Interactive sound analysis software (Version 1.5). The Cornell Lab of Ornithology. Retrieved from http://www.birds.cornell.edu/raven
Callaghan, C. T., Benedetti, Y., Wilshire, J. H., & Morelli, F. (2020). Avian trait specialization is negatively associated with urban tolerance. Oikos, 129(10), 1541-1551. https://doi.org/10.1111/oik.07356
Callaghan, C. T., Major, R. E., Wilshire, J. H., Martin, J. M., Kingsford, R. T., & Cornwell, W. K. (2019). Generalists are the most urban-tolerant of birds: A phylogenetically controlled analysis of ecological and life history traits using a novel continuous measure of bird responses to urbanization. Oikos, 128(6), 845-858. https://doi.org/10.1111/oik.06158
Callaghan, C. T., Roberts, J. D., Poore, A. G., Alford, R. A., Cogger, H., & Rowley, J. J. (2020). Citizen science data accurately predicts expert-derived species richness at a continental scale when sampling thresholds are met. Biodiversity and Conservation, 29(4), 1323-1337. https://doi.org/10.1007/s10531-020-01937-3
Cooper, N., Bielby, J., Thomas, G. H., & Purvis, A. (2008). Macroecology and extinction risk correlates of frogs. Global Ecology and Biogeography, 17(2), 211-221. https://doi.org/10.1111/j.1466-8238.2007.00355.x
Croci, S., Butet, A., & Clergeau, P. (2008). Does urbanization filter birds on the basis of their biological traits? The Condor, 110(2), 223-240. https://doi.org/10.1525/cond.2008.8409
Desrochers, A. (2010). Morphological response of songbirds to 100 years of landscape change in North America. Ecology, 91(6), 1577-1582. https://doi.org/10.1890/09-2202.1
Ducatez, S., Sayol, F., Sol, D., & Lefebvre, L. (2018). Are urban vertebrates city specialists, artificial habitat exploiters, or environmental generalists? Integrative and Comparative Biology, 58(5), 929-938. https://doi.org/10.1093/icb/icy101
ESA 2010 and UCLouvain. Retrieved from http://due.esrin.ESA.int/page_globcover.php
Evans, K. L., Chamberlain, D. E., Hatchwell, B. J., Gregory, R. D., & Gaston, K. J. (2011). What makes an urban bird? Global Change Biology, 17(1), 32-44. https://doi.org/10.1111/j.1365-2486.2010.02247.x
Fox, J., & Weisberg, S. (2019). An R companion to applied regression (3rd ed.). Sage. Retrieved from https://socialsciences.mcmaster.ca/jfox/Books/Companion/
Francesco Ficetola, G., & De Bernardi, F. (2004). Amphibians in a human-dominated landscape: the community structure is related to habitat features and isolation. Biological Conservation, 119(2), 219-230. https://doi.org/10.1016/j.biocon.2003.11.004
Gagné, S. A., & Fahrig, L. (2010). Effects of time since urbanization on anuran community composition in remnant urban ponds. Environmental Conservation, 37(2), 128-135. https://doi.org/10.1017/S0376892910000421
Gelman, A., & Su, Y.-S. (2018). arm: Data analysis using regression and multilevel/hierarchical models (Version 1.10-1). Retrieved from https://CRAN.R-project.org/package=arm
Gonzalez-Del-Pliego, P., Freckleton, R. P., Edwards, D. P., Koo, M. S., Scheffers, B. R., Pyron, R. A., & Jetz, W. (2019). Phylogenetic and trait-based prediction of extinction risk for data-deficient amphibians. Current Biology, 29(9), 1557-1563. https://doi.org/10.1016/j.cub.2019.04.005
Gorelick, N., Hancher, M., Dixon, M., Ilyushchenko, S., Thau, D., & Moore, R. (2017). Google Earth Engine: Planetary-scale geospatial analysis for everyone. Remote Sensing of Environment, 202, 18-27. https://doi.org/10.1016/j.rse.2017.06.031
Grueber, C. E., Nakagawa, S., Laws, R. J., & Jamieson, I. G. (2011). Multimodel inference in ecology and evolution: Challenges and solutions. Journal of Evolutionary Biology, 24(4), 699-711. https://doi.org/10.1111/j.1420-9101.2010.02210.x
Hayes, T. B., Falso, P., Gallipeau, S., & Stice, M. (2010). The cause of global amphibian declines: A developmental endocrinologist's perspective. Journal of Experimental Biology, 213(6), 921-933. https://doi.org/10.1242/jeb.040865
Henle, K., Davies, K. F., Kleyer, M., Margules, C., & Settele, J. (2004). Predictors of species sensitivity to fragmentation. Biodiversity and Conservation, 13(1), 207-251. https://doi.org/10.1023/B:BIOC.0000004319.91643.9e
Hero, J.-M., & Morrison, C. (2004). Frog declines in Australia: Global implications. Herpetological Journal, 14, 175-186.
Hero, J.-M., Williams, S. E., & Magnusson, W. E. (2005). Ecological traits of declining amphibians in upland areas of eastern Australia. Journal of Zoology, 267(03), 221. https://doi.org/10.1017/s0952836905007296
Hirschfeld, M., & Rodel, M. O. (2017). What makes a successful species? Traits facilitating survival in altered tropical forests. BMC Ecology, 17(1), 25. https://doi.org/10.1186/s12898-017-0135-y
Ho, L., & Ane, C. (2014). A linear-time algorithm for Gaussian and non-Gaussian trait evolution models. Systematic Biology, 63(3), 397-408. https://doi.org/10.1093/sysbio/syu005
Hobbs, N. T., & Hilborn, R. (2006). Alternatives to statistical hypothesis testing in ecology: A guide to self teaching. Ecological Applications, 16(1), 5-19. https://doi.org/10.1890/04-0645
Ives, C. D., Lentini, P. E., Threlfall, C. G., Ikin, K., Shanahan, D. F., Garrard, G. E., Bekessy, S. A., Fuller, R. A., Mumaw, L., Rayner, L., Rowe, R., Valentine, L. E., & Kendal, D. (2016). Cities are hotspots for threatened species. Global Ecology and Biogeography, 25(1), 117-126. https://doi.org/10.1111/geb.12404
Jetz, W., & Pyron, R. A. (2019). Data from: The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life. Dryad, Dataset, https://doi.org/10.5061/dryad.cc3n6j5
Johnson, C. N., Balmford, A., Brook, B. W., Buettel, J. C., Galetti, M., Guangchun, L., & Wilmshurst, J. M. (2017). Biodiversity losses and conservation responses in the Anthropocene. Science, 356(6335), 270-275. https://doi.org/10.1126/science.aam9317
Kaczmarski, M., Benedetti, Y., & Morelli, F. Y. (2020). Amphibian diversity in Polish cities: Taxonomic diversity, functional diversity and evolutionary distinctiveness. Basic and Applied Ecology, 44, 55-64. https://doi.org/10.1016/j.baae.2020.02.006
Keck, F., Rimet, F., Bouchez, A., & Franc, A. (2016). phylosignal: An R package to measure, test, and explore the phylogenetic signal. Ecology and Evolution, 6(9), 2774-2780. https://doi.org/10.1002/ece3.2051
Keinath, D. A., Doak, D. F., Hodges, K. E., Prugh, L. R., Fagan, W., Sekercioglu, C. H., Buchart, S. H. M., & Kauffman, M. (2017). A global analysis of traits predicting species sensitivity to habitat fragmentation. Global Ecology and Biogeography, 26(1), 115-127. https://doi.org/10.1111/geb.12509
Kennedy, C. M., Oakleaf, J. R., Theobald, D. M., Baruch-Mordo, S., & Kiesecker, J. (2019). Managing the middle: A shift in conservation priorities based on the global human modification gradient. Global Change Biology, 25(3), 811-826. https://doi.org/10.1111/gcb.14549
Knight, A. (2014). Sloane's Froglet interim habitat guide and management recommendations. Office of Environment and Heritage.
Kruger, D. J. D., Hamer, A. J., & Du Preez, L. H. (2015). Urbanization affects frog communities at multiple scales in a rapidly developing African city. Urban Ecosystems, 18(4), 1333-1352. https://doi.org/10.1007/s11252-015-0443-y
Lips, K. R., Reeve, J. D., & Witters, L. R. (2003). Ecological traits predicting amphibian population declines in Central America. Conservation Biology, 17(4), 1078-1088.
Liu, X., Huang, Y., Xu, X., Li, X., Li, X., Ciais, P., Lin, P., Gong, K., Ziegler, A. D., Chen, A., Gong, P., Chen, J., Hu, G., Chen, Y., Wang, S., Wu, Q., Huang, K., Estes, L., & Zeng, Z. (2020). High-spatiotemporal-resolution mapping of global urban change from 1985 to 2015. Nature Sustainability, 3(7), 564-570. https://doi.org/10.1038/s41893-020-0521-x
Moller, A. P. (2009). Successful city dwellers: A comparative study of the ecological characteristics of urban birds in the Western Palearctic. Oecologia, 159(4), 849-858. https://doi.org/10.1007/s00442-008-1259-8
Münkemüller, T., Lavergne, S., Bzeznik, B., Dray, S., Jombart, T., Schiffers, K., & Thuiller, W. (2012). How to measure and test phylogenetic signal. Methods in Ecology and Evolution, 3(4), 743-756. https://doi.org/10.1111/j.2041-210X.2012.00196.x
Murray, K. A., Rosauer, D., McCallum, H., & Skerratt, L. F. (2011). Integrating species traits with extrinsic threats: Closing the gap between predicting and preventing species declines. Proceedings of the Royal Society B: Biological Sciences, 278(1711), 1515-1523. https://doi.org/10.1098/rspb.2010.1872
Nori, J., Villalobos, F., & Loyola, R. (2018). Global priority areas for amphibian research. Journal of Biogeography, 45(11), 2588-2594. https://doi.org/10.1111/jbi.13435
Nowakowski, A. J., Frishkoff, L. O., Thompson, M. E., Smith, T. M., & Todd, B. D. (2018). Phylogenetic homogenization of amphibian assemblages in human-altered habitats across the globe. Proceedings of the National Academy of Sciences of the United States of America, 115(15), E3454-E3462. https://doi.org/10.1073/pnas.1714891115
Nowakowski, A. J., Thompson, M. E., Donnelly, M. A., & Todd, B. D. (2017). Amphibian sensitivity to habitat modification is associated with population trends and species traits. Global Ecology and Biogeography, 26(6), 700-712. https://doi.org/10.1111/geb.12571
Nowakowski, A. J., Watling, J. I., Thompson, M. E., Brusch, G. A., Catenazzi, A., Whitfield, S. M., Kurz, D. J., Suárez-Mayorga, Á., Aponte-Gutiérrez, A., Donnelly, M. A., & Todd, B. D. (2018). Thermal biology mediates responses of amphibians and reptiles to habitat modification. Ecology Letters, 21(3), 345-355. https://doi.org/10.1111/ele.12901
Öckinger, E., Schweiger, O., Crist, T. O., Debinski, D. M., Krauss, J., Kuussaari, M., Petersen, J. D., Pöyry, J., Settele, J., Summerville, K. S., & Bommarco, R. (2010). Life-history traits predict species responses to habitat area and isolation: A cross-continental synthesis. Ecology Letters, 13(8), 969-979. https://doi.org/10.1111/j.1461-0248.2010.01487.x
Olden, J. D., Poff, N. L., & Bestgen, K. R. (2008). Trait synergisms and the rarity, extirpation, and extinction risk of desert fishes. Ecology, 89(3), 847-856. https://doi.org/10.1890/06-1864.1
Parris, K. M., Velik-Lord, M., & North, J. M. (2009). Frogs call at a higher pitch in traffic noise. Ecology and Society, 14(1), 25. https://doi.org/10.5751/ES-02687-140125
Phillips, B. L., Brown, G. P., Webb, J. K., & Shine, R. (2006). Invasion and the evolution of speed in toads. Nature, 439(7078), 803. https://doi.org/10.1038/439803a
Pillsbury, F. C., & Miller, J. R. (2008). Habitat and landscape characteristics underlying anuran community structure along an urban-rural gradient. Ecological Applications, 18(5), 1107-1118. https://doi.org/10.1890/07-1899.1
R Core Team. (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing. Retrieved from https://www.R-project.org/
Richardson, J. L., Michaelides, S., Combs, M., Djan, M., Bisch, L., Barrett, K., Silveira, G., Butler, J., Aye, T. T., Munshi-South, J., DiMatteo, M., Brown, C., & McGreevy, T. J. (2020). Dispersal ability predicts spatial genetic structure in native mammals persisting across an urbanization gradient. Evolutionary Applications, 14(1), 163-177. https://doi.org/10.1111/eva.13133
Roca, I. T., Desrochers, L., Giacomazzo, M., Bertolo, A., Bolduc, P., Deschesnes, R., Martin, C. A., Rainville, V., Rheault, G., & Proulx, R. (2016). Shifting song frequencies in response to anthropogenic noise: A meta-analysis on birds and anurans. Behavioral Ecology, 27(5), 1269-1274. https://doi.org/10.1093/beheco/arw060
Rowley, J. J. L., & Callaghan, C. T. (2020). The FrogID dataset: Expert-validated occurrence records of Australia's frogs collected by citizen scientists. ZooKeys, 912, 139. https://doi.org/10.3897/zookeys.912.38253
Rowley, J. J. L., Callaghan, C. T., Cutajar, T., Portway, C., Potter, K., Mahony, S., & Woods, A. (2019). FrogID: Citizen scientists provide validated biodiversity data on frogs of Australia. Herpetological Conservation and Biology, 14(1), 155-170.
Scheffers, B. R., & Paszkowski, C. A. (2011). The effects of urbanization on North American amphibian species: Identifying new directions for urban conservation. Urban Ecosystems, 15(1), 133-147. https://doi.org/10.1007/s11252-011-0199-y
Schell, C. B., & Burgin, S. (2003). Swimming against the current: the brown striped marsh frog Limnodynastes peronii success story. Australian Zoologist, 32(3), 401-405.
Sih, A., Ferrari, M. C., & Harris, D. J. (2011). Evolution and behavioural responses to human-induced rapid environmental change. Evolutionary Applications, 4(2), 367-387. https://doi.org/10.1111/j.1752-4571.2010.00166.x
Sodhi, N. S., Bickford, D., Diesmos, A. C., Lee, T. M., Koh, L. P., Brook, B. W., Sekercioglu, C. H., & Bradshaw, C. J. A. (2008). Measuring the meltdown: Drivers of global amphibian extinction and decline. PLoS One, 3(2), e1636. https://doi.org/10.1371/journal.pone.0001636
Sullivan, A. P., Bird, D. W., & Perry, G. H. (2017). Human behaviour as a long-term ecological driver of non-human evolution. Nature Ecology & Evolution, 1(3), 0065. https://doi.org/10.1038/s41559-016-0065
Tilman, D., Clark, M., Williams, D. R., Kimmel, K., Polasky, S., & Packer, C. (2017). Future threats to biodiversity and pathways to their prevention. Nature, 546(7656), 73-81. https://doi.org/10.1038/nature22900
Tonini, J. F. R., Provete, D. B., Maciel, N. M., Morais, A. R., Goutte, S., Toledo, L. F., & Pyron, R. A. (2020). Allometric escape from acoustic constraints is rare for frog calls. Ecology and Evolution, 10(8), 3686-3695. https://doi.org/10.1002/ece3.6155
Urban, M. C., Phillips, B. L., Skelly, D. K., & Shine, R. (2007). The cane toad's (Chaunus [Bufo] marinus) increasing ability to invade Australia is revealed by a dynamically updated range model. Proceedings of the Royal Society B: Biological Sciences, 274(1616), 1413-1419. https://doi.org/10.1098/rspb.2007.0114
Villaseñor, N. R., Driscoll, D. A., Gibbons, P., Calhoun, A. J. K., & Lindenmayer, D. B. (2017). The relative importance of aquatic and terrestrial variables for frogs in an urbanizing landscape: Key insights for sustainable urban development. Landscape and Urban Planning, 157, 26-35. https://doi.org/10.1016/j.landurbplan.2016.06.006
Webb, C. T., Hoeting, J. A., Ames, G. M., Pyne, M. I., & LeRoy Poff, N. (2010). A structured and dynamic framework to advance traits-based theory and prediction in ecology. Ecology Letters, 13(3), 267-283. https://doi.org/10.1111/j.1461-0248.2010.01444.x
Wei, T., & Simko, V. (2017). R package “corrplot”: Visualization of a correlation matrix (Version 0.84). Retrieved from https://github.com/taiyun/corrplot
Westgate, M. J., Scheele, B. C., Ikin, K., Hoefer, A. M., Beaty, R. M., Evans, M., Osborne, W., Hunter, D., Rayner, L., & Driscoll, D. A. (2015). Citizen science program shows urban areas have lower occurrence of frog species, but not accelerated declines. PLoS One, 10(11), e0140973. https://doi.org/10.1371/journal.pone.0140973
Winchell, K. M., Reynolds, R. G., Prado-Irwin, S. R., Puente-Rolón, A. R., & Revell, L. J. (2016). Phenotypic shifts in urban areas in the tropical lizard Anolis cristatellus. Evolution, 70(5), 1009-1022. https://doi.org/10.1111/evo.12925
Anthropogenic habitat modification alters calling phenology of frogs