Skip to main content

Advertisement

SpringerLink
Log in

Species IUCN threat status level increases with elevation: a phylogenetic approach for Neotropical tree frog conservation

  • Original Paper
  • Published:
Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

Species conservation efforts are increasingly using genetic diversity and phylogeny to inform policy decisions. Evolutionary distinctiveness (ED), which estimates genetic diversity based on phylogenetic branch lengths and species richness, is commonly used to prioritize species conservation. Large-scale studies of ED in amphibians have reported correlations among threatened status, area of distribution and habitat lost. However, conservation priorities based on ED could be more impactful for clades with high species richness, as well as considering the risk factors associated with species vulnerability in a local setting. We implemented comparative phylogenetic methods and multivariate regression to test the factors influencing species threatened status in a large clade of frogs within the subfamily Hylinae. We present the most comprehensive molecular phylogeny for the group, including 139 species, 265 individuals, and 12 additional species that were not previously studied. Additional data for each species includes (1) conservation status on the IUCN red list; (2) evolutionary distinctiveness; (3) species distribution in square kilometers; and (4) elevation profiles. Using a Phylogenetic General Linear Model to test the relationships among these variables, we found a significant correlation between threatened status and elevation. The threatened status of species was not correlated with ED or distribution area, which is inconsistent with large-scale studies spanning multiple families. By taking evolutionary history into account and testing for relationships between IUCN threatened status and factors at a regional scale, we provide new information for redirecting tree frog conservation efforts in the Neotropics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

All relevant data is contain within the paper and the supplementary materials. Please contact the corresponding author for any additional request.

References

  • Allentoft ME, O’Brien J (2010) Global amphibian declines, loss of genetic diversity and fitness: a review. Diversity 2(1):47–71

    Article  Google Scholar 

  • AmphibiaWeb (2019) University of California, Berkeley, CA, USA. https://amphibiaweb.org. Accessed 16 May 2019

  • Antonelli A, Kissling WD, Flantua SG, Bermúdez MA, Mulch A, Muellner-Riehl AN, Kreft H, Linder HP, Badgley C, Fjeldså J, Fritz SA (2018) Geological and climatic influences on mountain biodiversity. Nat Geosci 10:718–725

    Article  CAS  Google Scholar 

  • Beebee TJ, Griffiths RA (2005) The amphibian decline crisis: a watershed for conservation biology? Biol Conserv 125(3):271–285

    Article  Google Scholar 

  • Börner J, Baylis K, Corbera E, Ezzine-de-Blas D, Honey-Rosés J, Persson UM, Wunder S (2017) The effectiveness of payments for environmental services. World Dev 96:359–374

    Article  Google Scholar 

  • Caviedes-Solis IW, Montes de Oca A (2018) A multilocus phylogeny of the genus Sarcohyla (Anura: Hylidae), and an investigation of species boundaries using statistical species delimitation. Mol Phylogenet Evol 118:184–193

    Article  PubMed  Google Scholar 

  • Caviedes-Solis IW, Leaché AD (2018) Leapfrogging the Mexican highlands: influence of biogeographical and ecological factors on the diversification of highland species. Biol J Linn Soc 123(4):767–781

    Article  Google Scholar 

  • Charif D, Lobry JR (2007) SeqinR 1.0–2: a contributed package to the R project for statistical computing devoted to biological sequences retrieval and analysis. Structural approaches to sequence evolution. Springer, Berlin, pp 207–232

    Chapter  Google Scholar 

  • Collen B, Turvey ST, Waterman C, Meredith HM, Kuhn TS, Baillie JE, Isaac NJ (2011) Investing in evolutionary history: implementing a phylogenetic approach for mammal conservation. Philos Trans R Soc B 366(1578):2611–2622

    Article  Google Scholar 

  • Colston TJ, Kulkarni P, Jetz W, Pyron RA (2019) Phylogenetic and spatial distribution of evolutionary isolation and threat in turtles and crocodilians (Non-Avian Archosauromorphs). bioRxiv 607796

  • Corey SJ, Waite TA (2008) Phylogenetic autocorrelation of extinction threat in globally imperilled amphibians. Divers Distrib 14(4):614–629

    Article  Google Scholar 

  • Díaz-García JM, López-Barrera F, Toledo-Aceves T, Andresen E, Pineda E (2020) Does forest restoration assist the recovery of threatened species? A study of cloud forest amphibian communities. Biol Conserv 242:108400

    Article  Google Scholar 

  • Drummond AJ, Rambau A, Suchard M (2013) BEAST 1.8. 0

  • Duellman WE (2001) The hylid frogs of Middle America Vol 1. Society for the Study of Amphibians and Reptiles. Natural History Museum of the University of Kansas, Ithaca

    Google Scholar 

  • Duellman WE, Marion AB, Hedges SB (2016) Phylogenetics, classification, and biogeography of the treefrogs (Amphibia: Anura: Arboranae). Zootaxa 4104(1):1–109

    Article  PubMed  Google Scholar 

  • EDGE (2019) https://www.edgeofexistence.org/

  • Faivovich J, Haddad CF, Garcia PC, Frost DR, Campbell JA, Wheeler WC (2005) Systematic review of the frog family Hylidae, with special reference to Hylinae: phylogenetic analysis and taxonomic revision. Bull Am Mus Nat Hist 294:1–240

    Article  Google Scholar 

  • Faivovich J, Pereyra MO, Luna MC, Hertz A, Blotto BL, Vásquez-Almazán CR, McCranie JR, Sánchez DA, Baêta D, Araujo-Vieira K, Köhler G (2018) On the monophyly and relationships of several genera of Hylini (Anura: Hylidae: Hylinae), with comments on recent taxonomic changes in hylids. S Am J Herpetol 13(1):1–33

    Article  Google Scholar 

  • Fetzner JW Jr (1999) Extracting high-quality DNA from shed reptile skins: a simplified method. Biotechniques 26:1052–1054

    Article  CAS  PubMed  Google Scholar 

  • Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Glob Ecol Biogeogr 16(3):265–280

    Article  Google Scholar 

  • Fritz SA, Rahbek C (2012) Global patterns of amphibian phylogenetic diversity. J Biogeogr 39(8):1373–1382

    Article  Google Scholar 

  • Frost DR, Grant T, Faivovich J, Bain RH, Haas A, Haddad CF, De Sa RO, Channing A, Wilkinson M, Donnellan SC, Raxworthy CJ (2006) The amphibian tree of life. Bull Am Museum Nat Hist 2006:1–291

    Google Scholar 

  • Frost DR (2019). Amphibian species of the world: an online reference. Version 6.0 (Date of access). American Museum of Natural History, New York, USA. https://research.amnh.org/herpetology/amphibia/index.html

  • Gascon C (2007) Amphibian conservation action plan: proceedings IUCN/SSC Amphibian Conservation Summit 2005. IUCN

  • Graber S (2013) Phylogenetic comparative methods for discrete responses in evolutionary biology. Doctoral dissertation, University of Zurich

  • GBIF.org (2018) GBIF . OccurrenceDownload

  • Gordon JE (2020) Geoconservation principles and protected area management. Int J Geoheritage Parks 7:199–210

    Article  Google Scholar 

  • Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W (2007) GEIGER: investigating evolutionary radiations. Bioinformatics 24(1):129–131

    Article  CAS  PubMed  Google Scholar 

  • Hijmans RJ, van Etten J, Cheng J, Mattiuzzi M, Sumner M, Greenberg JA, Lamigueiro OP, Bevan A, Racine EB, Shortridge A, Hijmans MRJ (2015) Package ‘raster’. R package.

  • Isaac NJ, Turvey ST, Collen B, Waterman C, Baillie JE (2007) Mammals on the EDGE: conservation priorities based on threat and phylogeny. PLoS ONE 2(3):296

    Article  Google Scholar 

  • Isaac NJ, Redding DW, Meredith HM, Safi K (2012) Phylogenetically-informed priorities for amphibian conservation. PLoS ONE 7(8):43912

    Article  CAS  Google Scholar 

  • IPBES (2020) https://ipbes.net/global-assessment Accessed Mar 2020

  • IUCN (2019) The IUCN Red List of Threatened Species. Version 2019–2. https://www.iucnredlist.org. Accessed 21 Mar 2019

  • IUCN (2020) World commission of protected areas. Mountains https://www.iucn.org/commissions/world-commission-protected-areas/our-work/mountains

  • Jetz W, Pyron RA (2018) The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life. Nat Ecol Evol 2(5):850

    Article  PubMed  Google Scholar 

  • Jimenez-Arcos VH, Calzada-Arciniega RA, Alfaro-Juantorena LA, Vazquez-Reyes LD, Blair C, Parra-Olea G (2019) A new species of Charadrahyla (Anura: Hylidae) from the cloud forest of western Oaxaca. Mexico Zootaxa 4554(2):371–385

    Article  PubMed  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649

    Article  PubMed Central  PubMed  Google Scholar 

  • Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26(11):1463–1464

    Article  CAS  PubMed  Google Scholar 

  • Köhler J, Vieites DR, Bonett RM, García FH, Glaw F, Steinke D, Vences M (2005) New amphibians and global conservation: a boost in species discoveries in a highly endangered vertebrate group. Bioscience 55(8):693–696

    Article  Google Scholar 

  • Korner C, Spehn EM (eds) (2019) Mountain biodiversity: a global assessment, vol 7. Routledge, London

    Google Scholar 

  • Lips KR, Mendelson JR, Muñoz-Alonso A, Canseco-Márquez L, Mulcahy DG (2004) Amphibian population declines in montane southern Mexico: resurveys of historical localities. Biol Conserv 119:555–564

    Article  Google Scholar 

  • Lips KR, Burrowes PA, Mendelson JR III, Parra-Olea G (2005) Amphibian population declines in Latin America: a synthesis 1. Biotrop J Biol Conserv 37(2):222–226

    Google Scholar 

  • MacManes M (2013) MacManes salt extraction protocol. Figshare. http://dx.doi.org/10.6084/m9.figshare,658946

  • Martin-Lopez B, Leister I, Cruz PL, Palomo I, Grêt-Regamey A, Harrison PA, Lavorel S, Locatelli B, Luque S, Walz A (2019) Nature’s contributions to people in mountains: a review. PLoS ONE 14(6):24

    Article  CAS  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  PubMed  Google Scholar 

  • Nowakowski AJ, Watling JI, Thompson ME, Brusch GA IV, Catenazzi A, Whitfield SM, Kurz DJ, Suárez-Mayorga Á, Aponte-Gutiérrez A, Donnelly MA, Todd BD (2018) Thermal biology mediates responses of amphibians and reptiles to habitat modification. Ecol Lett 21(3):345–355

    Article  PubMed  Google Scholar 

  • Ogilvie H, Bouckaert R, Drummond A (2017) StarBEAST2 brings faster species tree inference and accurate estimates of substitution rates. Mol Biol Evol 34:2101–2114

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Orme D, Freckleton R, Thomas G, Petzoldt T (2013) The caper package: comparative analysis of phylogenetics and evolution in R. R Package Version 5(2):1–36

    Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20(2):289–290

    Article  CAS  PubMed  Google Scholar 

  • Pearman PB, Garner TW (2005) Susceptibility of Italian agile frog populations to an emerging strain of Ranavirus parallels population genetic diversity. Ecol Lett 8(4):401–408

    Article  Google Scholar 

  • Portik D, Wiens J (2019) SuperCRUNCH: A toolkit for creating and manipulating supermatrices and other large phylogenetic datasets. bioRxiv 538728.

  • Pyron RA, Wiens JJ (2011) A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol Phylogenet Evol 61(2):543–583

    Article  PubMed  Google Scholar 

  • Pyron RA, Wiens JJ (2013) Large-scale phylogenetic analyses reveal the causes of high tropical amphibian diversity. Proc R Soc 280(1770):20131622

    Article  Google Scholar 

  • Redding DW, Mazel F, Mooers AØ (2014) Measuring evolutionary isolation for conservation. PLoS ONE 9(12):113490

    Article  CAS  Google Scholar 

  • Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3(2):217–223

    Article  Google Scholar 

  • Rzedowski J (1996) Análisis preliminar de la flora vascular de los bosques mesófilos de montaña de México. Acta Botánica Mexicana 35:25–44

    Article  Google Scholar 

  • Sitas N, Baillie JEM, Isaac NJB (2009) What are we saving? Developing a standardized approach for conservation action. Anim Conserv 12(3):231–237

    Article  Google Scholar 

  • Savage AE, Becker CG, Zamudio KR (2015) Linking genetic and environmental factors in amphibian disease risk. Evolut Appl 8(6):560–572

    Article  CAS  Google Scholar 

  • Smith SA, Nieto-Montes de Oca A, Reeder TW, Wiens JJ (2007) A phylogenetic perspective on elevational species richness patterns in Middle American treefrogs: why so few species in lowland tropical rainforests? Evolution 61:1188–1207

    Article  PubMed  Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313

    Article  CAS  PubMed Central  PubMed  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(5702):1783–1786

    Article  CAS  PubMed  Google Scholar 

  • Toledo-Aceves T, Meave JA, González-Espinosa M, Ramírez-Marcial N (2011) Tropical montane cloud forests: current threats and opportunities for their conservation and sustainable management in Mexico. J Environ Manag 92(3):974–981

    Article  Google Scholar 

  • Tonini JFR, Beard KH, Ferreira RB, Jetz W, Pyron RA (2016) Fully-sampled phylogenies of squamates reveal evolutionary patterns in threat status. Biol Conserv 204:23–31

    Article  Google Scholar 

  • Vaidya G, Lohman DJ, Meier R (2011) SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27(2):171–180

    Article  PubMed  Google Scholar 

  • Wiens JJ, Fetzner JW Jr, Parkinson CL, Reeder TW (2005) Hylid frog phylogeny and sampling strategies for speciose clades. Syst Biol 54(5):778–807

    Article  PubMed  Google Scholar 

  • Wiens JJ, Graham CH, Moen DS, Smith SA, Reeder TW (2006) Evolutionary and ecological causes of the latitudinal diversity gradient in hylid frogs: treefrog trees unearth the roots of high tropical diversity. Am Nat 168(5):579–596

    Article  PubMed  Google Scholar 

  • Winter DJ (2017) rentrez: An R package for the NCBI eUtils API (No. e3179v1). PeerJ Preprints.

  • Zarza E, Connors EM, Maley JM, Tsai WL, Heimes P, Kaplan M, McCormack JE (2018) Combining ultraconserved elements and mtDNA data to uncover lineage diversity in a Mexican highland frog (Sarcohyla; Hylidae). PeerJ 6:6045

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the Museo de Zoologia de la Facultad de Ciencias, “Alfonso L. Herrera” MZFC, Coleccion de Anfibios y Reptiles del Instituto de Ecologia CARIES, González-Bernal E., Jimenez-Arcos V., and Palacios-Aguilar R. for tissue donations. Thank you to Dr. Fausto Mendez de la Cruz for his support with specimen collection under permit 01205 SEMARNAT. Itzue W. Caviedes-Solis was funded by Consejo Nacional de Ciencia y Tecnologia, Mexico, CONACyT Fellowship Number 313501 “Becas CONACyT al Extranjero’ and the Burke Museum of Natural History and Cultures. Sequencing was funded by the Wyckoff Fellowship granted by the Biology Department at the University of Washington. For assistance with fieldwork, we thank Ross Furbush, Laura Frost, Luis Felipe Vazquez-Vega, Israel Solano-Zavaleta, Gustavo Campillo, and Yire A. Gomez-Jimenez. We thank Andrew Magee for assistance with phylogenetic analyses. We are especially grateful to the communities in Mexico that granted us permission to search for frogs in their forests and for hosting us in the field.

Funding

Itzue W. Caviedes-Solis was funded by Consejo Nacional de Ciencia y Tecnologia, Mexico, CONACyT Fellowship Number 313501 “Becas CONACyT al Extranjero’, the Burke Museum of Natural History and Cultures. Sequencing was funded by the Wyckoff Fellowship granted by the Biology Department at the University of Washington.

Author information

Author notes

  1. Nicholas Kim

    Present address: GRECC Department, Veteran’s Affair Puget Sound Healthcare System, Building 8 Room 103, 1660 South Columbian Way, Seattle, WA, 98108, USA

Authors and Affiliations

  1. Department of Biology and Burke Museum of Natural History and Culture, University of Washington, Box 351800, Seattle, WA, 98195, USA

    Itzue W. Caviedes-Solis, Nicholas Kim & Adam D. Leaché

  2. Science Unit, Lingnan University, NAB116/6, 1/F New Academic Block, Tuen Mun, New Territories, Hong Kong

    Itzue W. Caviedes-Solis

Authors
  1. Itzue W. Caviedes-Solis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nicholas Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adam D. Leaché
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Itzue W. Caviedes-Solis.

Ethics declarations

Conflict of interest

All the authors declared that they have no conflict of interest.

Ethics approval

We collected animals with approval from the UW Institutional Animal Care and Use Committee (IACUC protocol # 4209-01).

Informed consent

All the authors consented to participate in the project and publication.

Additional information

Communicated by Dirk Sven Schmeller.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Caviedes-Solis, I.W., Kim, N. & Leaché, A.D. Species IUCN threat status level increases with elevation: a phylogenetic approach for Neotropical tree frog conservation. Biodivers Conserv 29, 2515–2537 (2020). https://doi.org/10.1007/s10531-020-01986-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-020-01986-8

Keywords

Search

Navigation