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Doomed before they are described? The need for conservation assessments of cryptic species complexes using an amblyopsid cavefish (Amblyopsidae: Typhlichthys) as a case study

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Abstract

The delimitation of cryptic species and lineages is a common finding of phylogenetic studies. Species previously considered to be of low conservation priority might actually be comprised of multiple lineages with substantially smaller geographic ranges and smaller populations that are of much greater conservation concern and that require different conservation strategies. Cryptic biodiversity is an especially common finding in phylogenetic studies of subterranean fauna; however, most cryptic lineages remain undescribed and have not been subjected to conservation assessments. As many subterranean species are of high conservation concern, the conservation assessment of cryptic lineages is important for developing effective conservation and management strategies. In particular, some lineages might be in need of immediate conservation action even before formal taxonomic description. Here we explore this issue by conducting IUCN Red List and NatureServe conservation assessments on recently discovered cryptic lineages of the southern cavefish (Typhlichthys subterraneus) species complex. We ascertained threats associated with extinction risk, identified priority lineages and populations for immediate conservation efforts, and identified knowledge gaps to expedite the development of conservation and management strategies before formal taxonomic description. Most cryptic lineages are at an elevated risk of extinction, including one lineage classified as “Critically Endangered.” We identified ten threats impacting cavefish lineages that vary in both scope and severity, including groundwater pollution, hydrological changes from impoundments, and over-collection. Our threat assessments and recommendations can be used by stakeholders to prioritize effective and appropriate management initiatives aiding in the conservation of these lineages even before they are formally recognized.

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References

  • Agapow PM, Bininda-Emonds ORP, Crandall KA, Gittleman JL, Mace GM, Marshall JC, Purvis A (2004) The impact of species concept on biodiversity studies. Q Rev Biol 79:161–179

    Article  PubMed  Google Scholar 

  • Akcakaya HR, Ferson S, Burgman MA, Keith DA, Mace GM, Todd CR (2000) Making consistent IUCN classifications under uncertainty. Conserv Biol 14:1001–1013

    Article  Google Scholar 

  • Aley T (1990) Delineation and hydrogeologic study of the Key Cave Aquifer, Lauderdale County, Alabama. Technical report. U.S. Fish and Wildlife Service, Washington, p 114

  • Aley T, Aley C, Moss P, Hertzler E (2008) Hydrological characteristics of delineated recharge areas for 40 biologically significant cave and spring systems in Missouri, Arkansas, Oklahoma, and Illinois. In: Elliott W (ed) Proceedings of the 18th National Cave and Karst Management Symposium, St. Louis, Missouri, pp 154–167

  • Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell, Malden

    Google Scholar 

  • Bachman S, Moat J, Hill AW, de Torre J, Scott B (2011) Supporting Red List threat assessments with GeoCAT: geospatial conservation assessment tool. Zookeys 150:117–126

    Article  PubMed  Google Scholar 

  • Bailey V, Bailey FM, Giovannoli L (1933) Cave life of Kentucky, mainly in the Mammoth Cave region. Am Midl Nat 14:385–635

    Article  Google Scholar 

  • Barr TC, Holsinger JR (1985) Speciation in cave faunas. Annu Rev Ecol Syst 16:313–337

    Article  Google Scholar 

  • Barua M (2011) Mobilizing metaphors: the popular use of keystone, flagship and umbrella species concepts. Biodivers Conserv 20:1427–1440

    Article  Google Scholar 

  • Beheregaray LB, Caccone A (2007) Cryptic biodiversity in a changing world. J Biol 6:1–5

    Article  Google Scholar 

  • Bernardo J (2011) A critical appraisal of the meaning and diagnosability of cryptic evolutionary diversity, and its implications for conservation in the face of climate change. In: Hodkinson T, Jones M, Waldren S, Parnell J (eds) Climate change, ecology and systematics. Cambridge University Press, Cambridge, pp 380–438 (Systematics Association Special Series)

    Chapter  Google Scholar 

  • Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155

    Article  PubMed  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 JZ, Johnson JE (2001) Population biology and growth of Ozark cavefishes in Logan Cave National Wildlife Refuge, Arkansas. Environ Biol Fishes 62:161–169

    Article  Google Scholar 

  • Brown JH, Lomolino MV (1998) Biogeography. Sinauer Press, Sunderland

  • Cooper JE, Cooper MR (2011) Observations on the biology of the endangered stygobiotic shrimp Palaemonias alabamae, with notes on P. ganteri (Decapoda: Atyidae). Subterr Biol 8:9–20

    Google Scholar 

  • Culver DC, Pipan T (2009) The biology of caves and other subterranean habitats. Oxford University Press, Oxford

    Google Scholar 

  • Culver DC, Kane TC, Fong DW (1995) Adaptation and natural selection in caves: the evolution of Gammarus minus. Harvard University Press, London

    Google Scholar 

  • Culver DC, Master LL, Christman MC, Hobbs HH III (2000) Obligate cave fauna of the 48 contiguous United States. Conserv Biol 14:386–401

    Article  Google Scholar 

  • Dragoni W, Sukhija BS (2008) Climate change and groundwater: a short review. Geol Soc Lond 288:1–12

    Article  Google Scholar 

  • Eigenmann C (1909) Cave vertebrates of North America, a study in degenerative evolution. Carnegie Inst Wash Publ 104:1–241

    Google Scholar 

  • Elliott WR (2000) Conservation of North American cave and karst biota. In: Wilkens H, Culver DC, Humphreys WF (eds) Ecosystems of the world, vol 30., Subterranean ecosystemsElsevier, Amsterdam, pp 665–690

    Google Scholar 

  • Faber-Langendoen D, Master L, Nichols J, Snow K, Tomaino A, Bittman R, Hammerson G, Heidel B, Ramsay L, Young B (2009) NatureServe conservation status assessments: methodology for assigning ranks. NatureServe, Arlington

    Google Scholar 

  • Finston T, Johnson M, Humphreys W, Eberhard SM, Halse SA (2007) Cryptic speciation in two widespread subterranean amphipod genera reflects historical drainage patterns in an ancient landscape. Mol Ecol 16:355–365

    Article  PubMed  CAS  Google Scholar 

  • Ford D, Williams P (2007) Karst hydrogeology and geomorphology. Wiley, New York

    Book  Google Scholar 

  • Funk WC, Caminer M, Ron SR (2012) High levels of cryptic species diversity uncovered in Amazonian frogs. Proc R Soc B 279:1806–1814

    Article  PubMed  Google Scholar 

  • Gaston KJ, Fuller RA (2009) The sizes of species geographic ranges. J Appl Ecol 46:1–9

    Article  Google Scholar 

  • Gibert J, Deharveng L (2002) Subterranean ecosystems: a truncated functional biodiversity. Bioscience 52:473–481

    Article  Google Scholar 

  • Gillespie GR, Scroggie MP, Roberts JD, Cogger HG, Mahony MJ, McDonald KR (2011) The influence of uncertainty on conservation assessments: Australian frogs as a case study. Biol Conserv 144:1516–1525

    Article  Google Scholar 

  • Graening GO, Fenolio DB, Niemiller ML, Brown AV, Beard JB (2010) The 30-year recovery effort for the Ozark cavefish (Amblyopsis rosae): analysis of current distribution, population trends, and conservation status of this threatened species. Environ Biol Fishes 87:55–88

    Article  Google Scholar 

  • Holsinger JR (2000) Ecological derivation, colonization, and speciation. In: Wilkens H, Culver DC, Humphreys WF (eds) Ecosystems of the world, vol 30., Subterranean ecosystemsElsevier, Amsterdam, pp 399–415

    Google Scholar 

  • Hubbs CL, Innes WT (1936) The first known blind fish of the family Characidae: a new genus from Mexico. Occ Pap Mus Zool 342:1–7

    Google Scholar 

  • Isaac NJB, Mallet J, Mace GM (2004) Taxonomic inflation: its influence on macroecology and conservation. Trends Ecol Evol 19:464–469

    Article  PubMed  Google Scholar 

  • IUCN (2001) IUCN Red List categories, version 3.1. Prepared by IUCN Species Survival Commission. IUCN, Gland, Switzerland, and Cambridge, UK. http://www.iucnredlist.org/static/categories_criteria. Accessed 17 Jan 2013

  • IUCN (2010) Guidelines for using the IUCN Red List categories and criteria, version 8.1. Prepared by the Standards and Petitions Subcommittee in March 2010

  • Kuhajda BR, Mayden RL (2001) Status of the federally endangered Alabama cavefish, Speoplatyrhinus poulsoni (Amblyopsidae), in Key Cave and surrounding caves, Alabama. Environ Biol Fishes 62:215–222

    Article  Google Scholar 

  • Lamoreux J (2004) Stygobites are more wide-ranging than troglobites. J Cave Karst Stud 66:8–19

    Google Scholar 

  • Lewis JJ (1996) The devastation and recovery of caves affected by industrialization. In: Proceedings of the 1995 National Cave Management Symposium, pp 214–227

  • Mace GM, Collar NJ, Gaston KJ, Hilton-Taylor C, Akcakaya HR, Leader-Williams N, Milner-Gulland EJ, Stuart SN (2008) Quantification of extinction risk: IUCN’s system for classifying threatened species. Conserv Biol 22:1424–1442

    Article  PubMed  Google Scholar 

  • Master L, Faber-Langendoen D, Bittman R, Hammerson GA, Heidel B, Nichols J, Ramsay L, Tomaino A (2009) NatureServe conservation status assessments: factors for assessing extinction risk. NatureServe, Arlington

    Google Scholar 

  • Means ML, Johnson JE (1995) Movement of threatened Ozark cavefish in Logan Cave National Wildlife Refuge, Arkansas. Southwest Nat 40:308–313

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • NatureServe (2013) NatureServe explorer: an online encyclopedia of life [web application], version 7.1, NatureServe, Arlington. http://www.natureserve.org/explorer. Accessed 17 Jan 2013

  • Niemiller ML, Fitzpatrick BM (2008) Phylogenetics of the southern cavefish (Typhlichthys subterraneus): implications for conservation and management. In: Proceedings of the 18th National Cave and Karst Management Symposium, St. Louis, Missouri, pp 79–88

  • Niemiller ML, Poulson TL (2010) Studies of the Amblyopsidae: past, present, and future. In: Trajano E, Bichuette ME, Kappor BG (eds) The biology of subterranean fishes. Science Publishers, Enfield, pp 169–280

    Chapter  Google Scholar 

  • Niemiller ML, Fitzpatrick BM, Miller BT (2008) Recent divergence with gene flow in Tennessee cave salamanders (Plethodontidae: Gyrinophilus) inferred from gene genealogies. Mol Ecol 17:2258–2275

    Article  PubMed  CAS  Google Scholar 

  • Niemiller ML, Near TJ, Fitzpatrick BM (2012) Delimiting species using multilocus data: diagnosing cryptic diversity in the southern cavefish Typhlichthys subterraneus (Teleostei: Amblyopsidae). Evolution 66:846–866

    Article  PubMed  Google Scholar 

  • Niemiller ML, Fitzpatrick BM, Shah P, Schmitz L, Near TJ (2013a) Evidence for repeated loss of selective constraint in rhodopsin of amblyopsid cavefishes (Teleostei: Amblyopsidae). Evolution 67:732–748

    Article  PubMed  CAS  Google Scholar 

  • Niemiller ML, McCandless JR, Reynolds RG, Caddle J, Tillquist CR, Near TJ, Pearson WD, Fitzpatrick BM (2013b) Effects of climatic and geological processes during the Pleistocene on the evolutionary history of the northern cavefish, Amblyopsis spelaea (Teleostei: Amblyopsidae). Evolution 67:1011–1025

    Article  PubMed  Google Scholar 

  • Palmer AN (2000) Hydrogeological control of cave patterns. In: Klimchouk A, Ford DC, Palmer AN, Dreybrodt W (eds) Speleogenesis. Evolution of karst aquifers. National Speleological Society, Huntsville, pp 77–90

    Google Scholar 

  • Parenti LR (2006) Typhlichthys eigenmanni Charlton, 1933, an available name for a blind cavefish (Teleostei: Amblyopsidae), differentiated on the basis of characters of the central nervous system. Zootaxa 1374:55–59

    Google Scholar 

  • Pearson WD, Boston CH (1995) Distribution and status of the northern cavefish, Amblyopsis spelaea. Final report, Nongame and Endangered Wildlife Program, Indiana Department of Natural Resources, Indianapolis

  • Pfenninger M, Schwenk K (2007) Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evol Biol 7:121–126

    Article  PubMed  Google Scholar 

  • Poulson TL (1963) Cave adaptation in amblyopsid fishes. Am Midl Nat 70:257–290

    Article  Google Scholar 

  • Proudlove GS (2006) Subterranean fishes of the world. International Society for Subterranean Biology, Moulis

    Google Scholar 

  • Quinlan JF (1982) Groundwater basin delineation with dye-tracing, potentiometric surface mapping, and cave mapping, Mammoth Cave Region, Kentucky, USA. Beitrage zur Geologie der Schweiz Hydrologic 28:177–189

  • Quinlan JF, Ewers RO (1981) Preliminary speculations on the evolution of groundwater basins in the Mammoth Cave Region, Kentucky. In: Roberts TG (ed) GSA Cincinnati 1981 Field Trip Guidebooks 3. American Geological Institute, Washington, DC, pp 496–501

    Google Scholar 

  • Quinlan JF, Ray JA (1989) Groundwater basins in the Mammoth Cave Region, Kentucky. Friends of Karst, occasional publication no. 2. Mammoth Cave, Kentucky

  • Ryan ME, Johnson JR, Fitzpatrick BM, Lowenstine LJ, Picco AM, Shaffer HB (2013) Lethal effects of water quality on threatened California tiger salamanders but not on co-occurring hybrid salamanders. Conserv Biol 27:95–102

    Article  PubMed  Google Scholar 

  • Salafsky N, Salzer D, Stattersfield AJ, Hilton-Taylor C, Neugarten R, Butchart SHM, Collen B, Cox N, Master LL, O’Connor S, Wilkie D (2008) A standard lexicon for biodiversity conservation: unified classifications of threats and actions. Conserv Biol 22:897–911

    Article  PubMed  Google Scholar 

  • Swofford DL (1982) Genetic variability, population differentiation, and biochemical relationships in the family Amblyopsidae. Master’s Thesis, Eastern Kentucky University, Richmond

  • Treidel H, Martin-Bordes JL, Gurdak JJ (2012) Introduction. In: Treidel H, Martin-Bordes JL, Gurdak JJ (eds) Climate change effects on groundwater resources: a global synthesis of findings and recommendations. CRC Press, London, pp 1–14

    Google Scholar 

  • Trontelj P, Douady CJ, Fiser C, Gibert J, Goricki S, LeFebure T, Sket B, Zakšek V (2009) A molecular test for cryptic diversity in ground water: how large are the ranges of macro-stygobionts? Freshw Biol 54:727–744

    Article  CAS  Google Scholar 

  • Vandike JE (1982) The effects of the November 1981 liquid fertilizer pipeline break on groundwater in Phelps County, Missouri. Report for Water Resources Data and Research, Missouri Department of Natural Resources, Division of Geology and Land Survey, Rolla

  • Verovnik R, Sket B, Prevorcnik S, Trontelj P (2003) Random amplified polymorphic DNA diversity among surface and subterranean populations of Asellus aquaticus (Crustacea: Isopoda). Genetica 119:155–165

    Article  PubMed  CAS  Google Scholar 

  • Waldron A (2010) Lineages that cheat death: surviving the squeeze on range size. Evolution 64:2278–2292

    PubMed  Google Scholar 

  • White WB (1988) Geomorphology and hydrology of karst terrains. Oxford University Press, Oxford

    Google Scholar 

  • Wiens JJ, Chippindale PT, Hillis DM (2003) When are phylogenetic analyses misled by convergence? A case study in Texas cave salamanders. Syst Biol 52:501–514

    PubMed  Google Scholar 

  • World Conservation Monitoring Centre (1996) Typhlichthys subterraneus. In: IUCN 2011, IUCN Red List of threatened species, version 2011.2. http://www.iucnredlist.org. Accessed 17 Jan 2013

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Acknowledgments

This work was supported by the National Science Foundation (DEB-1011216 to M.L.N.), Tennessee Wildlife Resources Agency (Contract Nos. ED-06-02149-00 and ED-08023417-00 to M.L.N. and B.M.F.), KDFWR (Contract No. PON2 660 1000003354 to M.L.N. and B.M.F.), National Park Service (Contract No. CA353039004 and Award No. H5530010070 to W.D.P.), Cave Research Foundation (to M.L.N.), and National Speleological Society (to M.L.N.). We thank the Alabama Natural Heritage Program, Kentucky Department of Fish and Wildlife Resources (KDFWR), Missouri Speleological Survey, and the Missouri Department of Conservation, and Tennessee Cave Survey for sharing data. Many also shared data or assisted in this project including J. Armbruster, T. Barr, J. Cooper, W. Elliott, S. House, B. Kuhajda, J. Jensen, T. Jones, B. Miller, R. Olsen, T. Poulson, L. Simpson, B. Wagner, and B. Walden.

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Correspondence to Matthew L. Niemiller.

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Niemiller, M.L., Graening, G.O., Fenolio, D.B. et al. Doomed before they are described? The need for conservation assessments of cryptic species complexes using an amblyopsid cavefish (Amblyopsidae: Typhlichthys) as a case study. Biodivers Conserv 22, 1799–1820 (2013). https://doi.org/10.1007/s10531-013-0514-4

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