, Volume 191, Issue 4, pp 931–944 | Cite as

Inferences of environmental and biotic effects on patterns of eukaryotic alpha and beta diversity for the spring systems of Ash Meadows, Nevada

  • Elizabeth L. PaulsonEmail author
  • Andrew P. Martin
Community ecology – original research


Freshwater springs are important ecosystems. In the arid regions of North America, groundwater extraction has caused the desiccation of springs and the extinction of taxa. To better describe the biodiversity of freshwater springs in the hope of establishing a sensitive approach for monitoring the predicted change in spring systems, we used high-resolution genetic methods to estimate the alpha and beta diversity of 19 springs and two reservoirs within the Ash Meadows National Wildlife Refuge in southwestern Nevada. We discovered a large number of distinct taxa based on eukaryote ribosomal gene sequences and show water temperature, spring size, and the presence or absence of non-native predators predicts alpha diversity, and temperature predicts beta diversity. Our study highlights how DNA data support inferences of environmental factors influencing community diversity and demonstrates the method may be an important tool for monitoring ecological communities.


Alpha diversity Beta diversity Eukaryotes Ecological communities Groundwater springs 



Funding was provided by a departmental Graduate Student Research Grant. Thanks to Ash Meadows National Wildlife Refuge for permitting sampling of springs. Thanks also to Cristi Baldino, Darrick Weissenfluh, Will Thomas, Jon Leff, Joey Knelman, Jessica Henley, Noah Fierer, Diana Nemergut, Kendi Davies, Nolan Kane, and the Martin Lab group. We are especially grateful for the reviews provided by Leon Barmuta, Joel Trexler, and two anonymous reviewers; their knowledge and attention to detail greatly improved our paper. All remaining errors and omissions are attributable to the authors.

Author contribution statement

ELP and APM conceived of and designed the study. ELP performed the fieldwork and lab work. ELP and APM conducted analyses and wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. Abele SL (ed) (2011) Nevada springs conservation plan. The Nature Conservancy, RenoGoogle Scholar
  2. Agostinho AA, Zalewski M (1995) The dependence of fish community structure and dynamics on floodplain and riparian ecotone zone in Parana River, Brazil. Hydrobiologia 303:141–148. CrossRefGoogle Scholar
  3. Amaral-Zettler LA, McCliment EA, Ducklow HW, Huse SM (2009) A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS One 4:e6372. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Baas Becking L (1934) Geobiologie of inleiding tot de milieukunde. W.P. Van Stockum & Zoon N.V, Den HagueGoogle Scholar
  5. Bangyeekhun E, Ryynänen H, Henttonen P et al (2001) Sequence analysis of the ribosomal internal transcribed spacer DNA of the crayfish parasite Psorospermium haeckeli. Dis Aquat Organ 46:217–222. CrossRefPubMedGoogle Scholar
  6. Bogan MT, Noriega-Felix N, Vidal-Aguilar SL et al (2014) Biogeography and conservation of aquatic fauna in spring-fed tropical canyons of the southern Sonoran Desert, Mexico. Biodivers Conserv 23:2705–2748. CrossRefGoogle Scholar
  7. Bradford TM, Morgan MJ, Lorenz Z et al (2013) Microeukaryote community composition assessed by pyro sequencing is associated with light availability and phytoplankton primary production along a lowland river. Freshw Biol 58:2401–2413. CrossRefGoogle Scholar
  8. Bråte J, Logares R, Berney C et al (2010) Freshwater Perkinsea and marine-freshwater colonizations revealed by pyrosequencing and phylogeny of environmental rDNA. ISME J 4:1144–1153. CrossRefPubMedGoogle Scholar
  9. Burnham KP, Anderson DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304. CrossRefGoogle Scholar
  10. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Carignan V, Villard M-A (2002) Selecting indicator species to monitor ecological integrity: a review. Environ Monit Assess 78:45–61CrossRefGoogle Scholar
  12. Cayan DR, Das T, Pierce DW et al (2010) Future dryness in the southwest US and the hydrology of the early 21st century drought. Proc Natl Acad Sci 107:21271–21276. CrossRefPubMedGoogle Scholar
  13. Charvet S, Vincent WF, Comeau A, Lovejoy C (2012) Pyrosequencing analysis of the protist communities in a high arctic meromictic lake: DNA preservation and change. Front Microbiol 3:1–14. CrossRefGoogle Scholar
  14. Clarke KR, Ainsworth M (1993) A method of linking multivariate community structure to environmental variables. Mar Ecol Prog Ser 92:205–219CrossRefGoogle Scholar
  15. Contreras-Balderas S, Lozano-Vilano M (1996) Extinction of most Sandia and Potosí valleys (Nuevo León, Mexico) endemic pupfishes, crayfishes and snails. Ichtyological Explor Freshw 7:33–40Google Scholar
  16. Dallas T (2014) Metacom: an R package for the analysis of metacommunity structure. Ecography 37:402–405. CrossRefGoogle Scholar
  17. Davis J, Kerezsy A, Nicol S (2017) Springs: conserving perennial water is critical in arid landscapes. Biol Conserv 211:30–35. CrossRefGoogle Scholar
  18. Deacon JE, Williams CD (1991) Ash meadows and the legacy of the Devils hole pupfish. In: Minckley CO, Deacon JE (eds) Battle against extinction: native fish management in the American West. University of Arizona Press, Tucson, pp 69–92Google Scholar
  19. Deacon JE, Williams AE, Williams CD, Williams JE (2007) Fueling population growth in Las Vegas: how large-scale groundwater withdrawal could burn regional biodiversity. Bioscience 57:688–698. CrossRefGoogle Scholar
  20. Debroas D, Hugoni M, Domaizon I (2015) Evidence for an active rare biosphere within freshwater protists community. Mol Ecol 24:1236–1247. CrossRefPubMedGoogle Scholar
  21. Debroas D, Domaizon I, Humbert J-F et al (2017) Overview of freshwater microbial eukaryotes diversity: a first analysis of publicly available metabarcoding data. FEMS Microbiol Ecol 93:1–14. CrossRefGoogle Scholar
  22. Delong MD, Brusven MA (1998) Macroinvertebrate community structure along the longitudinal gradient of an agriculturally impacted stream. Environ Manag 22:445–457CrossRefGoogle Scholar
  23. Dudgeon D, Arthington AH, Gessner MO et al (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81:163–182. CrossRefPubMedGoogle Scholar
  24. Dudley W, Larsen J (1976) Effect of irrigation pumping on desert pupfish habitats in Ash Meadows. Nye County, NevadaGoogle Scholar
  25. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Elmore AJ, Manning SJ, Mustard JF, Craine JM (2006) Decline in alkali meadow vegetation cover in California: the effects of groundwater extraction and drought. J Appl Ecol 43:770–779. CrossRefGoogle Scholar
  27. Finlay BJ, Maberly SC, Cooper JI (1997) Microbial diversity and ecosystem function. Oikos 80:209–213CrossRefGoogle Scholar
  28. Freeman KR, Martin AP, Karki D et al (2009) Evidence that chytrids dominate fungal communities in high-elevation soils. Proc Natl Acad Sci 106:18315–18320. CrossRefPubMedGoogle Scholar
  29. Friberg N, DybkjÆr JB, Olafsson JS et al (2009) Relationships between structure and function in streams contrasting in temperature. Freshw Biol 54:2051–2068. CrossRefGoogle Scholar
  30. Glennon R (2002) The tourist’s mirage—San Antonio’s river walk, the Edwards aquifer, and endangered species. In: Glennon R (ed) Water follies: groundwater pumping and the fate of America’s fresh waters. Island Press, Washington DC, pp 87–97Google Scholar
  31. Green J, Bohannan BJM (2006) Spatial scaling of microbial biodiversity. Trends Ecol Evol 21:501–507. CrossRefPubMedGoogle Scholar
  32. Haag WR, Warren ML (1998) Role of ecological factors and reproductive strategies in structuring freshwater mussel communities. Can J Fish Aquat Sci 55:297–306CrossRefGoogle Scholar
  33. Hahn MW (2006) The microbial diversity of inland waters. Curr Opin Biotechnol 17:256–261. CrossRefPubMedGoogle Scholar
  34. Hansel-Welch N, Butler MG, Carlson TJ, Hanson MA (2003) Changes in macrophyte community structure in Lake Christina (Minnesota), a large shallow lake, following biomanipulation. Aquat Bot 75:323–337. CrossRefGoogle Scholar
  35. Hershler R, Liu H-P, Bradford C (2013) Systematics of a widely distributed western North American springsnail, Pyrgulopsis micrococcus (Caenogastropoda, Hydrobiidae), with descriptions of three new congeners. Zookeys 330:27–52. CrossRefGoogle Scholar
  36. Hershler R, Liu H-P, Howard J (2014) Springsnails: a new conservation focus in western North America. Bioscience 64:693–700. CrossRefGoogle Scholar
  37. Hunter ML, Acuña V, Marie D et al (2017) Conserving small natural features with large ecological roles: a synthetic overview. Biol Conserv 211:88–95. CrossRefGoogle Scholar
  38. Jackson RB, Carpenter SR, Clifford ND et al (2001) Water in a changing world. Ecol Appl 11:1027–1045.;2 CrossRefGoogle Scholar
  39. Korbel KL, Hancock PJ, Serov P, Lim RP, Hose GC (2013) Groundwater ecosystems vary with land use across a mixed agricultural landscape. J Environ Qual 42:380–390. CrossRefPubMedGoogle Scholar
  40. Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. Proc Natl Acad Sci 103:11211–11216. CrossRefPubMedGoogle Scholar
  41. Leibold MA, Mikkelson GM (2002) Coherence, species turnover, and boundary clumping: elements of meta-community structure. Oikos 97:237–250CrossRefGoogle Scholar
  42. Lougheed VL, Crosbie B, Chow-Fraser P (2001) Primary determinants of macrophyte community structure in 62 marshes across the Great Lakes basin: latitude, land use, and water quality effects. Can J Fish Aquat Sci 58:1603–1612. CrossRefGoogle Scholar
  43. Mangot J-F, Domaizon I, Taib N et al (2013) Short-term dynamics of diversity patterns: evidence of continual reassembly within lacustrine small eukaryotes. Environ Microbiol 15:1745–1758. CrossRefPubMedGoogle Scholar
  44. McCreary NJ (1991) Competition as a mechanism of submersed macrophyte community structure. Aquat Bot 41:177–193. CrossRefGoogle Scholar
  45. Meerhoff M, Clemente JM, de Mello FT et al (2007) Can warm climate-related structure of littoral predator assemblies weaken the clear water state in shallow lakes? Glob Chang Biol 13:1888–1897. CrossRefGoogle Scholar
  46. Meinzer OE (1923) Outline of ground-water hydrology, with definitionsGoogle Scholar
  47. Mihaljevic JR, Joseph MB, Johnson PTJ (2015) Using multispecies occupancy models to improve the characterization and understanding of metacommunity structure. Ecology 96:1783–1792. CrossRefPubMedGoogle Scholar
  48. Milner AM, Robertson AL, Monaghan KA et al (2008) Colonization and development of an Alaskan stream community over 28 years. Front Ecol Environ 6:413–419. CrossRefGoogle Scholar
  49. Monchy S, Sanciu G, Jobard M et al (2011) Exploring and quantifying fungal diversity in freshwater lake ecosystems using rDNA cloning/sequencing and SSU tag pyrosequencing. Environ Microbiol 13:1433–1453. CrossRefPubMedGoogle Scholar
  50. Morrison RR, Stone MC, Sada DW (2013) Environmental response of a desert springbrook to incremental discharge reductions, death Valley National Park, California, USA. J Arid Environ 99:5–13. CrossRefGoogle Scholar
  51. Nolte V, Pandey RV, Jost S et al (2010) Contrasting seasonal niche separation between rare and abundant taxa conceals the extent of protist diversity. Mol Ecol 19:2908–2915. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Oksanen J, Blanchet FG, Kindt R et al (2011) Vegan: community ecology packageGoogle Scholar
  53. Paulson EL, Martin AP (2014) Discerning invasion history in an ephemerally connected system: landscape genetics of Procambarus clarkii in Ash Meadows, Nevada. Biol Invasions 16:1719–1734. CrossRefGoogle Scholar
  54. Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. CrossRefPubMedPubMedCentralGoogle Scholar
  55. R Core Team (2018) R: a language and environment for statistical computingGoogle Scholar
  56. Röhl O, Peršoh D, Mittelbach M et al (2017) Distinct sensitivity of fungal freshwater guilds to water quality. Mycol Prog 16:155–169. CrossRefGoogle Scholar
  57. Ruhí A, Chappuis E, Escoriza D et al (2014) Environmental filtering determines community patterns in temporary wetlands: a multi-taxon approach. Hydrobiologia 723:25–39. CrossRefGoogle Scholar
  58. Schlosser IJ (1982) Fish community structure and function along two habitat gradients in a headwater stream. Ecol Monogr 52:395–414CrossRefGoogle Scholar
  59. Seager R, Ting M, Held I et al (2007) Model projections of an imminent transition to a more arid climate in southwestern North America. Science (80-) 316:1181–1184. CrossRefGoogle Scholar
  60. Sharp CE, Brady AL, Sharp GH et al (2014) Humboldt’s spa: microbial diversity is controlled by temperature in geothermal environments. ISME J 8:1166–1174. CrossRefGoogle Scholar
  61. Shepard WD (1993) Desert springs—both rare and endangered. Aquat Conserv Mar Freshw Ecosyst 3:351–359CrossRefGoogle Scholar
  62. Shepard WD, Blinn DW, Hoffman RJ, Kantz PT (2000) Algae of devils hole, Nevada, death valley National Park. West N Am Nat 60:410–419Google Scholar
  63. Sohlberg E, Bomberg M, Miettinen H et al (2015) Revealing the unexplored fungal communities in deep groundwater of crystalline bedrock fracture zones in Olkiluoto, Finland. Front Microbiol 6:1–11. CrossRefGoogle Scholar
  64. Soltz DL, Naiman RJ (1978) The natural history of native fishes in the Death Valley system. Natural History Museum of Los Angeles, Los AngelesGoogle Scholar
  65. Stevens LE, Bailowitz RA (2008) Odonata of ash meadows national wildlife refuge, Southern Nevada, USA. J Ariz-Nev Acad Sci 40:128–135CrossRefGoogle Scholar
  66. Stevens LE, Meretsky VJ (eds) (2008) Aridland springs in North America: ecology and conservation. University of Arizona Press, TucsonGoogle Scholar
  67. Stoeck T, Breiner H-W, Filker S et al (2014) A morphogenetic survey on ciliate plankton from a mountain lake pinpoints the necessity of lineage-specific barcode markers in microbial ecology. Environ Microbiol 16:430–444. CrossRefPubMedGoogle Scholar
  68. Strickler KM, Fremier AK, Goldberg CS (2015) Quantifying effects of UV-B, temperature, and pH on eDNA degradation in aquatic microcosms. Biol Conserv 183:85–92. CrossRefGoogle Scholar
  69. Tang CQ, Leasi F, Obertegger U et al (2012) The widely used small subunit 18S rDNA molecule greatly underestimates true diversity in biodiversity surveys of the meiofauna. Proc Natl Acad Sci 109:16208–16212. CrossRefPubMedGoogle Scholar
  70. Thomas JM, Moser DP, Fisher JC et al (2013) Using water chemistry, isotopes and microbiology to evaluate groundwater sources, flow paths and geochemical reactions in the Death Valley flow system, USA. Procedia Earth Planet Sci 7:842–845. CrossRefGoogle Scholar
  71. Torstensson A, Dinasquet J, Chierici M et al (2015) Physicochemical control of bacterial and protist community composition and diversity in Antarctic sea ice. Environ Microbiol 17:3869–3881. CrossRefPubMedGoogle Scholar
  72. Unmack PJ, Minckley WL (2008) The demise of desert springs. In: Meretsky VJ, Stevens LE (eds) Aridland springs in North America: ecology and conservation. The University of Arizona Press, Tucson, pp 12–34Google Scholar
  73. Vaughn CC, Nichols SJ, Spooner DE (2008) Community and foodweb ecology of freshwater mussels. J N Am Benthol Soc 27:409–423. CrossRefGoogle Scholar
  74. Vörösmarty CJ, McIntyre PB, Gessner MO et al (2010) Global threats to human water security and river biodiversity. Nature 467:555–561. CrossRefPubMedGoogle Scholar
  75. Walker GE, Eakin TE (1963) Geology and ground water of Amargosa Desert, Nevada-CaliforniaGoogle Scholar
  76. Walther G-R, Post E, Convey P et al (2002) Ecological responses to recent climate change. Nature 416:389–395. CrossRefGoogle Scholar
  77. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. CrossRefPubMedPubMedCentralGoogle Scholar
  78. Welborn GA, Skelly DK, Werner EE (1996) Mechanisms creating community structure across a freshwater habitat gradient. Annu Rev Ecol Syst 27:337–363CrossRefGoogle Scholar
  79. Winograd IJ, Thordarson W (1975) Hydrogeologic and hydrochemical framework, south-central Great Basin, Nevada-California, with special reference to the Nevada Test SiteGoogle Scholar
  80. Zektser S, Loáiciga HA, Wolf JT (2005) Environmental impacts of groundwater overdraft: selected case studies in the southwestern United States. Environ Geol 47:396–404. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA

Personalised recommendations