Population extinctions driven by climate change, population size, and time since observation may make rare species databases inaccurate


Autoři: Thomas N. Kaye aff001;  Matt A. Bahm aff001;  Andrea S. Thorpe aff001;  Erin C. Gray aff001;  Ian Pfingsten aff003;  Chelsea Waddell aff004
Působiště autorů: Institute for Applied Ecology, Corvallis, Oregon, United States of America aff001;  Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, United States of America aff002;  Nonindigenous Aquatic Species Program, Cherokee Nation Technology Solutions, Wetland and Aquatic Research Center, Gainesville, FL, United States of America aff003;  Wildlife/Botany & Fisheries/Aquatics Data Coordinator, Branch of Biological Resources, United States Bureau of Land Management, Oregon State Office, Portland, OR, United States of America aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0210378

Souhrn

Loss of biological diversity through population extinctions is a global phenomenon that threatens many ecosystems. Managers often rely on databases of rare species locations to plan land use actions and conserve at-risk taxa, so it is crucial that the information they contain is accurate and dependable. However, small population sizes, long gaps between surveys, and climate change may be leading to undetected extinctions of many populations. We used repeated survey records for a rare but widespread orchid, Cypripedium fasciculatum (clustered lady’s slipper), to model population extinction risk based on elevation, population size, and time between observations. Population size and elevation were negatively associated with extinction, while extinction probability increased with time between observations. We interpret population losses at low elevations as a potential signal of climate change impacts. We used this model to estimate the probability of persistence of populations across California and Oregon, and found that 39%-52% of the 2415 populations reported in databases from this region are likely extinct. Managers should be aware that the number of populations of rare species in their databases is potentially an overestimate, and consider resurveying these populations to document their presence and condition, with priority given to older reports of small populations, especially those at low elevations or in other areas with high vulnerability to climate or land cover change.

Klíčová slova:

California – Climate change – Conservation science – Extinction risk – Fungi – Oregon – Population size – Species extinction


Zdroje

1. Oostermeijer JGB. Threats to rare plant persistence. In: Brigham CA, Schwartz MW, editors. Population Viability in Plants: Conservation, Management, and Modeling of Rare Plants. Berlin: Springer; 2003. pp. 17–58.

2. Harrison S, Bruna E. Habitat fragmentation and large‐scale conservation: what do we know for sure? Ecography 1999;22: 225–232.

3. Kéry M, Matthies D, Spillmann H. Reduced fecundity and offspring performance in small populations of the declining grassland plants Primula veris and Gentiana lutea. J Ecol. 2000;88: 17–30.

4. Matthies D, Bräuer I, Maibom W, Tscharntke T. Population size and the risk of local extinction: empirical evidence from rare plants. Oikos 2004;105: 481–488.

5. Darwin C. On the origins of species by means of natural selection or the preservation of favoured races in the struggle for life [reprinted 1964]. Cambridge: Harvard University Press; 1859.

6. Koopowitz H. A stochastic model for the extinction of tropical orchids. Selbyana 1992;13: 115–122.

7. Solow AR. Inferring extinction from sighting data. Ecol. 1993;74: 962–964.

8. Cribb PJ, Kell SP, Dixon KW, Barrett RL. Orchid conservation: A global perspective. In: Dixon KW, Kell SP, Barrett RL, Cribb PJ, editors. Orchid conservation. Kota Kinabalu: Natural History Publications; 2003. pp. 1–24.

9. Solow AR, Roberts DL. A nonparametric test for extinction based on a sighting record. Ecol. 2003;84: 1329–1332.

10. Pokorny J, Raynal-Roques A, Roguenant A, Prat D. Degree of threat of extinction and causes of disappearance, of the Orchidaceae in the Sudeten Mountains (Poland). In: Raynal-Roques A, Roguenant A, Prat D. editor, Proceedings of the 18th World Orchid Conference. Turreirs: Naturalia Publications; 2005. pp. 399–402.

11. Duffy KJ, Kingston NE, Sayers BA, Roberts DL, Stout JC. Inferring national and regional declines of rare orchid species with probabilistic models. Conserv Biol. 2009;23: 184–195. doi: 10.1111/j.1523-1739.2008.01064.x 18798858

12. Swarts ND, Dixon KW. Terrestrial orchid conservation in the age of extinction. Ann Bot. 2009;104: 543–556. doi: 10.1093/aob/mcp025 19218582

13. Pierce S, Ceriani RM, Villa M, Cerabolini B. Quantifying relative extinction risks and targeting intervention for the orchid flora of a natural park in the European Prealps. Conserv Biol. 2006;20: 1804–1810. doi: 10.1111/j.1523-1739.2006.00539.x 17181816

14. Cribb P, Sandison MS. A preliminary assessment of the conservation status of Cypripedium species in the wild. Bot J Linn Soc. 1998;126: 183–190.

15. Schemske DW, Husband BC, Ruckelshaus MH, Goodwillie C, Parker IM, Bishop JG. Evaluating approaches to the conservation of rare and endangered plants. Ecol. 1994;75: 584–606.

16. Lawler JJ, Campbell SP, Guerry AD, Kolozsvary MB, O'Connor RJ, Seward LC. The scope and treatment of threats in endangered species recovery plans. Ecol Appl. 2002;12: 663–667.

17. Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E. Quantifying threats to imperiled species in the United States. BioSci. 1998;48: 607–615.

18. Parmesan C. Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst. 2006;37: 637–669.

19. Parmesan C, Yohe G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 2003;421: 37–42. doi: 10.1038/nature01286 12511946

20. Chen IC, Hill JK, Ohlemüller R, Roy DB, Thomas CD. Rapid range shifts of species associated with high levels of climate warming. Science 2011;333: 1024–1026. doi: 10.1126/science.1206432 21852500

21. Lenoir J, Gégout JC, Marquet PA, De Ruffray P, Brisse H. A significant upward shift in plant species optimum elevation during the 20th century. Science 2008;320: 1768–1771. doi: 10.1126/science.1156831 18583610

22. Kelly AE, Goulden ML. Rapid shifts in plant distribution with recent climate change. Proc Natl Acad Sci U S A. 2008;105: 11823–11826. doi: 10.1073/pnas.0802891105 18697941

23. Thuiller W, Lavorel S, Araújo MB, Sykes MT, Prentice IC. Climate change threats to plant diversity in Europe. Proc Natl Acad Sci U S A. 2005;102: 8245–8250. doi: 10.1073/pnas.0409902102 15919825

24. Colwell RK, Brehm G, Cardelús CL, Gilman AC, Longino JT. Global warming, elevational range shifts, and lowland biotic attrition in the wet tropics. Science 2008;322: 258–261. doi: 10.1126/science.1162547 18845754

25. Caswell H. Matrix Population Models. Sunderland: Sinauer Associates; 1989.

26. Morris WF, Doak DF Quantitative conservation biology: theory and practice of population viability analysis. Sunderland: Sinauer Associates; 2002.

27. Eisto AK, Kuitunen M, Lammi A, Saari V, Suhonen J, Syrjäsuo S, Tikka PM. Population persistence and offspring fitness in the rare bellflower Campanula cervicaria in relation to population size and habitat quality. Conserv Biol. 2000;14: 1413–1421.

28. Berec L, Angulo E, Courchamp F. Multiple Allee effects and population management. Trends Ecol Evol. 2007;22: 185–191. doi: 10.1016/j.tree.2006.12.002 17175060

29. Thorpe AS, Kaye TN. Conservation and reintroduction of the endangered Willamette daisy: effects of population size on seed viability and the influence of local adaptation. Native Plants J. 2011;12: 289–298.

30. Menges ES. Seed germination percentage increases with population size in a fragmented prairie species. Conserv Biol. 1991;5: 158–164.

31. Fischer M, Matthies D. Effects of population size on performance in the rare plant Gentianella germanica. J Ecol. 1998;86: 195–204.

32. Paland S, Schmid B. Population size and the nature of genetic load in Gentianella germanica. Evol. 2003;57: 2242–2251.

33. Lande R. Risks of population extinction from demographic and environmental stochasticity and random catastrophes. Am Nat. 1993;142: 911–927. doi: 10.1086/285580 29519140

34. Fischer M, Stöcklin J. Local extinctions of plants in remnants of extensively used calcareous grasslands 1950–1985. Conserv Biol. 1997;11: 727–737.

35. NatureServe. NatureServe Explorer: An online encyclopedia of life [web application]. Version 7.1. NatureServe, Arlington, Virginia. 2017. Available http://explorer.natureserve.org., Cited 21 February 2018.

36. Kaye TN, Cramer JR. Conservation Assessment for Cypripedium fasciculatum and Cypripedium montanum. Sacramento: USDA Forest Service, Region 5. 2005. Available from: https://appliedeco.org/wp-content/uploads/cypripedium_ca_2005_final1.pdf

37. Shefferson RP, Weiss M, Kull T, Taylor DL. High specificity generally characterizes mycorrhizal association in rare lady’s slipper orchids, genus Cypripedium. Mol Ecol. 2005;14: 613–626. doi: 10.1111/j.1365-294X.2005.02424.x 15660950

38. Gray E.C., Kaye T.N., and Thorpe A.S. Population viability analysis for the clustered lady’s slipper (Cypripedium fasciculatum). Institute for Applied Ecology, 2012. Available from: https://appliedeco.org/wp-content/uploads/CYFA-2012-report.pdf.

39. Nicole F, Brzosko E, TILL‐BOTTRAUD IRÈNE. Population viability analysis of Cypripedium calceolus in a protected area: longevity, stability and persistence. J Ecol. 2005;93: 716–726.

40. Venables WN, Ripley BD. Modern applied statistics with S. New York: Springer; 2002.

41. Sakamoto Y, Ishiguro M, Kitagawa G. Akaike information criterion statistics. D. Reidel Publishing Company; 1986.

42. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2019: Available from https://www.R-project.org/.

43. Efron B, Tibshirani R. An introduction to the bootstrap. Chapman & Hall Press; 1993.

44. Gillman MP, Dodd ME. The variability of orchid population size. Bot J Linn Soc. 1998;126: 65–74.

45. IUCN Red List of Threatened Species, Cypripedium kentuckiense (Kentucky Lady's Slipper, Southern Lady's Slipper, Southern Yellow Lady's Slipper). https://doi.org/10.2305/IUCN.UK.2014-1.RLTS.T13254117A13254142.en Cited 9 December 2016.

46. Alexandersson R, Ågren J. Population size, pollinator visitation and fruit production in the deceptive orchid Calypso bulbosa. Oecologia 1996;107: 533–540. doi: 10.1007/BF00333945 28307397

47. Johnson SD, Torninger E, Ågren J. Relationships between population size and pollen fates in a moth-pollinated orchid. Biol Lett. 2009;5: 282–285. doi: 10.1098/rsbl.2008.0702 19324662

48. Jacquemyn H, Vandepitte K, Brys R, Honnay O, Roldán-Ruiz I. Fitness variation and genetic diversity in small, remnant populations of the food deceptive orchid Orchis purpurea. Biol Conserv. 2007;139: 203–210.

49. Chung MY, Nason JD, Chung MG. Implications of clonal structure for effective population size and genetic drift in a rare terrestrial orchid, Cremastra appendiculata. Conserv Biol. 2004;18: 1515–1524.

50. Jacquemyn H, Brys R, Adriaens D, Honnay O, Roldán-Ruiz I. Effects of population size and forest management on genetic diversity and structure of the tuberous orchid Orchis mascula. Conserv Genet. 2009;10: 161–168.

51. Devillers-Terschuren J. Action plan for Cypripedium calceolus in Europe. Nature and Environment, no. 100. Strasbourg: Council of Europe Publishing; 1992.

52. Wilson RJ, Gutiérrez D, Gutiérrez J, Martínez D, Agudo R, Monserrat VJ. Changes to the elevational limits and extent of species ranges associated with climate change. Ecol Lett. 2005;8: 1138–1146. doi: 10.1111/j.1461-0248.2005.00824.x 21352437

53. Willis CG, Ruhfel B, Primack RB, Miller-Rushing AJ, Davis CC. Phylogenetic patterns of species loss in Thoreau's woods are driven by climate change. Proc Natl Acad Sci U S A. 2008;105: 17029–17033. doi: 10.1073/pnas.0806446105 18955707

54. Soto-Arenas M, Gómez RS, Hágsater E. Risk of extinction and patterns of diversity loss in Mexican orchids. Lankesteriana 2007;7: 1–2.

55. Liu H, Feng CL, Luo YB, Chen BS, Wang ZS, Gu HY. Potential challenges of climate change to orchid conservation in a wild orchid hotspot in southwestern China. Bot Rev. 2010;76: 174–192.

56. Lavergne S, Molina J, Debussche M. Fingerprints of environmental change on the rare Mediterranean flora: A 115‐year study. Glob Chang Biol. 2006;12: 1466–1478.

57. Kéry M, Gregg KB. Demographic analysis of dormancy and survival in the terrestrial orchid Cypripedium reginae. J Ecol. 2004;92: 686–695.

58. Mann EM, Gleich PH. Climate change and California drought in the 21st century. Proc Natl Acad Sci U S A. 2015;112: 3858–3859. doi: 10.1073/pnas.1503667112 25829537

59. Vogt-Schilb H, Munoz F, Richard F, Schatz B. Recent declines and range changes of orchids in Western Europe (France, Belgium and Luxembourg). Biol. Conserv. 2015;190: 133–141.

60. Payne R. J., Dise N. B., Field C. D., Dore A. J., Caporn S. J., & Stevens C. J. (2017). Nitrogen deposition and plant biodiversity: past, present, and future. Front Ecol Environ. 2017;15: 431–436.

61. Harrison S, Maron J, Huxel G. Regional turnover and fluctuation in populations of five plants confined to serpentine seeps. Conserv Biol. 2000;14: 769–779.

62. Wiegmann SM, Waller DM. Fifty years of change in northern upland forest understories: identity and traits of “winner” and “loser” plant species. Biol Conserv. 2006;129: 109–123.

63. Damschen EI, Harrison S, Grace JB. Climate change effects on an endemic‐rich edaphic flora: resurveying Robert H. Whittaker's Siskiyou sites (Oregon, USA). Ecol. 2010;91: 3609–3619. doi: 10.1890/09-1057.1 21302832

64. Waller DM, Amatangelo KL, Johnson S, Rogers DA. Wisconsin Vegetation Database–plant community survey and resurvey data from the Wisconsin Plant Ecology Laboratory. Biodivers Ecol. 2012;4: 255–264.

65. Kéry M, Spillmann JH, Truong C, Holderegger R. How biased are estimates of extinction probability in revisitation studies? J Ecol. 2006;94: 980–986.

66. Chen G, Kéry M, Zhang J, Ma K. Factors affecting detection probability in plant distribution studies. J Ecol. 2009;97: 1383–1389.

67. Tingley MW, Beissinger SR. Detecting range shifts from historical species occurrences: New perspectives on old data. Trends Ecol Evol. 2009;24: 625–633. doi: 10.1016/j.tree.2009.05.009 19683829

68. Kull T. Population dynamics of north temperate orchids. In: Kull T, Arditti J, editors. Orchid Biology: Reviews and Perspecitves, VIII. Dordrecht: Kluwer Academic Publishers; 2002. pp. 139–165.

69. Cochran ME, Ellner S. Simple methods for calculating age-based life history parameters for stage-structured populations. Ecol Monogr. 1992;62: 345–364.

70. Shefferson RP, Sandercock BK, Proper J, Beissinger SR Estimating dormancy and survival of a rare herbaceous perennial using mark–recapture models. Ecol. 2001;82: 145–156.

71. Shefferson RP, Proper J, Beissinger SR, Simms EL. Life history trade-offs in a rare orchid: the costs of flowering, dormancy, and sprouting. Ecol. 2003;84: 1199–1206.

72. Brzosko E. Dynamics of island populations of Cypripedium calceolus in the Biebrza River valley (north-east Poland). Bot J Linn Soc. 2002;139: 67–77.

73. Shefferson RP. Survival costs of adult dormancy and the confounding influence of size in lady's slipper orchids, genus Cypripedium. Oikos 2006;115: 253–262.

74. Kaye TN. Timber harvest and Cypripedium montanum: Results of a long-term study on the Medford District BLM. Institute for Applied Ecology, Corvallis, Oregon. 1999. Available from: http://appliedeco.org/wp-content/uploads/cypripedium_montanum_logging.pdf

75. Shefferson R. P., Tali K., 2007. Dormancy is associated with decreased adult survival in the burnt orchid, Neotinea ustulata. J Ecol. 2007;95: 217–225.

76. Rock‐Blake R, McCormick MK, Brooks HE, Jones CS, Whigham DF. Symbiont abundance can affect host plant population dynamics. Am J Bot. 2017;104: 72–82. doi: 10.3732/ajb.1600334 28062407

77. Correll DS. Native orchids of North America north of Mexico. Standford: Stanford University Press; 1978.

78. McCormick MK, Whigham DF, O’Neill J. Mycorrhizal diversity in photosynthetic terrestrial orchids. New Phytol. 2004;163: 425–438.

79. Shefferson RP, Mizuta R, Hutchings MJ. Predicting evolution in response to climate change: the example of sprouting probability in three dormancy-prone orchid species. R Soc Open Sci. 2017;4: 160647. https://doi.org/10.1098/rsos.160647 28280565

80. McLachlan JS, Hellmann JJ, Schwartz MW. A framework for debate of assisted migration in an era of climate change. Conserv Biol. 2007;21: 297–302. doi: 10.1111/j.1523-1739.2007.00676.x 17391179

81. Vitt P, Havens K, Kramer AT, Sollenberger D, Yates E. Assisted migration of plants: Changes in latitudes, changes in attitudes. Biological Conserv. 2010;143: 18–27.

82. Hällfors MH, Aikio S, Schulman LE. Quantifying the need and potential of assisted migration. Biological Conserv. 2017;205: 34–41.

83. Ramsay MM, Stewart J. Re‐establishment of the lady's slipper orchid (Cypripedium calceolus L.) in Britain. Bot J Linn Soc. 1998;126: 173–181.

84. Huber AG. Mountain Lady’s Slipper (Cypripedium montanum): Establishment from seeds in forest openings. Native Plants J. 2002;3: 151–154.

85. Yan N, Hu H, Huang JL, Xu K, Wang H, Zhou ZK. Micropropagation of Cypripedium flavum through multiple shoots of seedlings derived from mature seeds. Plant Cell Tissue Organ Cult. 2006;84: 114–118.

86. Kranabetter JM, Stoehr M, O'Neill GA. Ectomycorrhizal fungal maladaptation and growth reductions associated with assisted migration of Douglas‐fir. New Phytol. 2015;206: 1135–1144. doi: 10.1111/nph.13287 25623442


Článek vyšel v časopise

PLOS One


2019 Číslo 10