Biodiversity and Conservation

, Volume 25, Issue 5, pp 905–922 | Cite as

Shifting targets: spatial priorities for ex situ plant conservation depend on interactions between current threats, climate change, and uncertainty

  • Adam B. SmithEmail author
  • Quinn G. Long
  • Matthew A. Albrecht
Original Paper


Few strategies for conservation seed banking consider current and climate threats simultaneously and few—if any—represent uncertainty inherent in the assessment process. Here we evaluate the vulnerability of 5148 populations of 71 rare plant species in the North American Central Highlands to current threat, threat from climate change, and their combination. We calculated priorities based on current threat using existing conservation status and protection, and priorities based on climate threat using ecological niche models and species-level traits related to reproduction and dispersal. Current- and climate-based priorities were integrated using a weighted average of rank priority. We managed uncertainty using either a precautionary strategy that avoids any extinctions or a resource-conservative strategy that directs attention to species known to be vulnerable with high certainty. Priorities based on current threats highlighted presently rare species while priorities based on climate threat emphasized presently common species. The location of geographic “hotspots” providing opportunities for efficient seed banking depended strongly on the weight of the climate module relative to the current module, the strategy used to handle uncertainty, and emissions scenario. Integrating threats highlighted some hotspots that were not identified using just current or climate threat, indicating the importance of considering current and climate threats simultaneously. Only the Central Basin of Tennessee, a known center of endemism, was consistently emphasized. We urge (1) integrating current and climate threats when designing seed-banking strategies; and (2) reporting of uncertainty in a manner that allows decision-makers to choose actions based on available resources and tolerable risk.


Climate change vulnerability Conservation seed banking Endemism North American Central Highlands Species distribution model Uncertainty 



We thank Iván Jiménez and Sebastián Tello for helpful discussions and J. Leighton Reid for helpful comments on the manuscript. This work was funded by an Institute of Museum and Library Services National Leadership Grant (LG-25-10-0035-10). We thank NatureServe and the Tennessee Department of Environment and Conservation, Georgia Department of Natural Resources, Missouri Department of Conservation, Kentucky State Nature Preserves Commission, Alabama Natural Heritage Program, Illinois Department of Natural Resources, and Arkansas Natural Heritage Commission. Two anonymous reviewers generously helped to improve the manuscript.

Supplementary material

10531_2016_1097_MOESM1_ESM.pdf (2.1 mb)
Supplementary material 1 (PDF 2131 kb)


  1. Aizen MA, Feinsinger P (1994) Forest fragmentation, pollination, and plant reproduction in a Chaco dry forest, Argentina. Ecology 75:330–351CrossRefGoogle Scholar
  2. Anacker BL, Gogol-Prokurat M, Leidholm K, Schoenig S (2013) Climate change vulnerability assessment of rare plants in California. Madroño 60:193–210CrossRefGoogle Scholar
  3. Baskin JM, Baskin CC (2003) The vascular flora of cedar glades of the southeastern United States and its phytogeographical relationships. J Torrey Bot Soc 130:101–118CrossRefGoogle Scholar
  4. Benscoter AM, Reece JS, Noss RF, Brandt LA, Mazzotti FJ, Romañach SS, Watling JI (2013) Threatened and endangered subspecies with vulnerable ecological traits also have high susceptibility to sea level rise and habitat fragmentation. PLoS One 8:e70647CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bower AD, Clair BS, Erickson V (2014) Generalized seed transfer zones for native plants. Ecol Appl 24:913–919CrossRefPubMedGoogle Scholar
  6. Carmel Y, Stoller-Cavari L (2006) Comparing environmental and biological surrogates for biodiversity at a local scale. Isr J Ecol Evol 52:11–27CrossRefGoogle Scholar
  7. Cochrane JA, Crawford AD, Monks LT (2007) The significance of ex situ seed conservation to reintroduction of threatened plants. Aust J Bot 55:356–361CrossRefGoogle Scholar
  8. Estill JC, Cruzan MB (2001) Phytogeography of rare plant species endemic to the southeastern United States. Castanea 66:3–23Google Scholar
  9. Farnsworth EJ, Klionsky S, Brumback WE, Havens K (2006) A set of simple decision matrices for prioritizing collection of rare plant species for ex situ conservation. Biol Conserv 128:1–12CrossRefGoogle Scholar
  10. Foden WB, Butchart SHM, Stuart SN, Vié J-C, Akçakaya R, Angulo A, DeVaniter LD, Gutsche A, Turak E, Cao L, Donner SD, Katariya V, Bernard R, Hollamd RA, Hughes AF, O’Hanlon SE, Garnett ST, Şekercioğlu ÇH, Mace GM (2013) Identifying the world’s most climate change vulnerable species: a systematic trait-based assessment of all birds, amphibians and corals. PLoS One 8:e65427CrossRefPubMedPubMedCentralGoogle Scholar
  11. Gardali T, Seavy NE, DiGuadio RT, Comrack LA (2012) A climate change vulnerability assessment of California’s at-risk birds. PLoS One 7:e29507CrossRefPubMedPubMedCentralGoogle Scholar
  12. Gauthier R, Debussche M, Thompson JD (2010) Regional priority setting for rare species based on a method combining three criteria. Biol Conserv 143:1501–1509CrossRefGoogle Scholar
  13. Godefroid S, Vanderborght T (2010) Seed banking of endangered plants: Are we conserving the right species to address climate change? Biol Conserv 19:3049–3058Google Scholar
  14. Guerrant EO Jr, Havens K, Maunder M (2004) Ex situ plant conservation: supporting species survival in the wild. Island Press, WashingtonGoogle Scholar
  15. Guerrant EO Jr, Havens K, Vitt P (2014) Sampling for effective ex situ plant conservation. Int J Plant Sci 175:11–20CrossRefGoogle Scholar
  16. Havens K, Vitt P, Still S, Kramer A, Fant J, Schatz K (2015) Seed sourcing for restoration in an era of climate change. Nat Areas J 35:122–133CrossRefGoogle Scholar
  17. Hoban S, Schlarbaum S (2014) Optimal sampling of seeds from plant populations for ex situ conservation of genetic biodiversity, considering realistic population structure. Biol Conserv 177:90–99CrossRefGoogle Scholar
  18. Honnay O, Jacquemyn H (2007) Susceptibility of common and rare plant species to the genetic consequences of habitat fragmentation. Conserv Biol 21:1–9CrossRefGoogle Scholar
  19. Johnson R, Stritch L, Olwell P, Lambert S, Horning ME, Cronn R (2010) What are the best seed sources for ecosystem restoration on BLM and USFS lands? Nativ Plants J 11:117–131CrossRefGoogle Scholar
  20. Keith DA, Mahoney M, Hines H, Elith J, Regan TJ, Baumgartner JB, Hunter D, Heard GW, Mitchell NJ, Parris KM, Penman T, Scheele B, Simpson CC, Tingley R, Tracy CR, West M, Akçakaya HR (2014) Detecting extinction risk from climate change by IUCN Red List criteria. Conserv Biol 28:810–819CrossRefPubMedGoogle Scholar
  21. Kricsfalusy VV, Trevisan N (2014) Prioritizing regionally rare plant species for conservation using herbarium data. Biodivers Conserv 23:39–61CrossRefGoogle Scholar
  22. Lewandowski AS, Noss RF, Parsons DR (2010) The effectiveness of surrogate taxa for the representation of biodiversity. Conserv Biol 24:1367–1377CrossRefPubMedGoogle Scholar
  23. Lomba A, Pellissier L, Randin C, Vicente J, Horondo J, Guisan A (2010) Overcoming the rare species modeling complex: a novel hierarchical framework applied to an Iberian endemic plant. Biol Conserv 143:2647–2657CrossRefGoogle Scholar
  24. Maunder M, Havens K, Guerrant EO Jr, Falk DA (2004) Ex situ methods: a vital but underused set of conservation resources. In: Guerrant EO Jr, Havens K, Maunder M (eds) Ex situ plant conservation: supporting species survival in the wild. Island Press, Washington, pp 3–20Google Scholar
  25. Mayden RL (1987) Historical ecology and North American Highland fishes: a research program in community ecology. In: Matthews WJ, Heins DC (eds) Community and evolutionary ecology of North American stream fishes. University of Oklahoma Press, Norman, pp 210–220Google Scholar
  26. McCarthy MA (2014) Contending with uncertainty in conservation management decisions. Ann N Y Acad Sci 1322:77–91CrossRefPubMedPubMedCentralGoogle Scholar
  27. Moyle PB, Kiernan JD, Crain PK, Quiñones RM (2013) Climate change vulnerability of native and alien freshwater fishes of California: a systematic assessment approach. PLoS One 8:e63883CrossRefPubMedPubMedCentralGoogle Scholar
  28. NatureServe (2014) NatureServe explorer: an online encyclopedia of life. Version 7.1. NatureServe, Arlington, Virginia. Accessed 9 Mar 2014
  29. Noss RF (2013) Forgotten grasslands of the south. Island Press, WashingtonCrossRefGoogle Scholar
  30. Omernik JM (1987) Ecoregions of the conterminous United States. Map (scale 1:7,500,000). Ann Assoc Am Geogr 77:118–125CrossRefGoogle Scholar
  31. Pacifici M, Foden WB, Visconti P, Watson JEM, Butchart SHM, Kovacs KM, Scheffers BR, Hole DG, Martin TG, Akçakaya HR, Corlett RT, Huntley B, Brickford D, Carr JA, Hoffmann AA, Midgley GF, Pearce-Kelly P, Pearson RG, Williams SE, Willis SG, Yoing B, Rondinini C (2015) Assessing species vulnerability to climate change. Nat Clim Change 5:215–225CrossRefGoogle Scholar
  32. Pearson RG, Stanton JC, Shoemaker KT, Aiello-Lammens ME, Ersts PJ, Horning N, Fordham DA, Raxworthy CJ, Ryu HY, McNees J, Akçakaya HR (2014) Life history and spatial traits predict extinction risk due to climate change. Nat Clim Change 4:217–221CrossRefGoogle Scholar
  33. Pierson JC, Barton PS, Lane PW, Lindenmayer DB (2015) Can habitat surrogates predict the response of target species to landscape change? Biol Conserv 184:1–10CrossRefGoogle Scholar
  34. Platts PJ, Garcia RA, Hof C, Foden W, Hansen LA, Rahbek C, Burgess ND (2014) Conservation implications of omitting narrow-ranging taxa from species distribution models, now and in the future. Divers Distrib 20:1307–1320CrossRefGoogle Scholar
  35. Reece JS, Noss RF (2014) Prioritizing species by conservation value and vulnerability—a new index applied to species threatened by sea-level rise and other risks in Florida. Nat Areas J 34:31–45CrossRefGoogle Scholar
  36. Reece JS, Noss RF, Oetting J, Hoctor T, Volk, M (2013) A vulnerability assessment of 300 species in Florida: Threats from sea level rise, land use, and climate change. PloS one 8:e80658CrossRefPubMedPubMedCentralGoogle Scholar
  37. Regan HM, Ben-Haim Y, Langford B, Wilson WG, Lundburg P, Andelman SJ, Burgman MA (2005) Robust decision-making under severe uncertainty in conservation management. Ecol Appl 15:1471–1477CrossRefGoogle Scholar
  38. Shoo LP, Hoffmann AA, Garnett S, Pressey RL, Williams YM, Taylor M, Falconi L, Yates CJ, Scot JK, Alagador D, Williams SE (2013) Making decisions to conserve species under climate change. Clim Change 119:239–246CrossRefGoogle Scholar
  39. Stanton JC, Shoemaker KT, Pearson RG, Akçakaya HR (2015) Warning times for species extinctions due to climate change. Glob Change Biol 21:1066–1077CrossRefGoogle Scholar
  40. Still SM, Frances AL, Treher AC, Oliver L (2015) Using two climate change vulnerability assessment methods to prioritize and manage rare plants: a case study. Nat Areas J 35:106–121CrossRefGoogle Scholar
  41. Thomas CD, Hill JK, Anderson BJ, Bailey S, Beale CM, Bradbury RB, Bulman CR, Crick HQP, Eigenbrod F, Griffiths HM, Kunin WE, Oliver TH, Walmsley CA, Watts K, Worsfold NT, Yardley T (2011) A framework for assessing threats and benefits to species responding to climate change. Methods Ecol Evol 2:125–142CrossRefGoogle Scholar
  42. Van der Veken S, Hermy M, Vellend M, Knapen A, Verheyen K (2008) Garden plants get a head start on climate change. Front Ecol Environ 6:212–216CrossRefGoogle Scholar
  43. Vitt P, Havens K, Kramer AT, Sollenberger D, Yates E (2010) Assisted migration of plants: changes in latitudes, changes in attitudes. Biol Conserv 143:18–27CrossRefGoogle Scholar
  44. Wang T, Hamann A, Spittlehouse DL, Murdock TQ (2012) ClimateWNA—High resolution spatial climate data for Western North America. J Appl Meteorol Climatol 51:16–29CrossRefGoogle Scholar
  45. Ware S (2002) Rock outcrop plant communities (glades) in the Ozarks: a synthesis. Southwest Nat 47:585–597CrossRefGoogle Scholar
  46. Warren M, Robertson MP, Greeif JM (2010) A comparative approach to understanding factors limiting abundance patterns and distributions in a fig tree-wasp mutualism. Ecography 33:148–158CrossRefGoogle Scholar
  47. Wiegand T, Moloney KA (2014) Handbook of spatial point-pattern analysis in ecology. Taylor & Francis, Boca RatonGoogle Scholar
  48. Willis SG, Foden W, Baker DJ, Belle E, Burgess ND, Carr JA, Doswald N, Garcia RA, Hartley A, Hof C, Newbold T, Rahbek C, Smith CJ, Visconti P, Young BE, Butchart SHM (2015) Integrating climate change vulnerability assessments from species distribution models and trait-based approaches. Biol Conserv 190:167–178CrossRefGoogle Scholar
  49. Wolf AT, Harrison SP (2001) Effects of habitat size and patch isolation on reproductive success of the serpentine morning glory. Conserv Biol 15:111–121CrossRefGoogle Scholar
  50. Wright AN, Hijmans RJ, Schwartz MW, Shaffer HB (2015) Multiple sources of uncertainty affect metrics for ranking conservation risk under climate change. Divers Distrib 21:111–122CrossRefGoogle Scholar
  51. Wyse Jackson P (2008) The potential impact of climate change on native plant diversity in Ireland. National Botanic Gardens of Ireland. Accessed 1 July 2015
  52. Wyse Jackson P, Kennedy K (2009) The global strategy for plant conservation: a challenge and opportunity for the international community. Trends Plant Sci 14:578–580CrossRefPubMedGoogle Scholar
  53. Young BE, Byers E, Hammerson G, Frances A, Oliver L, Treher A (2015) Guidelines for using the natureserve climate change vulnerability index, Rlease 3.0. NatureServe, ArlingtonGoogle Scholar
  54. Zollner D, MacRoberts MH, MacRoberts BR, Ladd D (2005) Endemic vascular plants of the Interior Highlands, U.S.A. Sida 21:1781–1791Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Adam B. Smith
    • 1
  • Quinn G. Long
    • 1
  • Matthew A. Albrecht
    • 1
  1. 1.Center for Conservation & Sustainable DevelopmentMissouri Botanical GardenSaint LouisUSA

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