Abstract
As the world’s biodiversity is increasingly threatened by destruction and/or climate change, rare species reintroductions may be necessary to conserve species threatened with extinction. When ecological processes change or a species’ range is heavily fragmented, it may be difficult to determine microsite characteristics needed for a successful reintroduction. In such cases, experimental reintroductions can be used to learn more about the species’ reproductive niche while establishing new self-sustaining populations. We reintroduced the Florida endangered species, Tephrosia angustissima var. corallicola, to examine native microsite requirements and feasibility of reintroduction into nearby suitable habitat. We transplanted Tephrosia into three microsites with varying light and substrate and characterized their wet and dry season soil moisture, soil bulk density, and light conditions. We monitored transplant and recruited seedling growth, reproduction, and survival and seedling germination in each microsite for 6 years. The microsite supporting greatest survival changed across developmental stages and time. Although no original transplants survived to 2009, the reintroduced population persists in 2015 through recruitment. Highest recruit growth, flowering, and survival occurred in shady, dry microsites. Recruits germinated more in the wettest microsite, reproduced most in the driest, and persisted longest in the wettest. Recruits germinated in shadier locations than where adults were planted. Although assessing whether a reintroduction is self-sustaining will require decades of monitoring, this experimental reintroduction elucidated the necessity for heterogeneous microsites at recipient sites and the efficacy of planting reproductive individuals for rapid next generation recruitment. Determining appropriate microsites for species requiring human assisted migration may also benefit from these techniques.
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References
Albrecht MA, McCue KA (2010) Changes in demographic processes over long time scales reveal the challenge of restoring an endangered plant. Restor Ecol 18(S2):235–243. doi:10.1111/j.1526-100X.2009.00584.x
Albrecht MA, Guerrant EO Jr, Kennedy K, Maschinski J (2011) A long-term view of rare plant reintroduction. Biol Conserv 144:2557–2558. doi:10.1016/j.biocon.2011.07.021
Baeten L, Jacquemyn H, van Calster H, van Beek E, Devlaeminck R, Verheyen K, Hermy M (2009) Low recruitment across life stages partly accounts for the slow colonization of forest herbs. J Ecol 97(1):109–117. doi:10.1111/j.1365-2745.2008.01455.x
Beyra Matos A (1998) Las Leguminosas (Fabaceae) de Cuba, II. Tribus Crotalarieae, Aeschynoimeneae, Millettieae y Robinieae. Institute Botanica. Collectanea Botanica 24(1998):149–332
Brauns M, Gucker B, Wagner C, Garcia X-F, Walz N, Pusch MT (2011) Human lakeshore development alters the structure and trophic basis of littoral food webs. J Appl Ecol 48(4):916–925. doi:10.1111/j.1365-2664.2011.02007.x
Bullied WJ, Van Acker RC, Bullock PR (2012) Review: microsite characteristics influencing weed seedling recruitment and implications for recruitment modeling. Can J Plant Sci 92:627–650. doi:10.4141/CJPS2011-281
Clark JT, Poulsen JR, Levey DJ, Osenberg CW (2007) Are plant populations seed limited? A critique and meta-analysis of seed addition. Am Nat 170(1):128–142. doi:10.1086/518565
Coile NC, Garland MA (2003) Notes on Florida’s endangered and threatened plants. Florida Department of Agriculture and Consumer Services, Gainesville
Cook TD, DeMets DL (eds) (2008) Introduction to statistical methods for clinical trials. CRC Press, Florida
Ericksson O (2002) Ontogenetic niche shifts and their implications for recruitment in three clonal Vaccinium shrubs: Vaccinium myrtillus, Vaccinium vitis-idaea, and Vaccinium oxycoccos. Can J Bot 80:635–641
Falk DA, Millar CI, Olwell M (1996) Restoring diversity: strategies for reintroduction of endangered plants. Center for plant conservation. Island Press, Washington, DC
Fiedler PL, Laven RD (1996) Selecting reintroduction sites. In: Falk DA, Millar CI, Olwell M (eds) Restoring diversity: strategies for reintroduction of endangered plants. Center for plant conservation. Island Press, Washington, DC
Fisher JB, Jayachandran K (2002) Arbuscular mycorrhizal fungi enhance seedling growth in two endangered plant species from south Florida. Int J Plant Sci 163(4):559–566. doi:10.1086/340428
Fisher JB, Jayachandran K (2005) Presence of arbuscular mycorrhizal fungi in South Florida native plants. Mycorrhiza 15(8):580–588. doi:10.1007/s00572-005-0367-0
Florida Natural Areas Inventory (FNAI) (2000) Narrowleaf hoarypea. http://www.fnai.org/FieldGuide/pdf/Tephrosia_angustissima.pdf. Accessed 6th April 2014
Florida Natural Areas Inventory (FNAI) (2007) Element tracking summary. 25th October. http://www.fnai.org/PDF/Element_tracking_summary_200709.pdf. Accessed 3 Dec 2007
Gann GD, Bradley KA, Woodmansee SW (2002) Rare plants of South Florida. River City Publishing, Jacksonville
Giri B, Kapoor R, Mukerji KG (2005) Effect of the arbuscular mycorrhizae Glomus fasciculatum and G. macrocarpum on the growth and nutrient content of Cassia siamea in a semi-arid Indian wasteland soil. New Forest 29(1):63–73. doi:10.1007/s11056-004-0246-0
Graham A (2011) The age and diversification of terrestrial New World ecosystems through Cretaceous and Cenozoic time. Am J Bot 98(3):336–351. doi:10.3732/ajb.1000353
Grubb PJ (1977) The maintenance of species-richness in plant communities: the importance of the regeneration niche. Biol Rev 52(1):107–145. doi:10.1111/j.1469-185X.1977.tb01347.x
Guerrant EO, Kaye TN (2007) Reintroduction of rare and endangered plants: common factors, questions and approaches. Aust J Bot 55:362–370. doi:10.1071/BT06033
Haskins KE, Pence V (2012) Transitioning plants to new environments: beneficial applications of soil microbes. In: Maschinski J, Haskins KE (eds) Plant reintroduction in a changing climate: promises and perils. Center for plant conservation. Island Press, Washington
Hoekstra JM, Boucher TM, Ricketts TH, Roberts C (2005) Confronting a biome crisis: global disparities of habitat loss and protection. Ecol Lett 8:23–29. doi:10.1111/j.1461-0248.2004.00686.x
Intergovernmental Panel on Climate Change (IPCC) (2007) Climate change 2007: synthesis report. Contribution of working groups I, II and III to the fourth assessment report of the intergovernmental panel on climate change [Core Writing Team, Pachauri RK and Reisinger A (eds.)]. IPCC, Geneva, Switzerland
International Union for the Conservation of Nature (IUCN) (2013) Guidelines for reintroductions and other conservation translocations. Version 1.0. IUCN Species Survival Commission, Gland. ISBN: 978-2-8317-1609-1
Jackson ST, Webb RS, Anderson KH, Overpeck JT, Webb T III, Williams JW, Hansen BCS (2000) Vegetation and environment in eastern North America during the last glacial maximum. Quat Sci Rev 19(6):489–508
Lee CY, Liew PM (2010) Late quaternary vegetation and climate changes inferred from a pollen record of Dongyuan lake in southern Taiwan. Palaeogeogr Palaeoclimatol Palaeoecol 287:58–66. doi:10.1016/j.palaeo.2010.01.015
Lees AC, Peres CA (2009) Gap-crossing movements predict species occupancy in Amazonian forest fragments. Oikos 118(2):280–290. doi:10.1111/j.1600-0706.2008.16842.x
Lewis PO, Crawford DJ (1995) Pleistocene refugium endemics exhibit greater allozymic diversity than widespread congeners in the genus Polygonella (Polygonaceae). Am J Bot 82(2):141–149
Long RW, Lakela O (1978) A flora of tropical Florida: a manual of seed plants and ferns of southern peninsular Florida. Banyan Books, Miami
Maschinski J, Haskins KE (eds) (2012) Plant reintroduction in a changing climate: Promises and perils. Island Press, Washington
Maschinski J, Baggs JE, Sacchi CF (2004) Seedling recruitment and survival of an endangered limestone endemic in its natural habitat and experimental introduction sites. Am J Bot 91(5):689–698
Maschinski J, Wendelberger KS, Wright SJ, Possley J, Walters D, Roncal J, Fisher J (2006) Conservation of South Florida endangered and threatened flora: 2005 Program at Fairchild Tropical Garden. Final report contract #009706. Florida Department of Agriculture and Consumer Services, Division of Plant Industry, Gainesville
Maschinski J, Albrecht MA, Monks L, Haskins KE (2012) Center for plant conservation best reintroduction practice guidelines. In: Maschinski J, Haskins KE (eds) Plant reintroduction in a changing climate: Promises and perils. Island Press, Washington
McGregor SE (1976) Insect pollination of cultivated crop plants. Agriclutural handbook no. 496. United States Department of Agriculture. U.S. Government Printing Office. Washington, DC
McLachlan JS, Hellmann JJ, Schwartz MW (2007) A framework for debate of assisted migration in an era of climate change. Conserv Biol 21(2):297–302. doi:10.1111/j.1523-1739.2007.00676.x
Mondo P, Marshall Mattson KD, Bennington CC (2010) The effect of shrubs on the establishment of an endangered perennial (Asclepias curtissii) endemic to Florida scrub. Southeast Nat 9(2):259–274
Muenchow G (1986) Ecological use of failure time analysis. Ecology 67(1):246–250
Niering WA, Whittaker RH, Lowe CH (1963) The Saguaro: a population in relation to environment. Science 142(3588):15–23
Noel F, Prati D, van Kleunen M, Gygax A, Moser D, Fischer M (2011) Establishment success of 25 rare wetland species introduced into restored habitats is best predicted by ecological distance to source habitats. Biol Conserv 144:602–609. doi:10.1016/j.biocon.2010.11.001
Padilla FM, Pugnaire FI (2006) The role of nurse plants in the restoration of degraded environments. Front Ecol Environ 4(4):196–202
Pavlik BM (1996) Defining and measuring success. In: Falk DA, Millar CI, Olwell M (eds) Restoring diversity: strategies for introduction of endangered plants. Island Press, Washington, DC, pp 127–155
Pinheiro J, Bates D, DebRoy S, Sarkar D, the R Core team (2008) nlme: Linear and nonlinear mixed effects models. R package version 3. pp. 1–89
Possley J, Maschinski J, Maguire J, Guerra C (2014) Vegetation monitoring to guide management decisions in Miami’s urban pine rockland preserves. Nat Areas J 34:154–165
Pruett CL, Winker K (2005) Biological impacts of climate change on a Beringian endemic: cryptic refugia in the establishment and differentiation of the rock sandpiper (Calidris ptilocnemis). Clim Change 68:219–240
Pyke DA, Brooks ML, D’Antonio C (2010) Fire as a restoration tool: a decision framework for predicting the control or enhancement of plants using fire. Restor Ecol 18(3):274–284. doi:10.1111/j.1526-100X.2010.00658.x
Rice JA (1988) Mathematical statistics and data analysis. Wadsworth & Brooks/Cole, Pacific Grove
Robertson WB Jr (1955) An analysis of the breeding-bird populations of tropical Florida in relation to the vegetation. PhD thesis, Univ. of Illinois, Urbana
Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332
Snyder JR, Herndon A, Robertson WB Jr (1990) South Florida rockland. In: Myers RL, Ewel JJ (eds) Ecosystems of Florida. The University of Central Florida Press, Gainesville, pp 230–278
Society for Ecological Restoration Science & Policy Working Group (SER) (2004) The SER primer on ecological restoration. Version 2. http://www.ser.org. Accessed 14 Nov 2013
Stepien CA, Murphy DJ, Lohner RN, Sepulveda-Villet OJ, Haponski AE (2009) Signatures of vicariance, postglacial dispersal and spawning philopatry: population genetics of the walleye Sander vitreus. Mol Ecol 18(16):3411–3428. doi:10.1111/j.1365-294X.2009.04291.x
R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0, Available from http://www.R-project.org
Therneau T, original report by Lumley T (2009) Survival: survival analysis, including penalized likelihood. R package version 2. http://CRAN.R-project.org/package=survival
Traill LW, Brook BW, Frankham RR, Bradshaw CJA (2009) Pragmatic population viability targets in a rapidly changing world. Biol Conserv 143(1):28–34. doi:10.1016/j.biocon.2009.09.001
Turnbull LA, Crawley MJ, Rees M (2000) Are plant populations seed-limited? a review of seed sowing experiments. Oikos 88(1):225–238. doi:10.1034/j.1600-0706.2000.880201.x
Vallee L, Hogbin T, Monks L, Makinson B, Matthes M, Rossetto M (2004) Guidelines for the translocation of threatened plants in Australia, 2nd ed. Australian Network for Plant Conservation, Canberra. http://www.anbg.gov.au/anpc/publications.html. Accessed 14 Nov 2013
Vitt P, Havens K, Kramer AT, Sollenberger D, Yates E (2010) Assisted migration of plants: changes in latitudes, changes in attitudes. Biol Conserv 143(1):18–27. doi:10.1016/j.biocon.2009.08.015
Wendelberger KS (2010) Assessing microsite and regeneration niche preferences when introducing endangered species. MS thesis. University of North Carolina, Chapel Hill
Wendelberger KS, Fellows MQN, Maschinski J (2008) Rescue and restoration: experimental translocation of Amorpha herbacea Walter. var. crenulata (Rybd.) sley into a novel urban habitat. Restor Ecol 16(4):542–552. doi:10.1111/j.1526-100X.2007.00325.x
Young TP, Petersen DA, Clary JJ (2005) The ecology of restoration: historical links, emerging issues and unexplored realms. Ecol Lett 8:662–673
Acknowledgments
The authors thank Dr. J. Weiss for his endless patience and assistance with the data analysis, Drs. P. White, B. Peet, A. Weakly, and J.H. Richards for their helpful feedback on the manuscript, the Florida Department of Agriculture and Consumer Services and the University of North Carolina’s W.C. Coker Fellowship and Alma Holland Beers Scholarship for funding, Miami-Dade Department of Environmental Resources Management and the Environmentally Endangered Lands Program (R. Gray-Urgelles) for allowing the study on their protected land and providing the 2009 fire data, Miami-Dade Department of Parks and Recreation (D. Hazelton, J. Maguire, C. Rodriguez, and S. Thompson) for permitting and field assistance, the United States Department of Agriculture Sub-Tropical Horticultural Station (R. Schnell) for permitting us access to their land. Thanks to Fairchild staff (T. Chormanski, A. Ferris, J. Fisher, A. Frances, P. Gonsiska, J. Goodman, K. Griffin, A. Muir, K. Neugent, G. Orihuela, J. Possley, D. Powell, J. Roncal, H. Thornton, A. Walker, C. Walters, D. Walters, S. Wright), interns (A. Bradley, T. Carroll, A. King, A. Rosenberg, C. Rye), and volunteers (C. Barjum, S. Berckmans, W. Brooks, A. Felan, S. Forman, M. Freedman, R. McGuire, E. McSweeny, B. Petzinger, M. Rose, A. Saha, M. Salvoch, C. Abley Vargas) for their help and perseverance in the field. We thank Island Press for granting copyright release for those portions of the paper published in Plant Reintroduction in a Changing Climate.
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Communicated by Thomas Abeli and Kingsley Dixon.
This manuscript is dedicated in loving memory to Richard Wendelberger who helped me save my first plant when I was 9 years old.
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Wendelberger, K.S., Maschinski, J. Assessing microsite and regeneration niche preferences through experimental reintroduction of the rare plant Tephrosia angustissima var. corallicola . Plant Ecol 217, 155–167 (2016). https://doi.org/10.1007/s11258-015-0521-5
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DOI: https://doi.org/10.1007/s11258-015-0521-5