Early performance of two tropical dry forest species after assisted migration to pine–oak forests at different altitudes: strategic response to climate change

Abstract

Assisted migration has been proposed as a strategy for adaptive management of forest species in response to expected effects of climate change, but it is controversial for several reasons. Tropical dry forests are among the most threatened ecosystems in the world. In Mexico, historically, land-use change and deforestation have been decreasing forest cover, and climate change is shifting the potential distribution of different forest types, exacerbating the risk of local extinctions. Assisted altitudinal migration could be a feasible strategy for reducing local extinctions in response to climate change and lack of landscape connectivity. Our objective was to evaluate survival and growth of Albizia plurijuga and Ceiba aesculifolia, two tropical deciduous forests species in Mexico. We transplanted 4-month-old seedlings to experimental raised beds at three altitudes (2100, 2400 and 2700 m a.s.l.), exceeding their upper regional limit of distribution (2000 m a.s.l.). We also tested seed germination at each altitude. We monitored the experiment for 10 months. For both species, as altitude increased and cold weather was more prevalent, plant performance declined. Within species, differences in individual growth were significant among altitudes. Overall survival was 18.5% for A. plurijuga and 24.5% for C. aesculifolia. Both species had higher survival and better growth at lower altitude, and no seedling emergence at any altitude. We conclude that assisted migration can be implemented for each species by an upward attitudinal shift within, and not exceeding, 400 m beyond their present upper altitudinal limit of distribution. Our results indicate that for many species that show altitudinal gradients at regional scales, unless current climate conditions change, the potential to establish outside their range is minimal.

Keywords

Albizia plurijuga / Ceiba aesculifolia / Climate change / Fabaceae / Forest management / Mitigation strategy / Range expansion

References

[1] Aitken SN, Yeaman S, Holliday JA, Wang T, Curtis-McLane S. Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol Appl, 2008, 1(1): 95-111.

[2] Andrade G, Calderón de Rzedowski G, Camargo-Ricalde S, Grether R, Hernández H, Martínez-Bernal A, Rico L, Rzedowski J, Sousa S (2007) Familia Leguminosae: Subfamilia Mimosoideae. In: Rzedowski J, Calderón de Rzedowski G (eds) Flora del Bajío y de regiones adyacentes. México, pp 1–229

[3] Bates D, Maechler M, Bolker B, Walker S. lme4: linear mixed-effects models using Eigen and S4. J Stat Softw, 2015, 67: 1-48.

[4] Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F. Impacts of climate change on the future of biodiversity: biodiversity and climate change. Ecol Lett, 2012, 15(4): 365-377.

[5] Bucharova A, Durka W, Hermann JM, Hölzel N, Michalski S, Kollmann J, Bossdorf O. Plants adapted to warmer climate do not outperform regional plants during a natural heat wave. Ecol Evol, 2016, 6(12): 4160-4165.

[6] Carranza E, Blanco-García A (2000) Familia Bombacaceae. In: Rzedowski J, Calderón de Rzedowski G (eds) Flora del Bajío y de regiones adyacentes. México, pp 1–16

[7] Castellanos-Acuña D, Lindig-Cisneros R, Sáenz-Romero C. Altitudinal assisted migration of Mexican pines as an adaptation to climate change. Ecosphere, 2015, 6(1): 1-16.

[8] Chen IC, Hill JK, Ohlemuller R, Roy DB, Thomas CD. Rapid range shifts of species associated with high levels of climate warming. Science, 2011, 333: 1024-1026.

[9] Christmas MJ, Breed MF, Lowe AJ. Constraints to and conservation implications for climate change adaptation in plants. Conserv Genet, 2016, 17(2): 305-320.

[10] Corlett RT, Westcott DA. Will plant movements keep up with climate change?. Trends Ecol Evol, 2013, 28(8): 482-488.

[11] Dalrymple S, Banks E, Stewart G, Pullin A (2012) A meta-analysis of threatened plant reintroductions from across the globe. In: Maschinski J, Haskins K (eds) Plant reintroduction in a changing climate: promises and perils. Washington, DC, pp 31–50

[12] Davis MB, Shaw RG. Range shifts and adaptive responses to quaternary climate change. Science, 2001, 292(5517): 673-679.

[13] Dumroese RK, Williams MI, Stanturf JA, Clair JBS. Considerations for restoring temperate forests of tomorrow: forest restoration, assisted migration, and bioengineering. New Forest, 2015, 46(5–6): 947-964.

[14] Feeley KJ, Rehm EM, Machovina B. The responses of tropical forest species to global climate change: acclimate, adapt, migrate, or go extinct?. Front Biogeogr, 2012, 4(2): 69-80.

[15] Frascaria-Lacoste N, Fernández-Manjarrés J. Assisted colonization of foundation species: lack of consideration of the extended phenotype concept-response to Kreyling et al. (2011). Restor Ecol, 2012, 20(3): 296-298.

[16] Gienapp P, Teplitsky C, Alho JS, Mills JA, Merilä J. Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol, 2008, 17(1): 167-178.

[17] González-Espinosa M (1998). Albizia plurijuga. The IUCN red list of threatened species 1998: e.T32948A9744319. http://dx.doi.org/10.2305/IUCN.UK.1998.RLTS.T32948A9744319.en. Accessed 13 Jan 2015

[18] Hamann A, Wang T. Potential effects of climate change on ecosystem and tree species distribution in British Columbia. Ecology, 2006, 87(11): 2773-2786.

[19] Harris JA, Hobbs RJ, Higgs E, Aronson J. Ecological restoration and global climate change. Restor Ecol, 2006, 14(2): 170-176.

[20] Hewitt N, Klenk N, Smith AL, Bazely DR, Yan N, Wood S, MacLellan JI, Lipsig-Mumme C, Henriques I. Taking stock of the assisted migration debate. Biol Conserv, 2011, 144(11): 2560-2572.

[21] Hoegh-Guldberg O, Hughes L, McIntyre S, Lindenmayer DB, Parmesan C, Possingham HP, Thomas CD. Assisted colonization and rapid climate change. Science, 2008, 321(5887): 345-346.

[22] Hunter ML Jr. Climate change and moving species: furthering the debate on assisted colonization. Conserv Biol, 2007, 21(5): 1356-1358.

[23] IPCC (2013) Climate Change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V Midgley PM (eds)]. Cambridge University Press, Cambridge, p 1535

[24] Jump AS, Penuelas J. Running to stand still: adaptation and the response of plants to rapid climate change. Ecol Lett, 2005, 8(9): 1010-1020.

[25] Kreyling J, Bittner T, Jaeschke A, Jentsch A, Steinbauer MJ, Thiel D, Beierkuhnlein C. Assisted Colonization: a question of focal units and recipient localities. Restor Ecol, 2011, 19(4): 433-440.

[26] Ledig FT, Rehfeldt GE, Saenz-Romero C, Flores-Lopez C. Projections of suitable habitat for rare species under global warming scenarios. Am J Bot, 2010, 97(6): 970-987.

[27] Lenoir J, Gegout JC, Marquet PA, de Ruffray P, Brisse H. A significant upward shift in plant species optimum elevation during the 20th century. Science, 2008, 320(5884): 1768-1771.

[28] Lunt ID, Byrne M, Hellmann JJ, Mitchell NJ, Garnett ST, Hayward MW, Martin TG, McDonald-Maddden E, Williams SE, Zander KK. Using assisted colonisation to conserve biodiversity and restore ecosystem function under climate change. Biol Conserv, 2013, 157: 72-177.

[29] Mueller JM, Hellmann JJ. An assessment of invasion risk from assisted migration. Conserv Biol, 2008, 22(3): 562-567.

[30] Pedlar J, McKenney D, Aubin I, Beardmore T, Beaulieu J, Iverson L, O’Neill GA, Winder RS, Ste-Marie C. Placing forestry in the assisted migration debate. Bioscience, 2012, 62(9): 835-842.

[31] Pinheiro J, Bates D, DebRoy S, Sarkar D (2016) nlme: linear and nonlinear mixed effects models. R package version 3.1-124. http://CRAN.R-project.org/package=nlme

[32] R Development Core Team. R: a language and environment for statistical computing, 2016, Viena: R Foundation for Statistical Computing.

[33] Rehfeldt GE (1994) Evolutionary genetics, the biological species and the ecology of the interior Cedar-Hemlock forest. In: Baumgartnet D, Lotan J, Tonn J (eds) Proceedings of the conference: interior cedar-Hemlock-White Pine forests—ecology and management. Washington State University Extension. Spokane, Washington, pp 91–100

[34] Rehfeldt GE (2006) A spline model of climate for the western United States. Gen. Tech. Rep. RMRS-GTR-165, Fort Collins, Colorado, USDA Forest Service, p 21

[35] Rehfeldt GE, Ying CC, Spittlehouse DL, Hamilton DA Jr. Genetic responses to climate in Pinus contorta: niche breadth, climate change, and reforestation. Ecol Monogr, 1999, 69(3): 375-407.

[36] Rehfeldt GE, Jaquish BC, Sáenz-Romero C, Joyce DG, Leites LP, StClair JB, López-Upton J. Comparative genetic responses to climate for the varieties of Pinus ponderosa and Pseudotsuga menziesii: reforestation. For Ecol Manag, 2014, 324: 147-157.

[37] Reusch TBH, Wood TE. Molecular ecology of global change. Mol Ecol, 2007, 16(19): 3973-3992.

[38] Reyes-Abrego GA (2014) Distribución potencial actual y bajo escenarios de cambio climático de especies arbóreas tropicales en México, mediante el modelaje del nicho ecológico. Tesis de Maestría en Ciencias Biológicas, Universidad Michoacana de San Nicolás de Hidalgo, Michoacan, Mexico

[39] Ricciardi A, Simberloff D. Assisted colonization is not a viable conservation strategy. Trends Ecol Evol, 2009, 24(5): 248-253.

[40] Richardson DM, Hellmann JJ, McLachlan JS, Sax DF, Schwartz MW, Gonzalez P, Brennan EJ, Camacho A, Root TL, Sala OE, Schneider SH, Ashe DM, Rappaport-Clark J, Early R, Etterson JR, Fielder ED, Gill JL, Minteer BA, Polasky S, Safford HD, Thompson AR, Vellend M. Multidimensional evaluation of managed relocation. Proc Natl Acad Sci USA, 2009, 106(24): 9721-9724.

[41] Rico-Arce M, Gale S, Maxted N. A taxonomic study of Albizia (Leguminosae: Mimosoideae: Ingeae) in Mexico and Central America. Anales del Jardín Botánico de Madrid, 2008, 65(2): 255-305.

[42] Rzedowski J, Calderón de Rzedowski G. El bosque tropical caducifolio de la región mexicana del Bajío. Trace, 1987, 12: 12-21.

[43] Rzedowski J, Zamudio S, Calderón de Rzedowski G, Paizanni A (2014) El Bosque Tropical Caducifolio en la cuenca lacustre de Pátzcuaro (Michoacán, México). In: Rzedowski J, Calderón de Rzedowski G (eds) Flora del Bajío y de regiones adyacentes, Fascículo complementario XXIX, México, p 18

[44] Sáenz-Romero C, Rehfeldt GE, Crookston NL, Duval P, St-Amant R, Beaulieu J, Richardson BA. Spline models of contemporary, 2030, 2060 and 2090 climates for Mexico and their use in understanding climate-change impacts on the vegetation. Clim Change, 2010, 102(3–4): 595-623.

[45] Sáenz-Romero C, Rehfeldt GE, Crookston NL, Duval P, Beaulieu J. Spline models of contemporary, 2030, 2060, and 2090 climates for Michoacan State, Mexico. Impacts on the vegetation. Rev Fitotec Mex, 2012, 35(4): 333-345.

[46] Schwartz MW. Elucidating biological opportunities and constraints on assisted colonization. Appl Veg Sci, 2016, 19(2): 185-186.

[47] Seddon PJ. From reintroduction to assisted colonization: moving along the conservation translocation spectrum. Restor Ecol, 2010, 18(6): 796-802.

[48] Tchebakova NM, Rehfeldt GE, Parfenova EI. Impacts of climate change on the distribution of Larix spp. and Pinus sylvestris and their climatypes in Siberia. Mitig Adapt Strat Global Change, 2005, 11(4): 861-882.

[49] Therneau TM, Grambsch PM. Modeling survival data: extending the Cox model, 2000, New York: Springer.

[50] Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, Erasmus BFN, Ferreira de Siqueira M, Grainger A, Hannah L, Hughes L, Huntley B, van Jaarsveld AS, Midgley GF, Miles L, Ortega-Huerta MA, Peterson AT, Phillips OL, Williams SE. Extinction risk from climate change. Nature, 2004, 427: 145-148.

[51] Valle-Díaz O, Blanco-García A, Bonfil C, Lindig-Cisneros R. Altitudinal range shift detected through seedling survival of Ceiba aesculifolia in an area under the influence of an urban heat island. For Ecol Manag, 2009, 258(7): 1511-1515.

[52] Velázquez A, Fregoso A, Bocco G, Cortez G. The use of a landscape approach in Mexican forest indigeneous communities to strengthen long-term forest management. Interciencia, 2003, 28(11): 632-638.

[53] Vitt P, Havens K, Kramer AT, Sollenberger D, Yates E. Assisted migration of plants: changes in latitudes, changes in attitudes. Biol Conserv, 2010, 143(1): 18-27.

[54] Williams MI, Dumroese RK. Preparing for climate change: forestry and assisted migration. J Forest, 2013, 111(4): 287-297.

[55] Winder R, Nelson E, Beardmore T. Ecological implications for assisted migration in Canadian forests. For Chron, 2011, 87(6): 731-744.

[56] Woodward FI, Fogg GE, Heber U. The impact of low temperatures in controlling the geographical distribution of plants. Philos Trans R Soc B Biol Sci, 1990, 326(1237): 585-593.