Convergence of three mangrove species towards freeze-tolerant phenotypes at an expanding range edge

Functional Ecology

Volumn 29, Issue 10, 2015, Pages 1332-1340

  Cook Patton, Susan C ^a   Lehmann, Michael ^b   Parker, John D ^a  

^a SMITHSONIAN ENVIRONMENTAL RESEARCH CENTER   (United States)

^b SMITHSONIAN MARINE STATION   (United States)

Author keywords

Rhizophora mangle; Avicennia germinans; Climate change; Freeze tolerance; Laguncularia racemosa; Latitudinal limits; Mangrove

Indexed keywords

ADULT; CLIMATE CHANGE; COASTAL ZONE; ECOPHYSIOLOGY; ENVIRONMENTAL FACTOR; FREEZE TOLERANCE; FUNCTIONAL RESPONSE; MANGROVE; PHENOTYPE;

FLORIDA [UNITED STATES]; UNITED STATES;

AVICENNIA GERMINANS; LAGUNCULARIA RACEMOSA; RHIZOPHORA MANGLE; RHIZOPHORACEAE;

EID: 84942837131     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12443     Document Type: Article

References (55)

1. Alberto, F.J., Aitken, S.N., Alia, R., González-Martínez, S.C., Hänninen, H., Kremer, A. et al. (2013) Potential for evolutionary responses to climate change - evidence from tree populations. Global Change Biology, 19, 1645-1661.
2. Albrecht, M., Kneeland, K.M., Lindroth, E. & Foster, J.E. (2013) Genetic diversity and relatedness of the mangrove Rhizophora mangle L. (Rhizophoraceae) using amplified fragment polymorphisms (AFLP) among locations in Florida, USA and the Caribbean. Journal of Coastal Conservation, 17, 483-491.
3. Angert, A.L., Sheth, S.N. & Paul, J.R. (2011) Incorporating population-level variation in thermal performance into predictions of geographic range shifts. Integrative and Comparative Biology, 51, 733-750.
4. Aranda, I., Castro, L., Alia, R., Pardos, J.A. & Gil, L. (2005) Low temperature during winter elicits differential responses among populations of the Mediterranean evergreen cork oak (Quercus suber). Tree Physiology, 25, 1085-1090.
5. Bartlett, M.K., Scoffoni, C., Ardy, R., Zhang, Y., Sun, S., Cao, K. et al. (2012) Rapid determination of comparative drought tolerance traits: using an osmometer to predict turgor loss point. Methods in Ecology and Evolution, 3, 880-888.
6. Boorse, G.C., Bosma, T.L., Meyer, A.C., Ewers, F.W. & Davis, S.D. (1998) Comparative methods of estimating freezing temperatures and freezing injury in leaves of chaparral shrubs. International Journal Of Plant Sciences, 159, 513-521.
7. Bridle, J.R. & Vines, T.H. (2007) Limits to evolution at range margins: when and why does adaptation fail? Trends in Ecology & Evolution, 22, 140-147.
8. Buckley, L.B. & Kingsolver, J.G. (2012) Functional and phylogenetic approaches to forecasting species' responses to climate change. Annual Review Of Ecology And Systematics, 43, 205-226.
9. Buot, I.E. & Okitsu, S. (1999) Leaf size zonation pattern of woody species along an altitudinal gradient Mt. Pulog, Philippines. Plant Ecology, 145, 197-208.
10. Burrows, M.T., Schoeman, D.S., Buckley, L.B., Moore, P., Poloczanska, E.S., Brander, K.M. et al. (2011) The pace of shifting climate in marine and terrestrial ecosystems. Science, 334, 652-655.
11. Carlson, J.E., Holsinger, K.E. & Prunier, R. (2010) Plant responses to climate in the Cape Floristic Region of South Africa: evidence for adaptive differentiation in the Proteaceae. Evolution, 65, 108-124.
12. Cavanaugh, K.C., Kellner, J.R., Forde, A.J., Gruner, D.S., Parker, J.D., Rodriguez, W. et al. (2014) Poleward expansion of mangroves is a threshold response to decreased frequency of extreme cold events. Proceedings of the National Academy of Sciences, 111, 723-727.
13. Cavender-Bares, J., Cortes, P., Rambal, S., Joffre, R., Miles, B. & Rocheteau, A. (2005) Summer and winter sensitivity of leaves and xylem to minimum freezing temperatures: a comparison of co-occurring Mediterranean oaks that differ in leaf lifespan. New Phytologist, 168, 597-612.
14. Chen, I.-C., Hill, J.K., Ohlemuller, R., Roy, D.B. & Thomas, C.D. (2011) Rapid range shifts of species associated with high levels of climate warming. Science, 333, 1024-1026.
15. Clissold, F.J., Sanson, G.D., Read, J. & Simpson, S.J. (2009) Gross vs. net income: How plant toughness affects performance of an insect herbivore. Ecology, 90, 3393-3405.
16. Coley, P.D. (1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecological Monographs, 53, 209-234.
17. Cook-Patton, S. & Agrawal, A.A. (2011) Relatedness predicts phenotypic plasticity in plants better than weediness. Evolutionary Ecology Research, 13, 527-542.
18. Costanza, R., d'Arge, R., de Groot, R., Farber, S., Grasso, M., Hannon, B. et al. (1997) The value of the world's ecosystem services and natural capital. Nature, 387, 253-260.
19. Duke, N.C., Ball, M.C. & Ellison, J.C. (1998) Factors influencing biodiversity and distribution gradients in mangroves. Global Ecology and Biogeography Letters, 7, 27-47.
20. Etterson, J.R. (2001) Constraint to adaptive evolution in response to global warming. Science, 294, 151-154.
21. Genty, B., Briantais, J.M. & Baker, N.R. (1989) The relationship between quantum yield and photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta, 990, 87-92.
22. Hemmi, A. & Jormalainen, V. (2002) Nutrient enhancement increases performance of a marine herbivore via quality of its food alga. Ecology, 83, 1052-1064.
23. Hogarth, P.J. (1999) The Biology of Mangroves. Oxford UP, Oxford.
24. Hsueh, M.-L. & Lee, H.-H. (2000) Diversity and distribution of the mangrove forests in Taiwan. Wetlands Ecology and Management, 8, 233-242.
25. Kearney, M.R. & Porter, W. (2009) Mechanistic niche modelling: combining physiological and spatial data to predict species' ranges. Ecology Letters, 12, 334-350.
26. Knight, C.A. & Ackerly, D.D. (2003) Evolution and plasticity of photosynthetic thermal tolerance, specific leaf area and leaf size: congeneric species from desert and coastal environments. New Phytologist, 160, 337-347.
27. Koehler, K., Center, A. & Cavender-Bares, J. (2011) Evidence for a freezing tolerance-growth rate trade-off in the live oaks (Quercus series Virentes) across the tropical-temperate divide. New Phytologist, 193, 730-744.
28. Kostal, V., Doležal, P., Rozsypal, J., Moravcová, M., Zahradníčková, H. & Šimek, P. (2011) Physiological and biochemical analysis of overwintering and cold tolerance in two Central European populations of the spruce bark beetle, Ips typographus. Journal of Insect Physiology, 57, 1136-1146.
29. Lovelock, C.E., Feller, I.C., Ball, M.C., Ellis, J. & Sorrell, B. (2007) Testing the growth rate vs. geochemical hypothesis for latitudinal variation in plant nutrients. Ecology Letters, 10, 1154-1163.
30. MacArthur, R.H. (1972) Patterns in the Distribution of Species. Harper & Row Publisher Inc, New York City, New York, USA.
31. Markley, J.L., McMillan, C. & Thompson, G.A. Jr (1982) Latitudinal differentiation in response to chilling temperatures among populations of three mangroves, Avicennia germinans, Laguncularia racemosa, and Rhizophora mangle from the western tropical Atlantic and Pacific Panama. Canadian Journal of Botany-Revue Canadienne De Botanique, 60, 2704-2715.
32. McCann, S., Greenlees, M.J., Newell, D. & Shine, R. (2014) Rapid acclimation to cold allows the cane toad to invade montane areas within its Australian range. Functional Ecology, 28, 1166-1174.
33. Morin, X., Ameglio, T., Ahas, R., Kurz-Besson, C., Lanta, V., Lebourgeois, F. et al. (2007) Variation in cold hardiness and carbohydrate concentration from dormancy induction to bud burst among provenances of three European oak species. Tree Physiology, 27, 817-825.
34. Pérez, F., Hinojosa, L.F., Ossa, C.G., Campano, F. & Orrego, F. (2014) Decoupled evolution of foliar freezing resistance, temperature-niche and morphological leaf traits in Chilean Myrceugenia. Journal of Ecology, 102, 972-980.
35. Pickens, C.N. & Hester, M.W. (2011) Temperature tolerance of early life history stages of black mangrove avicennia germinans: implications for range expansion. Estuaries and Coasts, 34, 824-830.
36. Rehfeldt, G.E., Wykoff, W.R. & Ying, C.C. (2001) Physiologic plasticity, evolution, and impacts of a changing climate on Pinus contorta. Climatic Change, 50, 355-376.
37. Ross, M.S., Ruiz, P.L., Sah, J.P. & Hanan, E.J. (2009) Chilling damage in a changing climate in coastal landscapes of the subtropical zone: a case study from south Florida. Global Change Biology, 15, 1817-1832.
38. Saintilan, N., Wilson, N.C., Rogers, K., Rajkaran, A. & Krauss, K.W. (2013) Mangrove expansion and salt marsh decline at mangrove poleward limits. Global Change Biology, 20, 147-157.
39. Sakai, A. & Weiser, C.J. (1973) Freezing resistance of trees in North America with reference to tree regions. Ecology, 54, 118-126.
40. Scarth, G.W. & Levitt, J. (1937) The frost-hardening mechanism of plant cells. Plant Physiology, 12, 51-78.
41. Scriber, J.M. (1977) Limiting effects of low leaf-water content on nitrogen utilization, energy budget, and larval growth of Hyalophora cecropia (Lepidoptera: Saturniidae). Oecologia, 28, 269-287.
42. Sherrod, C.L. & McMillan, C. (1981) Black mangrove, Avicennia germinans, in Texas - past and present distribution. Contributions in Marine Science, 24, 115-131.
43. Sherrod, C.L. & McMillan, C. (1985) The distributional history and ecology of mangrove vegetation along the northern gulf of Mexico coastal region. Contributions in Marine Science, 28, 129-140.
44. Shreve, F. (1914) The role of winter temperatures in determining the distribution of plants. American Journal of Botany, 1, 194-202.
45. Simpson, L.T., Feller, I.C. & Chapman, S.K. (2013) Effects of competition and nutrient enrichment on Avicennia germinans in the salt marsh-mangrove ecotone. Aquatic Botany, 104, 55-59.
46. Soares, M.L.G., Estrada, G.C.D., Fernandez, V. & Tognella, M.M.P. (2012) Southern limit of the Western South Atlantic mangroves: Assessment of the potential effects of global warming from a biogeographical perspective. Estuarine, Coastal and Shelf Science, 101, 44-53.
47. Spalding, M., Kainuma, M. & Collins, L. (2010) World Atlas of Mangroves. Earthscan Ltd, London.
48. Stuart, S.A., Choat, B., Martin, K.C., Holbrook, N.M. & Ball, M.C. (2006) The role of freezing in setting the latitudinal limits of mangrove forests. New Phytologist, 173, 576-583.
49. Suarez, A.V. & Tsutsui, N.D. (2008) The evolutionary consequences of biological invasions. Molecular Ecology, 17, 351-360.
50. Tomlinson, P.B. (1986) The Botany of Mangroves. Cambridge University Press, Cambridge.
51. Triest, L. (2008) Molecular ecology and biogeography of mangrove trees towards conceptual insights on gene flow and barriers: A review. Aquatic Botany, 89, 138-154.
52. Verges, A., Steinberg, P.D., Hay, M.E., Poore, A.G.B., Campbell, A.H., Ballesteros, E. et al. (2014) The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proceedings of the Royal Society of London Series B-Biological Sciences, 281, 20140846.
53. Wang, W., Siyang, Y., Wang, Y., Huang, L. & Wang, M. (2011) Influence of frost on nutrient resorption during leaf senescence in a mangrove at its latitudinal limit of distribution. Plant and Soil, 342, 105-115.
54. Wernberg, T., Smale, D.A., Tuya, F., Thomsen, M.S., Langlois, T., de Bettignies, T. et al. (2013) An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nature Climate Change, 3, 78-82.
55. Williams, A.A., Eastman, S.F., Eash-Loucks, W.E., Kimball, M.E., Lehmann, M.L. & Parker, J.D. (2014) Record northernmost endemic mangroves on the United States Atlantic Coast with a note on latitudinal migration. Southeastern Naturalist, 13, 56-63.