High heat tolerance in plants from the Andean highlands: Implications for paramos in a warmer world
Autoři:
Indira V. Leon-Garcia aff001; Eloisa Lasso aff001
Působiště autorů:
Departamento de Ciencias Biológicas, Universidad de los Andes, Bogotá, Cundinamarca, Colombia
aff001; Smithsonian Tropical Research Institute, Panamá, República de Panamá
aff002
Vyšlo v časopise:
PLoS ONE 14(11)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0224218
Souhrn
Tropical plant species are expected to have high heat tolerance reflecting phenotypic adjustments to warm regions or their evolutionary adaptation history. However, tropical highland specialists adapted to the colder temperatures found in the highlands, where short and prostrated vegetation decouples plants from ambient conditions, could exhibit different upper thermal limits than those of their lowland counterparts. Here we evaluated leaf heat tolerance of 21 tropical alpine paramo species to determine: 1) whether species with restricted distribution (i.e., highland specialists) have lower heat tolerance and are more vulnerable to warming than species with widespread distribution; 2) whether different growth forms have different heat tolerance; and 3) whether species height (i.e., microhabitat) influences its heat tolerance. We quantified heat tolerance by evaluating T50, which is the temperature that causes a reduction in 50% of initial Fv/Fm values and reflects an irreversible damage to the photosynthetic apparatus. Additionally, we estimated the thermal safety margins as the difference between T50 and the maximum leaf temperature registered for the species. All species presented high T50 values ranging between 45.4°C and 53.9°C, similar to those found for tropical lowland species. Heat tolerance was not correlated with species distributions or plant height, but showed a strong relationship with growth form, with rosettes having the highest heat tolerance. Thermal safety margins ranged from 12.1 to 31.0°C. High heat tolerance and broad thermal safety margins suggest low vulnerability of paramo species to warming as long as plants are capable of regulating the leaf temperature within this threshold. Whether paramo plants would be able to regulate leaf temperature if drought episodes become more frequent and transpirational cooling is compromised is the next question that needs to be answered.
Klíčová slova:
Plants – Grasses – Plant physiology – Leaves – Seedlings – Shrubs – Climate change – Tropical ecosystems
Zdroje
1. Kattan GH, Franco P, Rojas V, Morales G. Biological diversification in a complex region: A spatial analysis of faunistic diversity and biogeography of the Andes of Colombia. J Biogeogr. 2004;31: 1829–1839. doi: 10.1111/j.1365-2699.2004.01109.x
2. Ruiz D, Moreno HA, Gutiérrez ME, Zapata PA. Changing climate and endangered high mountain ecosystems in Colombia. Sci Total Environ. 2008;398: 122–32. doi: 10.1016/j.scitotenv.2008.02.038 18433837
3. Anderson P, Marengo J, Villalba R, Halloy S, Young B, Cordero D, et al. Consequences of Climate Change for ecosystems and ecosystem services in the Tropical Andes. Clim Chang Biodivers Trop Andes. 2011; 1–18. doi: 10.13140/2.1.3718.4969
4. Ramirez-Villegas J, Cuesta F, Devenish C, Peralvo M, Jarvis A, Arnillas CA. Using species distributions models for designing conservation strategies of Tropical Andean biodiversity under climate change. J Nat Conserv. Elsevier GmbH.; 2014;22: 391–404. doi: 10.1016/j.jnc.2014.03.007
5. Cuesta-Camacho F, Peralvoco M, Ganzenmüller A. Posibles efectos del calentamiento global sobre el nicho climático de algunas especies en los Andes Tropicales. Páramo y Cambio Climático. Quito; 2008. pp. 15–38.
6. Nogués-Bravo D, Araújo MB, Errea MP, Martínez-Rica JP. Exposure of global mountain systems to climate warming during the 21st Century. Glob Environ Chang. 2007;17: 420–428. doi: 10.1016/j.gloenvcha.2006.11.007
7. Scherrer D, Körner C. Topographically controlled thermal-habitat differentiation buffers alpine plant diversity against climate warming. J Biogeogr. 2011;38: 406–416. doi: 10.1111/j.1365-2699.2010.02407.x
8. Scherrer D, Schmid S, Körner C. Elevational species shifts in a warmer climate are overestimated when based on weather station data. Int J Biometeorol. 2011;55: 645–654. doi: 10.1007/s00484-010-0364-7 20924613
9. Broennimann O, Thuiller W, Hughes G, Midgley GF, Alkemade JMR, Guisan A. Do geographic distribution, niche property and life form explain plants’ vulnerability to global change? Glob Chang Biol. 2006;12: 1079–1093. doi: 10.1111/j.1365-2486.2006.01157.x
10. Smillie RM, Nott R. Heat Injury in Leaves of Alpine, Temperate and Tropical Plants. Funct Plant Biol. 1979;6: 135–141. doi: 10.1071/PP9790135
11. Braun V, Buchner O, Neuner G. Thermotolerance of photosystem 2 of three alpine plant species under field conditions. Photosynthetica. 2002;40: 587–595. doi: 10.1023/A:1024312304995
12. Buchner O, Neuner G. Variability of Heat Tolerance in Alpine Plant Species Measured at Different Altitudes. Aarctic, Antarct Alp Res. 2003;35: 411–420. doi: 10.1657/1523-0430(2003)035[0411:vohtia]2.0.co;2
13. Buchner O, Roach T, Gertzen J, Schenk S, Karadar M, Stöggl W, et al. Drought affects the heat-hardening capacity of alpine plants as indicated by changes in xanthophyll cycle pigments, singlet oxygen scavenging, α-tocopherol and plant hormones. Environ Exp Bot. Elsevier B.V.; 2017;133: 159–175. doi: 10.1016/j.envexpbot.2016.10.010
14. Calosi P, Bilton DT, Spicer JI. Thermal tolerance, acclimatory capacity and vulnerability to global climate change. Biol Lett. 2008;4: 99–102. doi: 10.1098/rsbl.2007.0408 17986429
15. Perez TM, Stroud JT, Feeley KJ. Thermal trouble in the tropics. Science (80-). 2016;351: 1392–1393. doi: 10.1126/science.aaf3343 27013713
16. Loik ME, Redar SP, Hartes J. Photosynthetic responses to a climate-warming manipulation for contrasting meadow species in the Rocky Mountains, Colorado, USA. Funct Ecol. 2000;14: 166–175.
17. Krause GH, Winter K, Krause B, Jahns P, García M, Aranda J, et al. High-temperature tolerance of a tropical tree, Ficus insipida: Methodological reassessment and climate change considerations. Funct Plant Biol. 2010;37: 890–900. doi: 10.1071/FP10034
18. Krause GH, Cheesman AW, Winter K, Krause B, Virgo A. Thermal tolerance, net CO2 exchange and growth of a tropical tree species, Ficus insipida, cultivated at elevated daytime and nighttime temperatures. J Plant Physiol. Elsevier GmbH.; 2013;170: 822–827. doi: 10.1016/j.jplph.2013.01.005 23399405
19. Maxwell K, Johnson GN. Chlorophyll fluorescence—a practical guide. J Exp Bot. 2000;51: 659–668. doi: 10.1093/jxb/51.345.659 10938857
20. Ducruet JM, Peeva V, Havaux M. Chlorophyll thermofluorescence and thermoluminescence as complementary tools for the study of temperature stress in plants. Photosynth Res. 2007;93: 159–171. doi: 10.1007/s11120-007-9132-x 17279439
21. Knight CA, Ackerly DD. Evolution and plasticity of photosynthetic thermal tolerance, specific leaf area and leaf size: Congeneric species from desert and coastal environments. New Phytol. 2003;160: 337–347. doi: 10.1046/j.1469-8137.2003.00880.x
22. Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, et al. Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci. 2008;105: 6668–6672. doi: 10.1073/pnas.0709472105 18458348
23. Krause GH, Weis E. Chlorophyll fluorescence as a tool in plant physiology—II. Interpretation of fluorescence signals. Photosynth Res. 1984;5: 139–157. doi: 10.1007/BF00028527 24458602
24. Araújo MB, Ferri-Yáñez F, Bozinovic F, Marquet PA, Valladares F, Chown SL. Heat freezes niche evolution. Ecol Lett. 2013;16: 1206–1219. doi: 10.1111/ele.12155 23869696
25. Slot M, Krause GH, Krause B, Hernández GG, Winter K. Photosynthetic heat tolerance of shade and sun leaves of three tropical tree species. Photosynth Res. 2018; doi: 10.1007/s11120-018-0563-3 30054784
26. Fick SE, Hijmans RJ. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int J Climatol. 2017;37: 4302–4315. doi: 10.1002/joc.5086
27. Körner C, Cochrane P. Influence of plant physiognomy on leaf temperature on clear midsummer days in the Snowy Mountains, south-eastern Australia. Acta Oecologica. 1983;4: 117–124.
28. Körner C, Hiltbrunner E. The 90 ways to describe plant temperature. Perspect Plant Ecol Evol Syst. Elsevier; 2018;30: 16–21. doi: 10.1016/j.ppees.2017.04.004
29. Sklenář P, Kučerová A, Macková J, Romoleroux K. Temperature Microclimates of Plants in a Tropical Alpine Environment: How Much does Growth Form Matter? Arctic, Antarct Alp Res. 2016;48: 61–78. doi: 10.1657/AAAR0014-084
30. Körner C. Alpine Plant Life: Functional Plant Ecology of High Mountain Ecosystems. Springer. 2003. doi: 10.1007/978-3-642-18970-8
31. Sastry A, Barua D. Leaf thermotolerance in tropical trees from a seasonally dry climate varies along the slow-fast resource acquisition spectrum. Sci Rep. Springer US; 2017;7: 1–11. doi: 10.1038/s41598-016-0028-x
32. Wahid A, Gelani S, Ashraf M, Foolad MR. Heat tolerance in plants: An overview. Environmental and Experimental Botany. 2007. pp. 199–223. doi: 10.1016/j.envexpbot.2007.05.011
33. Neuner G, Buchner O, Braun V. Short-term changes in heat tolerance in the alpine cushion plant Silene acaulis ssp. excapa [All.] J. Braun at different altitudes. Plant Biol. 2000;2: 677–683. doi: 10.1055/s-2000-16635
34. Squeo AFA, Rada F, Azocar A, Goldstein G. Freezing Tolerance and Avoidance in High Tropical Andean Plants: Is It Equally Represented in Species with Different Plant Height? Oecologia. 1991;86: 378–382. doi: 10.1007/BF00317604 28312924
35. Squeo FA, Rada F, García C, Ponce M, Rojas A, Azócar A. Cold resistance mechanisms in high desert Andean plants. Oecologia. 1996;105: 552–555. doi: 10.1007/BF00330019 28307149
36. Cavieres LA, Rada F, Azócar A, García-Núñez C, Cabrera HM. Gas exchange and low temperature resistance in two tropical high mountain tree species from the Venezuelan Andes. Acta Oecologica. 2000;21: 203–211. doi: 10.1016/S1146-609X(00)01077-8
37. Rada F, García-Núñez C, Rangel S. Low temperature resistance in saplings and ramets of Polylepis sericea in the Venezuelan Andes. Acta Oecologica. 2009;35: 610–613. doi: 10.1016/j.actao.2009.05.009
38. Sklenář P, Kučerová A, Macek P, Macková J. Does plant height determine the freezing resistance in the páramo plants? Austral Ecol. 2010;35: 929–934. doi: 10.1111/j.1442-9993.2009.02104.x
39. Sklenář P, Kučerová A, Macek P, Macková J. The frost-resistance mechanism in páramo plants is related to geographic origin. 2017;8643. doi: 10.1080/0028825X.2012.706225
40. Sunday JM, Bates AE, Kearney MR, Colwell RK, Dulvy NK, Longino JT, et al. Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation. Proc Natl Acad Sci. 2014;111: 5610–5615. doi: 10.1073/pnas.1316145111 24616528
41. Curtis EM, Knight CA, Petrou K, Leigh A. A comparative analysis of photosynthetic recovery from thermal stress: A desert plant case study. Oecologia. 2014;175: 1051–1061. doi: 10.1007/s00442-014-2988-5 24958368
42. O’sullivan OS, Heskel MA, Reich PB, Tjoelker MG, Weerasinghe LK, Penillard A, et al. Thermal limits of leaf metabolism across biomes. Glob Chang Biol. 2017;23: 209–223. doi: 10.1111/gcb.13477 27562605
43. Meinzer F, Goldstein G. Some Consequences of Leaf Pubescence in the Andean Giant Rosette Plant Espeletia Timotensis. America (NY). 1985;66: 512–520.
44. Cunningham SC, Read J. Foliar temperature tolerance of temperate and tropical evergreen rain forest trees of Australia. Tree Physiol. 2006;26: 1435–1443. doi: 10.1093/treephys/26.11.1435 16877328
45. Curiel Yuste J, Hereş A-M, Ojeda G, Paz A, Pizano C, García-Angulo D, et al. Soil heterotrophic CO2 emissions from tropical high-elevation ecosystems (Páramos) and their sensitivity to temperature and moisture fluctuations. Soil Biology and Biochemistry. 2017. doi: 10.1016/j.soilbio.2017.02.016
46. Krause GH, Winter K, Krause B, Jahns P, García M, Aranda J, et al. High-temperature tolerance of a tropical tree, Ficus insipida: Methodological reassessment and climate change considerations. Funct Plant Biol. 2010;37: 890–900. doi: 10.1071/FP10034
47. Leon-Garcia I V., Lasso E. Heat tolerance in plant leaves Protocol [Internet]. 2019. http://dx.doi.org/10.17504/protocols.io.29fgh3n
48. O’sullivan OS, Heskel MA, Reich PB, Tjoelker MG, Weerasinghe LK, Penillard A, et al. Thermal limits of leaf metabolism across biomes. Glob Chang Biol. 2017;23: 209–223. doi: 10.1111/gcb.13477 27562605
49. Dietrich L, Körner C. Thermal imaging reveals massive heat accumulation in flowers across a broad spectrum of alpine taxa. Alp Bot. 2014;124: 27–35. doi: 10.1007/s00035-014-0123-1
50. IPCC. Climate Change 2014: Synthesis Report. Climate Change 2014: Synthesis. 2014. doi: 10.1256/004316502320517344
51. Smith AP. Bud Temperature in Relation to Nyctinastic Leaf Movement in an Andean Giant Rosette Plant. Biotropica. 1974;6: 263–266. doi: 10.2307/2989670
52. Smith AP. Function of Dead Leaves in Espeletia schultzii (Compositae), and Andeae Caulescent Rosette Species. Biotropica. 1979;11: 43–47. doi: 10.2307/2388171
53. Rada F, Goldstein G, Azocar A, Meinzer F. Freezing avoidance in Andean giant rosette plants. Plant Cell Environ. 1985;8: 501–507. doi: 10.1111/j.1365-3040.1985.tb01685.x
54. Rada F, Goldstein G, Azocar A, Torres F. Supercooling along an Altitudinal Gradient in Espeletia schultzii, a Caulescent Giant Rosette Species. J Exp Bot. 1987;38: 491–497. Available: https://doi.org/10.1093/jxb/38.3.491
55. Zhu L, Bloomfield KJ, Hocart CH, Egerton JJG, O’Sullivan OS, Penillard A, et al. Plasticity of photosynthetic heat tolerance in plants adapted to thermally contrasting biomes. Plant Cell Environ. 2018;41: 1251–1262. doi: 10.1111/pce.13133 29314047
56. Beaumont LJ, Pitman A, Perkins S, Zimmermann NE, Yoccoz NG. Impacts of climate change on the world’s most exceptional ecoregions. PNAS. 2011;108. Available: www.pnas.org/cgi/doi/10.1073/pnas.1007217108
57. Ghalambor CK, Huey RB, Martin PR, Tewksbury JJ, Wang G. Are mountain passes higher in the tropics? Janzen’s hypothesis revisited. Integr Comp Biol. 2006;46: 5–17. doi: 10.1093/icb/icj003 21672718
58. Tewksbury JJ, Huey RB, Deutsch CA. Putting the Heat on Tropical Animals. Science (80-). 2008;320: 1296–1297. doi: 10.1126/science.1159328 18535231
59. Feeley KJ, Silman MR. Land-use and climate change effects on population size and extinction risk of Andean plants. Glob Chang Biol. 2010;16: 3215–3222. doi: 10.1111/j.1365-2486.2010.02197.x
60. Lenoir J, Svenning JC. Climate-related range shifts—a global multidimensional synthesis and new research directions. Ecography (Cop). 2015;38: 15–28. doi: 10.1111/ecog.00967
61. Feeley KJ, Silman MR, Duque A. Where are the tropical plants? A call for better inclusion of tropical plants in studies investigating and predicting the effects of climate change. Front Biogeogr. 2015;7. doi: 10.21425/f57427602
62. Cavieres LA, Badano EI, Sierra-almeida A, Marco A, Molina-montenegro MA. Microclimatic Modifications of Cushion Plants and Their Consequences for Seedling Survival of Native and Non-native Herbaceous Species in the High Andes of Central Chile. Artic, Antart Alp Res. 2007;39: 229–236. https://doi.org/10.1657/1523-0430(2007)39[229:MMOCPA]2.0.CO;2
63. Marcante S, Erschbamer B, Buchner O, Neuner G. Heat tolerance of early developmental stages of glacier foreland species in the growth chamber and in the field. 2014; 747–758. doi: 10.1007/s11258-014-0361-8
64. Briceño VF, Hoyle GL, Nicotra AB. Seeds at risk: How will a changing alpine climate affect regeneration from seeds in alpine areas? Alp Bot. 2015;125: 59–68. doi: 10.1007/s00035-015-0155-1
65. Graae BJ, Vandvik V, Armbruster WS, Eiserhardt WL, Svenning JC, Hylander K, et al. Stay or go—how topographic complexity influences alpine plant population and community responses to climate change. Perspect Plant Ecol Evol Syst. 2017; doi: 10.1016/j.ppees.2017.09.008
66. Ramirez LA, Rada F, Llambí LD. Linking patterns and processes through ecosystem engineering: effects of shrubs on microhabitat and water status of associated plants in the high tropical Andes. Plant Ecol. 2015; 213–225. doi: 10.1007/s11258-014-0429-5
67. Hupp N, Llambí LD, Ramirez LA, Callaway RM. Alpine cushion plants have species-specific effects on microhabitat and community structure in the tropical Andes. J Veg Sci. 2017; 928–938. doi: 10.1111/ijlh.12426
68. Mora MA, Llambí LD, Ramírez L. Giant stem rosettes have strong facilitation effects on alpine plant communities in the tropical Andes. Plant Ecol Divers. Taylor & Francis; 2018; doi: 10.1080/17550874.2018.1507055
69. Cavieres LA, Badano EI, Sierra-Almeida A, Gómez-González S, Molina-Montenegro MA. Positive interactions between alpine plant species and the nurse cushion plant Laretia acaulis do not increase with elevation in the Andes of central Chile. New Phytol. 2006; 59–69. doi: 10.1111/j.1469-8137.2005.01573.x 16390419
70. Körner C, Hiltbrunner E. The 90 ways to describe plant temperature. Perspect Plant Ecol Evol Syst. Elsevier; 2018;30: 16–21. doi: 10.1016/j.ppees.2017.04.004
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