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Facilitative interactions do not wane with warming at high elevations in the Andes

  • Global change ecology - Original research
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Abstract

Positive interactions between species are known to play an important role in the structure and dynamics of alpine plant communities. The balance between negative and positive interactions is known to shift along spatial and temporal gradients, with positive effects prevailing over negative ones as the environmental stress increases. Thus, this balance is likely to be affected by climate change. We hypothesized that increases in temperature (a global warming scenario) should decrease the importance of positive interactions for the survival and growth of alpine plant species. To test this hypothesis, we selected individuals of the native grass species Hordeum comosum growing within the nurse cushion species Azorella madreporica at 3,600 m.a.s.l. in Los Andes (Chile), and performed nurse removal and seedling survival experiments under natural and warmer conditions. For warmer conditions, we used open-top chambers, which increased the temperature by 4 °C. After two growing seasons, we compared the effect of nurse removal on the survival, biomass, and photochemical efficiency of H. comosum individuals under warmer and natural conditions. Nurse removal significantly decreased the survival, biomass, and photochemical efficiency of H. comosum, demonstrating the facilitative effects of nurse cushions. Seedling survival was also enhanced by cushions, even under warmer conditions. However, warmer conditions only partially mitigated the negative effects of nurse removal, suggesting that facilitative effects of cushions do not wane under warmer conditions. Thus, facilitative interactions are vital to the performance and survival of alpine species, and these positive interactions will continue to be important in the warmer conditions of the future in high-alpine habitats.

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References

  • ACIA (2004) Arctic climate impact assessment. Cambridge University Press, Cambridge

    Google Scholar 

  • Anthelme F, Buendia B, Mazoyer C, Dangles O (2012) Unexpected mechanisms sustain the stress gradient hypothesis in a tropical alpine environment. J Veg Sci 23:62–72

    Article  Google Scholar 

  • Antonsson H, Björk RG, Molau U (2009) Nurse plant effect of the cushion plant Silene acaulis (L.) Jacq. in an alpine environment in the subarctic Scandes, Sweden. Plant Ecol Divers 2:17–25

    Article  Google Scholar 

  • Arroyo MTK, Cavieres LA, Peñaloza A, Arroyo-Kalin MA (2003) Positive associations between the cushion plant Azorella monantha (Apiaceae) and alpine plant species in the Chilean Patagonian Andes. Plant Ecol 169:121–129

    Article  Google Scholar 

  • Badano EI, Jones CG, Cavieres LA, Wright JP (2006) Assessing impacts of ecosystem engineers on community organization: a general approach illustrated by effects of a high-Andean cushion plant. Oikos 115:369–385

    Article  Google Scholar 

  • Bahn M, Körner C (2003) Recent increases in summit flora caused by warming in the Alps. Ecol Stud 167:437–441

    Article  Google Scholar 

  • Bertness MD, Callaway RM (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193

    Article  PubMed  CAS  Google Scholar 

  • Brooker RW (2006) Plant–plant interactions and environmental change. New Phytol 171:271–289

    Article  PubMed  Google Scholar 

  • Brooker RW, Callaghan TV (1998) The balance between positive and negative interactions and its relationship to environmental gradient: a model. Oikos 81:196–207

    Article  Google Scholar 

  • Brooker RW, Maestre FT, Callaway RM, Lortie CL, Cavieres LA, Kunstler G, Liancourt P, Tielbörger K, Travis JMJ, Anthelme F, Armas C, Coll L, Corcket E, Delzon S, Forey E, Kikvidze Z, Olofsson J, Pugnaire FI, Quiroz CL, Saccone P, Schiffers K, Seifan M, Touzard B, Michalet R (2008) Facilitation in plant communities: the past, the present and the future. J Ecol 96:18–34

    Article  Google Scholar 

  • Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125

    Article  Google Scholar 

  • Callaway RM (1995) Positive interactions among plants. Bot Rev 61:306–349

    Article  Google Scholar 

  • Callaway RM (2007) Positive interactions and interdependence in plant communities. Springer, Berlin

    Google Scholar 

  • Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnarie FI, Newingham B, Aschehoug ET, Armas C, Kikodze D, Cook BJ (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848

    Article  PubMed  CAS  Google Scholar 

  • Cannone N, Sgorbati S, Guglielmin M (2007) Unexpected impact of climate change on alpine vegetation. Front Ecol Environ 5:360–364

    Article  Google Scholar 

  • Casanova-Katny MA, Torres-Mellado A, Goetz P, Cavieres LA (2011) The best for the guest: high Andean nurse cushions of Azorella madreporica enhance arbuscular mycorrhizal status in associated plant species. Mycorrhiza 21:613–622

    Article  PubMed  Google Scholar 

  • Cavieres LA, Badano EI (2009) Do facilitative interactions increase species richness at the entire community level? J Ecol 97:1181–1191

    Article  Google Scholar 

  • Cavieres LA, Peñaloza A, Arroyo MTK (2000) Altitudinal vegetation belts in the high Andes of central Chile (33°S). Revista Chilena de Historia Natural 73:331–344

    Article  Google Scholar 

  • Cavieres LA, Arroyo MTK, Peñaloza A, Molina-Montenegro M, Torres C (2002) Nurse effect of Bolax gummnifera cushion plants in the alpine vegetation of the Chilean Patagonian Andes. J Veg Sci 13:547–554

    Google Scholar 

  • Cavieres LA, Badano EI, Sierra-Almeida A, Gómez-González S, Molina-Montenegro M (2006) 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 169:59–69

    Article  PubMed  Google Scholar 

  • Cavieres LA, Badano EI, Sierra-Almeida A, Molina-Montenegro M (2007) Microclimatic modifications of cushion plants and their consequences for seedlings survival of native and non-native plants in the high-Andes of central Chile. Arct Antarct Alp Res 39:229–236

    Article  Google Scholar 

  • Cavieres LA, Quiroz CL, Molina-Montenegro MA (2008) Facilitation of the non-native Taraxacum officinale by native nurse cushion species in the high-Andes of central Chile: are there differences between nurses? Funct Ecol 22:148–156

    Article  Google Scholar 

  • Choler P, Michalet R, Callaway RM (2001) Facilitation and competition on gradients in alpine plant communities. Ecology 82:3295–3308

    Article  Google Scholar 

  • CONAMA (2006) Estudio de la variabilidad climática en Chile para el siglo XXI. Facultad de Ciencias Físicas y Matemáticas, Universidad de Chile, Departamento de Geofísica, Santiago

  • Cui X, Tang Y, Gu S, Nishimura S, Shi S, Zhao X (2003) Photosynthetic depression in relation to plant architecture in two alpine herbaceous species. Environ Exp Bot 50:125–135

    Article  CAS  Google Scholar 

  • Dormann C, Van der Wal R, Woodin SJ (2004) Neighbour identity modifies effects of elevated temperature on plant performance in the high Arctic. Glob Change Biol 10:1587–1598

    Article  Google Scholar 

  • Dullinger S, Kleinbauer I, Pauli H, Gottfried M, Brooker R, Nagy L, Theurillat JP, Holten JI, Abdaladze O, Benito JL, Borel JL, Coldea G, Ghosn D, Kanka R, Merzouki A, Klettner C, Moiseev P, Molau U, Reiter K, Rossi G, Stanisci A, Tomaselli M, Unterlugauer P, Vittoz P, Grabherr G (2007) Weak and variable relationships between environmental severity and small-scale co-occurrence in alpine plant communities. J Ecol 95:1284–1295

    Article  Google Scholar 

  • Fajardo A, Quiroz CL, Cavieres LA (2008) Spatial patterns in cushion-dominated plant communities of the high Andes of central Chile: how frequent are positive associations? J Veg Sci 19:87–96

    Article  Google Scholar 

  • Forbis TA (2003) Seedling demography in an alpine ecosystem. Am J Bot 90:1197–1206

    Article  PubMed  Google Scholar 

  • Fox GA (1993) Failure-time analysis: emergence, flowering survivorship, and other waiting time. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Chapman and Hall, New York, pp 253–266

  • Friend AD, Woodward FI (1990) Evolutionary and ecophysiological responses of mountain plants to the growing season environment. Adv Ecol Res 20:59–124

    Article  Google Scholar 

  • Germino MJ, Smith WK (2000) High resistance to low-temperature photoinhibition in two alpine, snowbank species. Physiol Plant 110:89–95

    Article  CAS  Google Scholar 

  • Germino MJ, Smith WK (2001) Relative importance of microhabitat, plant form and photosynthetic physiology to carbon gain in two alpine herbs. Funct Ecol 15:243–251

    Article  Google Scholar 

  • Grabherr G, Gottfried M, Pauli H (1994) Climate effects on mountain plants. Nature 369:448

    Article  Google Scholar 

  • Guisan A, Theurillat JP (2000) Assessing alpine vulnerability to climate change, a modelling perspective. Integr Assess 1:307–320

    Article  Google Scholar 

  • Hallinger M, Manthey M, Wilmking M (2010) Establishing a missing link: warm summers and winter snow cover promote shrubs expansion into alpine tundra in Scandinavia. New Phytol 186:890–899

    Article  PubMed  Google Scholar 

  • Henry GHR, Molau U (1997) Tundra plants and climate change: the International Tundra Experiment (ITEX). Glob Change Biol 3:1–9

    Article  Google Scholar 

  • Hobbie SE, Shevtsova A, Chapin FS (1999) Plant responses to species removal and experiment warming in Alaskan tussock tundra. Oikos 84:417–434

    Article  Google Scholar 

  • Klanderud K (2005) Climate change effects on species interactions in an alpine plant community. J Ecol 93:127–137

    Article  Google Scholar 

  • Klanderud K, Totland O (2005) The relative importance of neighbours and abiotic environmental conditions for population dynamic parameters of two alpine plant species. J Ecol 93:493–501

    Article  Google Scholar 

  • Klein JA, Harte J, Zhao ZQ (2004) Experimental warming causes large and rapid species loss, dampened by simulated gazing, on the Tibetan plateau. Ecol Lett 7:1170–1179

    Article  Google Scholar 

  • Körner C (2003) Alpine plant life (2nd ed). Springer, Berlin

  • Lambers H, Chapin FS, Pons TL (2008) Plant physiological ecology, 2nd edn. Springer, New York

  • le Roux PC, McGeoch MA (2008) Spatial variation in plant interactions across a severity gradient in the sub-Antarctic. Oecologia 155:831–844

    Article  PubMed  Google Scholar 

  • Maestre FT, Callaway RM, Valladares F, Lortie C (2009) Refining the stress-gradient hypothesis for competition and facilitation in plant communities. J Ecol 97:199–205

    Article  Google Scholar 

  • Marion GM, Henry GHR, Freckman DW, Johnstone J, Jones G, Jones MH, Lévesque E, Molau U, Molgaard P, Parsons AN, Svoboda J, Virginia RA (1997) Open-top designs for manipulating field temperature in high-latitude ecosystems. Glob Change Biol 3:20–32

    Article  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  PubMed  CAS  Google Scholar 

  • McMaster GS, Wilhelm WW (1997) Growing degree-days: one equation, two interpretations. Agric For Meteorol 87:291–300

    Article  Google Scholar 

  • Michalet R, Brooker RW, Cavieres LA, Kikvidze Z, Lortie CJ, Pugnaire FI, Valiente-Banuet A, Callaway RM (2006) Do biotic interactions shape both sides of the humped-back model of species richness in plant communities? Ecol Lett 9:767–773

    Article  PubMed  Google Scholar 

  • Nicora EG (1978) Graminae. In: Correa MN (ed) Flora Patagónica, Tomo VIII, Parte III. Colección Científica del Instituto Nacional de Tecnología Agropecuaria (INTA), Buenos Aires

  • Nogués-Bravo D, Araújo MD, Errea MP, Martínez-Rica JP (2007) Exposure of global mountain systems to climate warming during the 21st century. Glob Environ Change 17:420–428

    Google Scholar 

  • Nuñez C, Aizen M, Ezcurra C (1999) Species associations and nurse plant effects in patches of high-Andean vegetation. J Veg Sci 10:357–364

    Article  Google Scholar 

  • Pysek P, Lyska J (1991) Colonization of Sibbaldia tetrandra cushions on alpine scree in the Palmiro Alai mountains, Central Asia. Arct Alp Res 23:263–272

    Article  Google Scholar 

  • Quiroz CL, Badano EI, Cavieres LA (2009) Floristic changes induced by cushion species Azorella madreporica at two contrasting elevations. Revista Chilena de Historia Natural 82:171–184

    Google Scholar 

  • Rixen C, Mulder CPH (2009) Species removal and experimental warming in a subarctic tundra plant community. Oecologia 161:173–186

    Article  PubMed  Google Scholar 

  • Santibañez F, Uribe JM (1990) Atlas agroclimático de Chile. Universidad de Chile, Facultad de Ciencias Agrarias y Forestales, Santiago

  • Schreiber U, Bilger W, Neubauer C (1995) Chlorophyll fluorescence as a non-intrusive indicator for a rapid assessment of in vivo photosynthesis. In: Schulze E-D, Caldwell MM (eds) Ecophysiology of photosynthesis. Springer, Berlin, pp 49–70

  • Shetsova A, Haukioja E, Ojala A (1997) Growth response of subarctic dwarf shrubs, Empetrum nigrum and Vaccinium vitis-idaea, to manipulated environmental conditions and species removal. Oikos 78:440–458

    Article  Google Scholar 

  • Sierra-Almeida A, Cavieres LA, Bravo LA (2010) Freezing resistance of high-elevation plant species is not related to their height or growth-form in the Central Chilean Andes. Environ Exp Bot 69:273–278

    Article  Google Scholar 

  • Streb P, Feierabend J, Bligny R (1997) Resistance to photoinhibition of photosystem II and catalase and antioxidative protection in high mountain plants. Plant Cell Environ 20:1030–1040

    Article  CAS  Google Scholar 

  • Venn S, Morgan JW (2009) Patterns in alpine seedling emergence and establishment across a stress gradient of mountain summits in south-eastern Australia. Plant Ecol Divers 2:5–16

    Article  Google Scholar 

  • Venn S, Morgan JW, Green PT (2009) Do facilitative interactions with neighboring plants assist the growth of seedlings at high altitudes in Alpine Australia? Arct Antarct Alp Res 41:381–387

    Article  Google Scholar 

  • Walker MD, Wahren CH, Hollister RD (2006) Plant community responses to experimental warming across the tundra biome. Proc Natl Acad Sci USA 103:1342–1346

    Google Scholar 

  • Wipf S, Rixen C, Mulder CPH (2006) Advanced snowmelt causes shift toward positive neighbour interactions in a subarctic tundra community. Glob Change Biol 12:1–11

    Article  Google Scholar 

  • Yang Y, Niu Y, Cavieres LA, Sun H (2010) Positive associations between the cushion plant Arenaria polytrichoides (Caryophyllaceae) and other alpine plant species increases with altitude in the Sino-Himalayas. J Veg Sci 21:1048–1057

    Article  Google Scholar 

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Acknowledgments

We thank the staff of La Parva and Valle Nevado Ski Resort for their help with the access to our study sites. We also thank Victor and Angélica Rojas from Valparaiso Lodge, our second home. This study was supported by FONDECYT 1060710 and 1090389. Additional support was provided by projects P05-002 F ICM of the Millennium Scientific Initiative of the Ministry of Economy, Public Works, and Tourism of the Chilean Government, and CONICYT PFB-23, supporting the Center for Advanced Studies in Ecology and Research on Biodiversity (IEB).

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Authors and Affiliations

  1. ECOBIOSIS, Departamento de Botánica, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Concepción, Chile

    Lohengrin A. Cavieres & Angela Sierra-Almeida

  2. Instituto de Ecología y Biodiversidad (IEB), Santiago, Chile

    Lohengrin A. Cavieres & Angela Sierra-Almeida

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  1. Lohengrin A. Cavieres
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  2. Angela Sierra-Almeida
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Correspondence to Lohengrin A. Cavieres.

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Communicated by Allan Green.

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Cavieres, L.A., Sierra-Almeida, A. Facilitative interactions do not wane with warming at high elevations in the Andes. Oecologia 170, 575–584 (2012). https://doi.org/10.1007/s00442-012-2316-x

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