, Volume 170, Issue 2, pp 575–584 | Cite as

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

Global change ecology - Original research


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.


Facilitation Positive interactions Climate change Global warming Nurse effect Cushion plants Neighbor removal Photochemical efficiency Alpine 

Supplementary material

442_2012_2316_MOESM1_ESM.doc (2.1 mb)
Supplementary material 1 (DOC 2101 kb)


  1. ACIA (2004) Arctic climate impact assessment. Cambridge University Press, CambridgeGoogle Scholar
  2. Anthelme F, Buendia B, Mazoyer C, Dangles O (2012) Unexpected mechanisms sustain the stress gradient hypothesis in a tropical alpine environment. J Veg Sci 23:62–72CrossRefGoogle Scholar
  3. 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 2:17–25CrossRefGoogle Scholar
  4. 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 169:121–129CrossRefGoogle Scholar
  5. 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 115:369–385CrossRefGoogle Scholar
  6. Bahn M, Körner C (2003) Recent increases in summit flora caused by warming in the Alps. Ecol Stud 167:437–441CrossRefGoogle Scholar
  7. Bertness MD, Callaway RM (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193PubMedCrossRefGoogle Scholar
  8. Brooker RW (2006) Plant–plant interactions and environmental change. New Phytol 171:271–289PubMedCrossRefGoogle Scholar
  9. Brooker RW, Callaghan TV (1998) The balance between positive and negative interactions and its relationship to environmental gradient: a model. Oikos 81:196–207CrossRefGoogle Scholar
  10. 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 96:18–34CrossRefGoogle Scholar
  11. Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125CrossRefGoogle Scholar
  12. Callaway RM (1995) Positive interactions among plants. Bot Rev 61:306–349CrossRefGoogle Scholar
  13. Callaway RM (2007) Positive interactions and interdependence in plant communities. Springer, BerlinGoogle Scholar
  14. 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 417:844–848PubMedCrossRefGoogle Scholar
  15. Cannone N, Sgorbati S, Guglielmin M (2007) Unexpected impact of climate change on alpine vegetation. Front Ecol Environ 5:360–364CrossRefGoogle Scholar
  16. 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 21:613–622PubMedCrossRefGoogle Scholar
  17. Cavieres LA, Badano EI (2009) Do facilitative interactions increase species richness at the entire community level? J Ecol 97:1181–1191CrossRefGoogle Scholar
  18. Cavieres LA, Peñaloza A, Arroyo MTK (2000) Altitudinal vegetation belts in the high Andes of central Chile (33°S). Revista Chilena de Historia Natural 73:331–344CrossRefGoogle Scholar
  19. 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 13:547–554Google Scholar
  20. 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 169:59–69PubMedCrossRefGoogle Scholar
  21. 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 39:229–236CrossRefGoogle Scholar
  22. 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 22:148–156CrossRefGoogle Scholar
  23. Choler P, Michalet R, Callaway RM (2001) Facilitation and competition on gradients in alpine plant communities. Ecology 82:3295–3308CrossRefGoogle Scholar
  24. 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, SantiagoGoogle Scholar
  25. 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 50:125–135CrossRefGoogle Scholar
  26. 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 10:1587–1598CrossRefGoogle Scholar
  27. 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 95:1284–1295CrossRefGoogle Scholar
  28. 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 19:87–96CrossRefGoogle Scholar
  29. Forbis TA (2003) Seedling demography in an alpine ecosystem. Am J Bot 90:1197–1206PubMedCrossRefGoogle Scholar
  30. 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 253–266Google Scholar
  31. Friend AD, Woodward FI (1990) Evolutionary and ecophysiological responses of mountain plants to the growing season environment. Adv Ecol Res 20:59–124CrossRefGoogle Scholar
  32. Germino MJ, Smith WK (2000) High resistance to low-temperature photoinhibition in two alpine, snowbank species. Physiol Plant 110:89–95CrossRefGoogle Scholar
  33. Germino MJ, Smith WK (2001) Relative importance of microhabitat, plant form and photosynthetic physiology to carbon gain in two alpine herbs. Funct Ecol 15:243–251CrossRefGoogle Scholar
  34. Grabherr G, Gottfried M, Pauli H (1994) Climate effects on mountain plants. Nature 369:448CrossRefGoogle Scholar
  35. Guisan A, Theurillat JP (2000) Assessing alpine vulnerability to climate change, a modelling perspective. Integr Assess 1:307–320CrossRefGoogle Scholar
  36. 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 186:890–899PubMedCrossRefGoogle Scholar
  37. Henry GHR, Molau U (1997) Tundra plants and climate change: the International Tundra Experiment (ITEX). Glob Change Biol 3:1–9CrossRefGoogle Scholar
  38. Hobbie SE, Shevtsova A, Chapin FS (1999) Plant responses to species removal and experiment warming in Alaskan tussock tundra. Oikos 84:417–434CrossRefGoogle Scholar
  39. Klanderud K (2005) Climate change effects on species interactions in an alpine plant community. J Ecol 93:127–137CrossRefGoogle Scholar
  40. 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 93:493–501CrossRefGoogle Scholar
  41. 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 7:1170–1179CrossRefGoogle Scholar
  42. Körner C (2003) Alpine plant life (2nd ed). Springer, BerlinGoogle Scholar
  43. Lambers H, Chapin FS, Pons TL (2008) Plant physiological ecology, 2nd edn. Springer, New YorkGoogle Scholar
  44. le Roux PC, McGeoch MA (2008) Spatial variation in plant interactions across a severity gradient in the sub-Antarctic. Oecologia 155:831–844PubMedCrossRefGoogle Scholar
  45. Maestre FT, Callaway RM, Valladares F, Lortie C (2009) Refining the stress-gradient hypothesis for competition and facilitation in plant communities. J Ecol 97:199–205CrossRefGoogle Scholar
  46. 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 3:20–32CrossRefGoogle Scholar
  47. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668PubMedCrossRefGoogle Scholar
  48. McMaster GS, Wilhelm WW (1997) Growing degree-days: one equation, two interpretations. Agric For Meteorol 87:291–300CrossRefGoogle Scholar
  49. 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 9:767–773PubMedCrossRefGoogle Scholar
  50. Nicora EG (1978) Graminae. In: Correa MN (ed) Flora Patagónica, Tomo VIII, Parte III. Colección Científica del Instituto Nacional de Tecnología Agropecuaria (INTA), Buenos AiresGoogle Scholar
  51. 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 17:420–428Google Scholar
  52. Nuñez C, Aizen M, Ezcurra C (1999) Species associations and nurse plant effects in patches of high-Andean vegetation. J Veg Sci 10:357–364CrossRefGoogle Scholar
  53. Pysek P, Lyska J (1991) Colonization of Sibbaldia tetrandra cushions on alpine scree in the Palmiro Alai mountains, Central Asia. Arct Alp Res 23:263–272CrossRefGoogle Scholar
  54. Quiroz CL, Badano EI, Cavieres LA (2009) Floristic changes induced by cushion species Azorella madreporica at two contrasting elevations. Revista Chilena de Historia Natural 82:171–184Google Scholar
  55. Rixen C, Mulder CPH (2009) Species removal and experimental warming in a subarctic tundra plant community. Oecologia 161:173–186PubMedCrossRefGoogle Scholar
  56. Santibañez F, Uribe JM (1990) Atlas agroclimático de Chile. Universidad de Chile, Facultad de Ciencias Agrarias y Forestales, SantiagoGoogle Scholar
  57. 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 49–70Google Scholar
  58. 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 78:440–458CrossRefGoogle Scholar
  59. 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 69:273–278CrossRefGoogle Scholar
  60. 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 20:1030–1040CrossRefGoogle Scholar
  61. 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 2:5–16CrossRefGoogle Scholar
  62. 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 41:381–387CrossRefGoogle Scholar
  63. Walker MD, Wahren CH, Hollister RD (2006) Plant community responses to experimental warming across the tundra biome. Proc Natl Acad Sci USA 103:1342–1346Google Scholar
  64. Wipf S, Rixen C, Mulder CPH (2006) Advanced snowmelt causes shift toward positive neighbour interactions in a subarctic tundra community. Glob Change Biol 12:1–11CrossRefGoogle Scholar
  65. 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 21:1048–1057CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Lohengrin A. Cavieres
    • 1
    • 2
  • Angela Sierra-Almeida
    • 1
    • 2
  1. 1.ECOBIOSIS, Departamento de Botánica, Facultad de Ciencias Naturales y OceanográficasUniversidad de ConcepciónConcepciónChile
  2. 2.Instituto de Ecología y Biodiversidad (IEB)SantiagoChile

Personalised recommendations