Facilitative interactions are defined as positive effects of one species on another, but bidirectional feedbacks may be positive, neutral, or negative. Understanding the bidirectional nature of these interactions is a fundamental prerequisite for the assessment of the potential evolutionary consequences of facilitation. In a global study combining observational and experimental approaches, we quantified the impact of the cover and richness of species associated with alpine cushion plants on reproductive traits of the benefactor cushions. We found a decline in cushion seed production with increasing cover of cushion-associated species, indicating that being a benefactor came at an overall cost. The effect of cushion-associated species was negative for flower density and seed set of cushions, but not for fruit set and seed quality. Richness of cushion-associated species had positive effects on seed density and modulated the effects of their abundance on flower density and fruit set, indicating that the costs and benefits of harboring associated species depend on the composition of the plant assemblage. Our study demonstrates 'parasitic' interactions among plants over a wide range of species and environments in alpine systems, and we consider their implications for the possible selective effects of interactions between benefactor and beneficiary species.

D Research Institute Ilia State University 3 5 Cholokashvili Av Tbilisi 0162 Georgia

Departamento de Botánica Facultad de Ciencias Naturales y Oceanográficas Universidad de Concepción Casilla 160 C Concepción Chile

Department of Biological Sciences Minnesota State University Mankato MN USA

Department of Biology York University 4700 Keele Street Toronto ON M3J 1P3 Canada

Department of Botany Faculty of Science University of South Bohemia Branisovska 31 CZ 370 05 Ceske Budejovice Czech Republic

Department of Conservation Ecology and Entomology Stellenbosch University Private Bag X1 Matieland 7602 South Africa

Department of Forest and Conservation Sciences University of British Columbia 2621 2424 Main Mall Vancouver BC V6T 1Z4 Canada

Department of Geosciences and Geography University of Helsinki PO Box 64 00014 Helsinki Finland

Department TeSAF University of Padova Viale dell'Universitá 16 35020 Legnaro Italy

Division of Biological Sciences and the Institute on Ecosystems University of Montana Missoula MT 59812 USA

Estación Experimental de Zonas Áridas Consejo Superior de Investigaciones Científicas EEZA CSIC Carretera de Sacramento s n La Cañada de San Urbano 04120 Almería Spain

Institut de Recherche pour le Développement UMR AMAP Boulevard de la Lironde TA A 51 PS2 34398 Montpellier Cedex 5 France

Instituto de Ecología y Biodiversidad Casilla 653 Santiago Chile

Key Laboratory of Ecohydrology of Inland River Basin Cold and Arid Regions Environmental and Engineering Research Institute Chinese Academy of Sciences 320 Donggang West Road Lanzhou 730000 China

Merriam Powell Center for Environmental Research Northern Arizona University PO Box 6077 Flagstaff AZ 86011 USA

MOE Key Laboratory of Cell Activities and Stress Adaptations School of Life Sciences Lanzhou University Lanzhou 730000 China

The James Hutton Institute Craigiebuckler Aberdeen AB15 8QH UK

University of Bordeaux UMR CNRS 5805 EPOC 33405 Talence France

University of Bordeaux UMR INRA 1202 BIOGECO 33405 Talence France

Komentář v

New Phytol. 2014 Apr;202(1):4-6. doi: 10.1111/nph.12740. PubMed

Zobrazit více v PubMed

Armas C, Pugnaire FI. 2005. Plant interactions govern population dynamics in a semi-arid plant community. Journal of Ecology 93: 978-989.

Ayre DJ, Whelan RJ. 1989. Factors controlling fruit set in hermaphroditic plants: studies with the Australian Proteaceae. Trends in Ecology and Evolution 4: 267-272.

Bates D, Maechler M, Bolker B. 2011. lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-42. [WWW document] URL: http://CRAN.R-project.org/package=lme4 [accessed 15 November 2011].

Bronstein JL. 2009. The evolution of facilitation and mutualism. Journal of Ecology 97: 1160-1170.

Brooker RW, Callaway RM. 2009. Facilitation in the conceptual melting pot. Journal of Ecology 97: 1117-1120.

Bruno JF, Stachowicz JJ, Bertness MD. 2003. Inclusion of facilitation into ecological theory. Trends in Ecology and Evolution 18: 119-125.

Butterfield BJ, Cavieres LA, Callaway RM, Cook BJ, Kikvidze Z, Lortie CJ, Michalet R, Pugnaire FI, Schöb C, Xiao S et al. 2013. Alpine cushion plants inhibit the loss of phylogenetic diversity in severe environments. Ecology Letters 16: 478-486.

Callaway RM. 2007. Positive interactions and interdependence in plant communities. Dordrecht, the Netherlands: Springer.

Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET et al. 2002. Positive interactions among alpine plants increase with stress. Nature 417: 844-848.

Cavieres LA, Badano EI, Sierra-Almeida A, Gómez S, Molina-Montenegro MA. 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 Phytologist 169: 59-69.

Cavieres LA, Brooker RW, Butterfield BJ, Cook BJ, Kikvidze Z, Lortie CJ, Michalet R, Pugnaire FI, Schöb C, Xiao S et al. 2013. Facilitative plant interactions and climate simultaneously drive alpine plant diversity. Ecology Letters. doi: 10.1111/ele.12217.

Cranston BH, Callaway RM, Monks A, Dickinson KJM. 2012. Gender and abiotic stress affect community-scale intensity of facilitation and its costs. Journal of Ecology 100: 915-922.

Ehlers BK, Thompson J. 2004. Do co-occurring plant species adapt to one another? The response of Bromus erectus to the presence of different Thymus vulgaris chemotypes. Oecologia 141: 511-518.

Fargione JE, Tilman D. 2005. Diversity decreases invasion via both sampling and complementarity effects. Ecology Letters 8: 604-611.

Feldman TS, Morris WF, Wilson WG. 2004. When can two plant species facilitate each other's pollination? Oikos 105: 197-207.

Flores-Martínez A, Ezcurra E, Sánchez-Colón S. 1994. Effect of Neobuxbaumia tetetzo on growth and fecundity of its nurse plant Mimosa luisana. Journal of Ecology 82: 325-330.

Fox J. 2003. Effect displays in R for Generalised Linear Models. Journal of Statistical Software 8: 1-27.

Fox J, Weisberg S. 2011. An R companion to applied regression, 2nd edn. Thousand Oaks, CA, USA: Sage.

Fraser LH, Henry HAL, Carlyle CN, White SR, Beierkuhnlein C, Cahill CF Jr, Casper BB, Cleland C, Collins SL, Dukes JS et al. 2013. Coordinated distributed experiments: an emerging tool for testing global hypotheses in ecology and environmental science. Frontiers in Ecology and the Environment 11: 147-155.

Guitián J. 1993. Why Prunus mahaleb (Rosaceae) produced more flowers than fruits. American Journal of Botany 80: 1305-1309.

Harper JL, Lovell PH, Moore KG. 1970. The shapes and sizes of seeds. Annual Review of Ecology and Systematics 1: 327-355.

Holzapfel C, Mahall BE. 1999. Bidirectional facilitation and interference between shrubs and annuals in the Mojave desert. Ecology 80: 1747-1761.

Keddy PA. 2001. Competition, 2nd edn. Dordrecht, the Netherlands: Kluwer.

Körner C. 2003. Alpine plant life, 2nd edn. Berlin, Germany: Springer.

Lee TD. 1988. Patterns of fruit and seed production. In: Lovett Doust J, Lovett Doust L, eds. Plant reproductive ecology: patterns and strategies. Oxford, UK: Oxford University Press, 179-202.

Leist N, Krämer S, Pfäfflin J. 2003. ISTA working sheets on tetrazolium testing, 1st edn. Bassersdorf, Switzerland: ISTA.

McAuliffe JR. 1984. Sahuaro-nurse tree associations in the Sonoran Desert: competitive effects of the sahuaros. Oecologia 64: 319-321.

Michalet R, Xiao S, Touzard B, Smith DS, Cavieres LA, Callaway RM, Whitham TG. 2011. Phenotypic variation in nurse traits and community feedbacks define an alpine community. Ecology Letters 14: 433-443.

Mitchell RJ, Flanagan RJ, Brown BJ, Waser NM, Karron JD. 2009. New frontiers in competition for pollination. Annals of Botany 103: 1403-1413.

Molau U. 1997. Age-related growth and reproduction in Diapensia lapponica, an arctic-alpine cushion plant. Nordic Journal of Botany 17: 225-234.

Molenda O, Reid A, Lortie CJ. 2012. The alpine cushion plant Silene acaulis as foundation species: a bug's-eye view to facilitation and microclimate. PLoS ONE 7: e37223.

Morris WF, Doak DF. 1998. Life history of a long-lived gynodioecious plant, Silene acaulis (Caryophyllaceae), inferred from size-based population projection matrices. American Journal of Botany 85: 784-793.

Muñoz AA, Cavieres LA. 2008. The presence of a showy invasive plant disrupts pollinator service and reproductive output in native alpine species only at high densities. Journal of Ecology 96: 459-467.

Odum EP. 1968. Fundamentals of ecology, 2nd edn. London, UK: W.B. Saunders.

Pugnaire FI, Haase P, Puigdefábregas J. 1996. Facilitation between higher plant species in a semiarid environment. Ecology 77: 1420-1426.

R Core Team. 2013. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. [WWW document] URL: http://www.R-project.org/.

Reid AM, Lamarque LJ, Lortie CJ. 2010. A systematic review of the recent ecological literature on cushion plants: champions of plant facilitation. Web Ecology 10: 44-49.

Roughgarden J, Diamond J. 1986. The role of species interactions in community ecology. In: Diamond J, Chase TJ, eds. Community ecology. New York, NY, USA: Harper and Row Publishers Inc., 333-343.

Samson DA, Werk KS. 1986. Size-dependent effects in the analysis of reproductive effort in plants. The American Naturalist 127: 667-680.

Sarkar D. 2008. Lattice: multivariate data visualization with R. New York, NY, USA: Springer.

Schöb C, Butterfield BJ, Pugnaire FI. 2012. Foundation species influence trait-based community assembly. New Phytologist 196: 824-834.

Schöb C, Prieto I, Armas C, Pugnaire FI. 2013. Consequences of facilitation: one plant's benefit is another plant's cost. Functional Ecology. doi: 10.1111/1365-2435.12185.

Stachowicz JJ. 2001. Mutualism, facilitation, and the structure of ecological communities. BioScience 51: 235-246.

Stephenson AG. 1981. Flower and fruit abortion: proximate causes and ultimate functions. Annual Review of Ecology and Systematics 12: 253-279.

Stöcklin J. 1997. Competition and the compensatory regulation of fruit and seed set in the perennial herb Epilobium dodonaei (Onagraceae). American Journal of Botany 84: 763-768.

Thorpe AS, Aschehoug ET, Atwater DZ, Callaway RM. 2011. Interactions among plants and evolution. Journal of Ecology 99: 729-740.

Valiente-Banuet A, Rumebe AV, Verdú M, Callaway RM. 2006. Modern Quaternary plant lineages promote diversity through facilitation of ancient Tertiary lineages. Proceedings of the National Academy of Sciences, USA 103: 16812-16817.

Valiente-Banuet A, Vite F, Zavala-Hurtado JA. 1991. Interaction between the cactus Neobuxbaumia tetetzo and the nurse shrub Mimosa luisana. Journal of Vegetation Science 2: 11-14.

Violle C, Castro H, Richarte J, Navas ML. 2009. Intraspecific seed trait variations and competition: passive or adaptive response? Functional Ecology 23: 612-620.

Weiner J. 1988. The influence of competition on plant reproduction. In: Lovett Doust J, Lovett Doust L, eds. Plant reproductive ecology: patterns and strategies. Oxford, UK: Oxford University Press, 228-245.

Wirth LR, Waser NM, Graf R, Gugerli F, Landergott U, Erhardt A, Linder HP, Holderegger R. 2011. Effects of floral neighborhood on seed set and degree of outbreeding in a high-alpine cushion plant. Oecologia 167: 427-434.

Functionally distinct assembly of vascular plants colonizing alpine cushions suggests their vulnerability to climate change

Quantifying the effects of ecological constraints on trait expression using novel trait-gradient analysis parameters