BACKGROUND AND AIMS: The stress gradient hypothesis (SGH), the view that competition prevails in undisturbed and productive environments, and shifts to facilitation in disturbed or stressful environments, has become a central paradigm in ecology. However, an alternative view proposes that the relationship between biotic interactions and environmental severity should be unimodal instead of monotonic. Possible causes of discrepancies between these two views were examined in the high elevation desert of the arid Trans-Himalayas. METHODS: A putative nurse species and its associated plant community was surveyed over its entire elevation range, spanning from alpine to desert vegetation belts. The results were analysed at the community level (vegetation cover and species richness), considering the distinction between the intensity and the importance of biotic interactions. Interactions at the species level (pairwise interactions) were also considered, i.e. the variation of biotic interactions within the niche of a species, for which the abundance (species cover) and probability of occurrence (presence/absence) for the most widespread species along the gradient were distinguished. KEY RESULTS: Overall, facilitation was infrequent in our study system; however, it was observed for the two most widespread species. At the community level, the intensity and importance of biotic interactions showed a unimodal pattern. The departure from the prediction of the SGH happened abruptly where the nurse species entered the desert vegetation belt at the lowest elevation. This abrupt shift was attributed to the turnover of species with contrasting tolerances. At the species level, however, facilitation increased consistently as the level of stress increases and individuals deviate from their optimum (increasing strain). CONCLUSION: While the stress gradient hypothesis was not supported along our elevation gradient at the community level, the strain gradient hypothesis, considering how species perceive the ambient level of stress and deviate from their optimum, provided a parsimonious explanation for the outcome of plant-plant interactions at both scales.

Departamento de Biología y Geología Física y Química Inorgánica Escuela Superior de Ciencias Experimentales y Tecnología Universidad Rey Juan Carlos C Tulipán s n 28933 Móstoles Spain

Department of Botany Faculty of Science University of South Bohemia Na Zlate stoce 1 370 05 Ceske Budejovice Czech Republic

Institute of Botany Czech Academy of Sciences Dukelská 135 379 82 Trebon Czech Republic

WSL Institute for Snow and Avalanche Research SLF Davos Dorf Switzerland

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Armas C, Ordiales R, Pugnaire FI.. 2004. Measuring plant interactions: a new comparative index. Ecology 85: 2682–2686.

Armas C, Rodríguez-Echeverría S, Pugnaire FI.. 2011. A field test of the stress-gradient hypothesis along an aridity gradient: facilitation and the stress-gradient hypothesis. Journal of Vegetation Science 22: 818–827.

de Bello F, Doležal J, Dvorský M, et al.2011. Cushions of Thylacospermum caespitosum (Caryophyllaceae) do not facilitate other plants under extreme altitude and dry conditions in the north-west Himalayas. Annals of Botany 108: 567–573. PubMed PMC

Bertness MD, Callaway R.. 1994. Positive interactions in communities. Trends in Ecology and Evolution 9: 191–193. PubMed

Bertness MD, Gough L, Shumway SW.. 1992. Salt tolerances and the distribution of fugitive salt marsh plants. Ecology 73: 1842–1851.

ter Braak CJF, Smilauer P.. 2012. Canoco reference manual and user’s guide: sofware for ordination (version 5.0). Ithaca, NY: Microcomputer Power.

Brooker R, Kikvidze Z, Pugnaire FI, et al.2005. The importance of importance. Oikos 109: 63–70.

Brooker RW, Maestre FT, Callaway RM, et al.2008. Facilitation in plant communities: the past, the present, and the future. Journal of Ecology 96: 18–34.

Brooker R, Kikvidze Z, Kunstler G, Liancourt P, Seifan M.. 2013. The concept and measurement of importance: a comment on Rees et al. 2012. Journal of Ecology 101: 1369–1378.

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

Callaway RM. 2007. Positive interactions and interdependence in plant communities. Berlin: Springer-Verlag.

Cavieres LA, Badano EI, Sierra-Almeida A, Gómez-González 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. PubMed

Cavieres LA, Brooker RW, Butterfield BJ, et al.2014. Facilitative plant interactions and climate simultaneously drive alpine plant diversity. Ecology Letters 17: 193–202. PubMed

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

Dvorský M, Doležal J, de Bello F, Klimešová J, Klimeš L.. 2011. Vegetation types of East Ladakh: species and growth form composition along main environmental gradients. Applied Vegetation Science 14: 132–147.

Dvorský M, Doležal J, Kopecký M, et al.2013. Testing the stress-gradient hypothesis at the roof of the world: effects of the cushion plant Thylacospermum caespitosum on species assemblages. PLoS One 8: e53514. PubMed PMC

Gaucherand S, Liancourt P, Lavorel S.. 2006. Importance and intensity of competition along a fertility gradient and across species. Journal of Vegetation Science 17: 455–464.

Goldberg DE. 1994. Influence of competition at the community level: an experimental version of the null models approach. Ecology 75: 1503–1506.

Gómez-Aparicio L, Zamora R, Gómez JM, Hódar JA, Castro J, Baraza E.. 2004. Applying plant facilitation to forest restoration: a meta-analysis of the use of shrubs as nurse plants. Ecological Applications 14:1128–1138.

Gross N, Kunstler G, Liancourt P, De Bello F, Suding KN, Lavorel S.. 2009. Linking individual response to biotic interactions with community structure: a trait-based framework. Functional Ecology 23: 1167–1178.

Gross N, Liancourt P, Choler P, Suding KN, Lavorel S.. 2010. Strain and vegetation effects on local limiting resources explain the outcomes of biotic interactions. Perspectives in Plant Ecology, Evolution and Systematics 12: 9–19.

Gross N, Liancourt P, Butters R, Duncan RP, Hulme PE.. 2015. Functional equivalence, competitive hierarchy and facilitation determine species coexistence in highly invaded grasslands. New Phytologist 206: 175–186. PubMed

Hacker SD, Bertness MD.. 1999. Experimental evidence for factors maintaining plant species diversity in a New England salt marsh. Ecology 80: 2064–2073.

Hacker SD, Gaines SD.. 1997. Some implications of direct positive interactions for community species diversity. Ecology 78: 1990–2003.

Hartmann H. 2009. A summarizing report on the phytosociological and floristical explorations (1976–1997) in Ladakh (India). Switzerlan: Druckerei Landquart VBA.

He L, Cheng L, Hu L, Tang J, Chen X.. 2016. Deviation from niche optima affects the nature of plant–plant interactions along a soil acidity gradient. Biology Letters 12: 20150925. PubMed PMC

He Q, Bertness MD.. 2014. Extreme stresses, niches, and positive species interactions along stress gradients. Ecology 95: 1437–1443. PubMed

He Q, Bertness MD, Altieri AH.. 2013. Global shifts towards positive species interactions with increasing environmental stress. Ecology Letters 16: 695–706. PubMed

Holmgren M, Scheffer M.. 2010. Strong facilitation in mild environments: the stress gradient hypothesis revisited. Journal of Ecology 98: 1269–1275.

Holzner W, Kriechbaum M.. 2000. Pastures in south and central Tibet (China) I. Methods for a rapid assessment of pasture conditions. Die Bodenkultur 51: 247–254.

Hothorn T, Hornik K, van de Wiel MA, Zeileis A.. 2008. Implementing a class of permutation tests: the coin package. Journal of Statistical Software 28: 1–23. PubMed

Huston MA. 1979. A general hypothesis of species diversity. American Naturalist 113: 81–101.

Huston MA. 2014. Disturbance, productivity, and species diversity: empiricism vs. logic in ecological theory. Ecology 95: 2382–2396.

Keddy PA. 2007. Plants and vegetation: origins, processes, consequences. Cambridge: Cambridge University Press.

Keddy PA. 2001. Competition. Dordrecht: Springer Netherlands.

Kikvidze Z, Suzuki M, Brooker R.. 2011. Importance versus intensity of ecological effects: why context matters. Trends in Ecology and Evolution 26: 383–388. PubMed

Kitzberger T, Steinaker DF, Veblen TT.. 2000. Establishment of Austrocedrus chilensis in Patagonian forest-steppe ecotones: facilitation and climatic variability. Ecology 81: 1914–1924.

Körner C. 2003. Limitation and stress – always or never? Journal of Vegetation Science 14: 141–143.

Kumar A, Adhikari BS, Rawat GS.. 2016. Caragana versicolor Benth. (Fabaceae), a keystone species of high conservation concern in the Hindu Kush Himalayan region. Current Science 11: 985–987.

Larcher W. 2012. Bioclimatic temperatures in the high Alps In: Lütz C, ed. Plants in Alpine regions. Wein: Springer, 21–27.

Le Bagousse-Pinguet Y, Liancourt P, Gross N, Straile D.. 2012. Indirect facilitation promotes macrophyte survival and growth in freshwater ecosystems threatened by eutrophication. Journal of Ecology 100: 530–538.

Le Bagousse-Pinguet Y, Forey E, Touzard B, Michalet R.. 2013. Disentangling the effects of water and nutrients for studying the outcome of plant interactions in sand dune ecosystems. Journal of Vegetation Science 24: 375–383.

Le Bagousse-Pinguet Y, Xiao S, Brooker RW, et al.2014a. Facilitation displaces hotspots of diversity and allows communities to persist in heavily stressed and disturbed environments. Journal of Vegetation Science 25: 66–76.

Le Bagousse-Pinguet Y, Maalouf J.-P, Touzard B, Michalet R.. 2014b. Importance, but not intensity of plant interactions relates to species diversity under the interplay of stress and disturbance. Oikos 123: 777–785.

Lessard J-P, Belmaker J, Myers JA, Chase JM, Rahbek C.. 2012. Inferring local ecological processes amid species pool influences. Trends in Ecology and Evolution 27: 600–607. PubMed

Levitt J. 1980. Responses of plants to environmental stresses. New York, Academic Press.

Liancourt P, Callaway RM, Michalet R.. 2005. Stress tolerance and competitive-response ability determine the outcome of biotic interactions. Ecology 86: 1611–1618.

Liancourt P, Sharkhuu A, Ariuntsetseg L, et al.2012a. Temporal and spatial variation in how vegetation alters the soil moisture response to climate manipulation. Plant and Soil 351: 249–261.

Liancourt P, Choler P, Gross N, Thibert-Plante X, Tielbörger K.. 2012b. How facilitation may interfere with ecological speciation. International Journal of Ecology 2012: e725487.

Liancourt P, Spence LA, Song DS, et al.2013. Plant response to climate change varies with topography, interactions with neighbors, and ecotype. Ecology 94:444–453. PubMed

Liancourt P, Boldgiv B, Song DS, et al.2015. Leaf-trait plasticity and species vulnerability to climate change in a Mongolian steppe. Global Change Biology 21: 3489–3498. PubMed

López RP, Squeo FA, Armas C, Kelt DA, Gutiérrez JR.. 2016. Enhanced facilitation at the extreme end of the aridity gradient in the Atacama Desert: a community-level approach. Ecology 97: 1593–1604. PubMed

Maalouf J-P, Bagousse-Pinguet YL, Marchand L, Touzard B, Michalet R.. 2012. The interplay of stress and mowing disturbance for the intensity and importance of plant interactions in dry calcareous grasslands. Annals of Botany 110: 821–828. PubMed PMC

Maestre FT, Cortina J.. 2004. Do positive interactions increase with abiotic stress? A test from a semi-arid steppe. Proceedings of the Royal Society B: Biological Sciences 271(Suppl 5): S331–S333. PubMed PMC

Maestre FT, Callaway RM, Valladares F, Lortie CJ.. 2009. Refining the stress-gradient hypothesis for competition and facilitation in plant communities. Journal of Ecology 97: 199–205.

Malkinson D, Tielbörger K.. 2010. What does the stress-gradient hypothesis predict? Resolving the discrepancies. Oikos 119: 1546–1552.

Michalet R, Pugnaire FI.. 2016. Facilitation in communities: underlying mechanisms, community and ecosystem implications. Functional Ecology 30: 3–9.

Michalet R, Brooker RW, Cavieres LA, et al.2006. Do biotic interactions shape both sides of the humped-back model of species richness in plant communities? Ecology Letters 9: 767–773. PubMed

Michalet R, Xiao S, Touzard B, et al.2011. Phenotypic variation in nurse traits and community feedbacks define an alpine community. Ecology Letters 14: 433–443. PubMed

Michalet R, Le Bagousse-Pinguet Y, Maalouf J-P, Lortie CJ.. 2014a. Two alternatives to the stress-gradient hypothesis at the edge of life: the collapse of facilitation and the switch from facilitation to competition. Journal of Vegetation Science 25: 609–613.

Michalet R, Schöb C, Lortie CJ, Brooker RW, Callaway RM.. 2014b. Partitioning net interactions among plants along altitudinal gradients to study community responses to climate change. Functional Ecology 28: 75–86.

Mishra PK, Anoop A, Schettler G, et al.2015. Reconstructed late Quaternary hydrological changes from Lake Tso Moriri, NW Himalaya. Quaternary International 371: 76–86.

Noumi Z, Chaieb M, Michalet R, Touzard B.. 2015. Limitations to the use of facilitation as a restoration tool in arid grazed savanna: a case study. Applied Vegetation Science 18: 391–401.

Pennings SC, Selig ER, Houser LT, Bertness MD.. 2003. Geographic variation in positive and negative interactions among salt marsh plants. Ecology 84: 1527–1538.

Pugnaire FI, Luque MT.. 2001. Changes in plant interactions along a gradient of environmental stress. Oikos 93: 42–49.

Pugnaire FI, Zhang L, Li R, Luo T.. 2015. No evidence of facilitation collapse in the Tibetan plateau. Journal of Vegetation Science 26: 233–242.

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.

Rohmel J. 1997. The permutation distribution of the Friedman test. Computational Statistics and Data Analysis 26: 83–99.

le Roux PC, McGeoch MA.. 2010. Interaction intensity and importance along two stress gradients: adding shape to the stress-gradient hypothesis. Oecologia 162: 733–745. PubMed

Sammul M, Kull K, Oksanen L, Veromann P.. 2000. Competition intensity and its importance: results of field experiments with Anthoxanthum odoratum. Oecologia 125: 18–25. PubMed

SAS Institute. 2008. JMP version 8.0. Cary, NC: SAS Institute.

Seifan M, Seifan T, Ariza C, Tielbörger K.. 2010. Facilitating an importance index. Journal of Ecology 98: 356–361.

Smit C, Rietkerk M., Wassen M. J.. 2009. Inclusion of biotic stress (consumer pressure) alters predictions from the stress gradient hypothesis. Journal of Ecology 97: 1215–1219.

Soliveres S, Maestre FT.. 2014. Plant–plant interactions, environmental gradients and plant diversity: a global synthesis of community-level studies. Perspectives in Plant Ecology, Evolution and Systematics 16: 154–163 PubMed PMC

Soliveres S, Smit C, Maestre FT.. 2015. Moving forward on facilitation research: response to changing environments and effects on the diversity, functioning and evolution of plant communities. Biological Reviews 90: 297–313. PubMed PMC

Soliveres S, Eldridge DJ, Hemmings F, Maestre FT.. 2012. Nurse plant effects on plant species richness in drylands: the role of grazing, rainfall and species specificity. Perspectives in Plant Ecology, Evolution and Systematics 14: 402–410. PubMed PMC

Sthultz CM, Gehring CA, Whitham TG.. 2007. Shifts from competition to facilitation between a foundation tree and a pioneer shrub across spatial and temporal scales in a semiarid woodland. New Phytologist 173: 135–145. PubMed

Teilbörger K, Kadmon R.. 2000. Temporal environmental variation tips the balance between facilitation and interference in desert plants. Ecology 81: 1544–1553.

Travis JMJ, Brooker RW, Clark EJ, Dytham C.. 2006. The distribution of positive and negative species interactions across environmental gradients on a dual-lattice model. Journal of Theoretical Biology 241: 896–902. PubMed

Tylianakis JM, Didham RK, Bascompte J, Wardle DA.. 2008. Global change and species interactions in terrestrial ecosystems. Ecology Letters 11: 1351–1363. PubMed

Vanselow KA. 2011. The high-mountain pastures of the Eastern Pamirs (Tajikistan): an evaluation of the ecological basis and the pasture potential. PhD thesis, Erlangen-Nurnberg University.

Welden CW, Slauson WL.. 1986. The intensity of competition versus its importance: an overlooked distinction and some implications. Quarterly Review of Biology 61: 23–44. PubMed

Xiao S, Michalet R, Wang G, Chen S-Y.. 2009. The interplay between species’ positive and negative interactions shapes the community biomass–species richness relationship. Oikos 118: 1343–1348.

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