Skip to main content

Advertisement

SpringerLink
Log in

Shrub facilitation is an important driver of alpine plant community diversity and functional composition

  • Original Paper
  • Published:
Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

Facilitation often occurs in environments where extreme climatic factors favour positive rather than negative species interactions. This includes larger ‘nurse’ cushion plants in some alpine environments that shelter other species from abiotic filters such as abrasive winds and low temperatures. This type of facilitation can contribute to higher alpha (within habitat), beta (between habitats) and gamma diversity (across the community), by facilitating species with less stress tolerant but more competitive functional traits otherwise excluded from these communities. We assess whether shrubs play a similar role in facilitation, using the dominant prostrate shrub Epacris gunnii in a high conservation value plant community along the highest ridgeline in the Australian Alps. Differences in alpha and beta diversity, species and functional composition were compared in and out of shrubs using point sampling and quadrats. Shrub habitat enhanced alpha (species richness per plot) and beta diversity resulting in greater gamma diversity for the community as a whole, with twice as many species associated with the shrub than open quadrats. There were also differences in functional composition with vegetation in shrub quadrats being taller with larger leaves. It seems that E. gunnii creates micro-refugia that assist in the range expansion of more productive but less stress-tolerant species, including some endemics, in the community. Alpine shrubs can therefore occupy a similar facilitative role to that of cushion plants in alpine plant communities and therefore may also be important drivers of diversity and functional composition.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aguiar M, Soriana A, Sala A (1992) Competition and facilitation in the recruitment of seedlings in Patagonian steppe. Funct Ecol 6:66–70

    Article  Google Scholar 

  • Akhalkatsi M, Abdaladze O, Nakhutsrishvili G, Smith WK (2006) Facilitation of seedling microsites by Rhododendron caucasicum extends the Betula litwinowii alpine treeline, Caucasus Mountains, Republic of Georgia. Arct Antarct Alp Res 38:481–488

    Article  Google Scholar 

  • Araya YN, Silvertown J, Gowing DJ, McConway GJ, Linder HP, Midgley G (2011) A fundamental, eco-hydrological basis for niche segregation in plant communities. New Phytol 189:253–258

    Article  PubMed  Google Scholar 

  • Aubert S, Boucher F, Lavergne S, Renaud J, Choler P (2014) 1914–2014: a revised worldwide catalogue of cushion plants 100 years after Hauri and Schröter. Alp Bot 124:59–70

    Article  Google Scholar 

  • Badano EI, Cavieres LA, Molina-Montenegro MA, Quiroz CL (2005) Slope aspect influences plant association patterns in the Mediterranean matorral of central Chile. J Arid Environ 62:93–108

    Article  Google Scholar 

  • Ballantyne M, Pickering CM, Wright GT, McDougall KL (2014) Sustained impacts of a hiking trail on changing Windswept Feldmark vegetation in the Australian Alps. Aust J Bot 62:263–275

    Google Scholar 

  • Barrow MD (1968) Cyclical changes in an Australian Feldmark community. J Ecol 56:89–96

    Article  Google Scholar 

  • Bernhardt-Römermann M, Gray A, Vanbergen AJ, Bergés L, Bohner A, Brooker RW, De Bruyn L, De Cinti B, Dirnböck T, Grandin U, Hester AJ, Kanka R, Klotz S, Loucougaray G, Lundin L, Matteucci G, Mészáros I, Oláh V, Preda E, Prévosto B, Pykälä J, Schmidt W, Taylor ME, Vadineanu A, Waldmann T, Stadler J (2011) Functional traits and local environment predict vegetation responses to disturbance: a pan-European multi-site experiment. J Ecol 99:777–787

    Article  Google Scholar 

  • Bertness MD, Shumway SW (1993) Competition and facilitation in marsh plants. Am Nat 142:718–724

    Article  CAS  PubMed  Google Scholar 

  • Brittingham S, Walker LR (2000) Facilitation of Yucca brevifolia recruitment by Mojave Desert shrubs. West N Am Nat 60:374–383

    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 F, 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 

  • Butterfield BJ, Briggs JM (2011) Regeneration niche differentiates functional strategies of desert woody plant species. Oecologia 165:477–487

    Article  PubMed Central  PubMed  Google Scholar 

  • Butterfield BJ, Cavieres LA, Callaway RM, Cook BJ, Kikvidze Z, Lortie CJ, Michalet R, Pugnaire FI, Schöb C, Xiao S, Zaitchek B, Anthelme F, Gavilán R, Kanka R, Maalouf JP, Noroozi J, Parajuli R, Phoenix GK, Reid A, Ridenour W, Rixen C, Wipf S, Zhao L, Brooker RW (2013) Alpine cushion plants inhibit the loss of phylogenetic diversity in severe environments. Ecol Lett 16:478–486

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Callaway RM (1998) Competition and facilitation on elevation gradients in subalpine forests of the northern Rocky Mountains, USA. Oikos 82:561–573

    Article  Google Scholar 

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

    Google Scholar 

  • Callaway RM, Pugnaire FI (2007) Facilitation in plant communities. In: Pugnaire F, Valladares F (eds) Functional plant ecology, 2nd edn. CRC Press, Boca Raton, pp 435–456

    Google Scholar 

  • Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–1965

    Article  Google Scholar 

  • Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire 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  CAS  PubMed  Google Scholar 

  • Carlsson BA, Callaghan TV (1991) Positive plant interactions in tundra vegetation and the importance of shelter. J Ecol 79:973–983

    Article  Google Scholar 

  • Catorci A, Cesaretti S, Velasquez JL, Zeballos H (2011) Plant-plant spatial interactions in the dry Puna (southern Peruvian Andes). Alp Bot 121:113–121

    Article  Google Scholar 

  • Cavieres L, Arroyo MTK, Peñaloza A, Molina-Montenegro M, Torres C (2002) Nurse effect of Bolax gummifera 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 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 Phytol 169:59–69

    Article  PubMed  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 

  • Cavieres LA, Brooker RW, Butterfield BJ, Cook BJ, Kikvidze Z, Lortie CJ, Michalet R, Pugnaire FI, Schöb C, Xiao S, Anthelme F, Björk RG, Dickinson KJM, Cranston BH, Gavilán R, Gutiérrez-Girón A, Kanka R, Maalouf JP, Mark AF, Noroozi J, Parajuli R, Phoenix GK, Reid AM, Ridenour WM, Rixen C, Wipf S, Zhao L, Escudero A, Zaitchik BF, Lingua E, Aschehoug ET, Callaway RM (2014) Facilitative plant interactions and climate simultaneously drive alpine plant diversity. Ecol Lett 17:193–202

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of change in community structure. Aust Ecol 18:117–143

    Article  Google Scholar 

  • Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380

    Article  Google Scholar 

  • Cornwell WK, Ackerly DD (2009) Community assembly and shifts in the distribution of functional trait values across an environmental gradient in coastal California. Ecol Monogr 79:109–126

    Article  Google Scholar 

  • Costin A, Gray M, Totterdell C, Wimbush D (2000) Kosciuszko alpine flora, 2nd edn. CSIRO Publishing, Canberra

    Google Scholar 

  • Cranston BH, Hermanutz L (2013) Seed-seedling conflict in conifers as a result of plant-plant interactions at the forest-tundra ecotone. Plant Ecol Divers 6:319–327

    Article  Google Scholar 

  • Davis CJ (2013) Towards the development of long-term winter records for the Snowy Mountains. Aust Meteorol Oceanogr J 63:303–313

    Google Scholar 

  • De Bello F, Lavorel S, Díaz S, Harrington R, Corenlissen JHC, Bardgett RD, Berg MP, Cipriotti P, Feld CK, Hering D, Da Silva PM, Potts SG, Sandin L, Sousa JP, Storkey J, Wardle DA, Harrison PA (2010) Towards an assessment of multiple ecosystem processes and services via functional traits. Biodivers Conserv 19:2873–2893

    Article  Google Scholar 

  • Díaz S, Cabido M (2001) Vive la difference: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655

    Article  Google Scholar 

  • Dormann CF, Brooker RW (2002) Facilitation and competition in the high Arctic: the importance of the experimental approach. Acta Oecol 23:297–301

    Article  Google Scholar 

  • 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. Ecol Appl 14:1128–1138

    Article  Google Scholar 

  • Green K, Pickering CM (2009) The decline of snowpatches in the Snowy Mountains of Australia: importance of climate warming, variable snow, and wind. Arct Antarct Alp Res 41:212–218

    Article  Google Scholar 

  • Grime JP (1977) Evidence for existence of 3 primary strategies in plant and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194

    Article  Google Scholar 

  • Grime JP (1998) Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J Ecol 86:902–910

    Article  Google Scholar 

  • Gross K (2008) Positive interactions among competitors can produce species-rich communities. Ecol Lett 11:929–936

    Article  PubMed  Google Scholar 

  • Hill W, Pickering CM (2009) Differences in resistance of three sub-tropical vegetation types to experimental trampling. J Env Manag 90:1305–1312

    Article  Google Scholar 

  • Holmgren M, Scheffer M, Huston MA (1997) The interplay of facilitation and competition in plant communities. Ecology 78:1966–1975

    Article  Google Scholar 

  • Keppel G, Van Niel KP, Wardell-Johnson GW, Yates CJ, Byrne M, Mucina L, Schut AGT, Hopper SD, Franklin SE (2012) Refugia: identifying and understanding safe havens for biodiversity under climate change. Glob Ecol Biogeogr 21:393–404

    Article  Google Scholar 

  • Kikvidze Z, Nakhutsrishvili G (1998) Facilitation in subnival vegetation patches. J Veg Sci 9:261–264

    Article  Google Scholar 

  • Kleyer M, Bekker RM, Knevel IC, Bakker JP, Thompson K, Sonnenschein M, Poschlod P, Van Groenendael JM, Klimes L, Klimesová J, Klotz S, Rusch GM, Hermy M, Adriaens D, Boedeltje G, Bossuyt B, Dannemann A, Endels P, Götzenberger L, Hodgson JG, Jackel AK, Kühn I, Kunzmann D, Ozinga WA, Römermann C, Stadler M, Schlegelmilch J, Steendam HJ, Tackenberg O, Wilmann B, Cornelissen JHC, Eriksson O, Garnier E, Peco B (2008) The LEDA Traitbase: a database of life-history traits of northwest European flora. J Ecol 96:1266–1274

    Article  Google Scholar 

  • Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems, 2nd edn. Springer, Berlin

    Book  Google Scholar 

  • Körner K, Allison A, Hilscher H (1983) Altitudinal variation of leaf diffusive conductance and leaf anatomy in heliophytes of montane New Guinea and their interrelation with microclimate. Flora 174:91–135

    Google Scholar 

  • Krebs CJ (1994) Ecology: the experimental analysis of distribution and abundance, 4th edn. Harper Collins College Publishing, New York

    Google Scholar 

  • Lepš J, De Bello F, Lavorel S, Berman S (2006) Quantifying and interpreting functional diversity of natural communities: practical considerations matter. Preslia 78:481–501

    Google Scholar 

  • Lin Y, Berger U, Grimm V, Ji QR (2012) Differences between symmetric and asymmetric facilitation matter: exploring the interplay between modes of positive and negative plant interactions. J Ecol 100:1482–1491

    Article  Google Scholar 

  • Lopez RP, Valdivia S (2007) The importance of shrub cover for four cactus species differing in growth form in an Andean semi-desert. J Veg Sci 18:263–270

    Article  Google Scholar 

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

    Article  Google Scholar 

  • McDougall KL, Walsh NG (2007) Treeless vegetation of the Australian Alps. Cunninghamia 10:1–57

    Google Scholar 

  • McDougall KL, Wright GT (2004) The impact of trampling on feldmark vegetation in Kosciuszko National Park, New South Wales. Aust J Bot 52:315–320

    Article  Google Scholar 

  • McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185

    Article  PubMed  Google Scholar 

  • McIntire EJB, Fajardo A (2011) Facilitation within species: a possible origin of group-selected superorganisms. Am Nat 178:88–97

    Article  PubMed  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 

  • Nobel P (1988) Principles underlying the prediction of temperature in plants, with special reference to desert succulents. In: Long SF, Woodward FI (eds) Plants and temperature. Cambridge University Press, Cambridge, pp 1–23

    Google Scholar 

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

    Article  Google Scholar 

  • Olofsson J (2004) Positive and negative plant-plant interactions in two contrasting arctic-alpine plant communities. Arct Antarct Alp Res 36:464–467

    Article  Google Scholar 

  • Pickering CM, Hill W (2007) Impacts of recreation and tourism on plant biodiversity and vegetation in protected areas in Australia. J Env Manag 85:791–800

    Article  Google Scholar 

  • Pickering CM, Venn SE (2013) Increasing the resilience of the Australian flora to climate change and associated threats: a plant functional traits approach. National Climate Change Adaptation Research, Gold Coast

    Google Scholar 

  • Pickering CM, Green K, Barros A, Venn SA (2014) A resurvey of late-lying snowpatches reveals changes in both species and functional composition across snowmelt zones. Alp Bot 124:93–103

    Article  Google Scholar 

  • Pyšek P, Liška J (1991) Colonisation of Sibbaldia tetrandra cushions on alpine scree in the Pamiro-Alai Mountains, Central Asia. Arct Antarct Alp Res 23:263–272

    Article  Google Scholar 

  • Raffaele E, Veblen TT (1998) Facilitation by nurse shrubs of resprouting behaviour in a post-fire shrubland in northern Patagonia, Argentina. J Veg Sci 9:693–698

    Article  Google Scholar 

  • Raunkiær C (1934) The life forms of plants and statistical plant geography; being the collected papers of C. Raunkiær. Clarenden Press, Oxford

    Google Scholar 

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

    Article  Google Scholar 

  • Schöb C, Butterfield BJ, Pugnaire FI (2012) Foundation species influence trait-based community assembly. New Phytol 196:824–834

    Article  PubMed  Google Scholar 

  • Schöb C, Armas C, Guler M, Prieto I, Pugnaire FI (2013) Variability in functional traits mediates plant interactions along stress gradients. J Ecol 101:753–762

    Article  Google Scholar 

  • Silvertown J, Wilson JB (1994) Community structure in a desert perennial community. Ecology 72:409–417

    Article  Google Scholar 

  • Smit C, den Ouden J, Díaz M (2009) Facilitation of Quercus ilex recruitment by shrubs in Mediterranean open woodlands. J Veg Sci 19:193–200

    Article  Google Scholar 

  • Specht RL, Moll EJ (1983) Mediterranean-type heathlands and sclerophyllous scrublands of the world: an overview. Ecol Stud 43:41–65

    Article  CAS  Google Scholar 

  • Stachowicz JJ (2001) Mutualism, facilitation and the structure of ecological communities. Bioscience 51:235–246

    Article  Google Scholar 

  • Tewksbury JJ, Lloyd JD (2001) Positive interactions under nurse-plants: spatial scale, stress gradients and benefactor size. Oecologia 127:425–434

    Article  Google Scholar 

  • Valiente-Banuet A, Fernando V, Zavala-Hurtado JA (1991) Interaction between the cactus Neobuxbaumia tetetzo and the nurse shrub Mimosa luisana. J Veg Sci 2:11–14

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Venn SE, Pickering C, Green K (2014) Spatial and temporal functional changes in alpine summit vegetation are driven by increases in shrubs and graminoids. AoB PLANTS. doi:10.1093/aobpla/plu008:1-15

    PubMed Central  PubMed  Google Scholar 

  • Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Annu Rev Ecol Syst 33:125–159

    Article  Google Scholar 

  • Whittaker RH (1972) Evolution and measurement of species diversity. Taxon 21:213–251

    Article  Google Scholar 

  • Williams RJ, Wahren CH, Tolsma AD, Sanecki GM, Papst WA, Myers BA, McDougall KL, Heinze DA, Green K (2008) Large fires in Australian alpine landscapes: their part in the historical fire regime and their impacts on alpine biodiversity. Int J Wildland Fire 17:793–808

    Article  Google Scholar 

  • Worboys GL (2003) A brief report on the 2003 Australian Alps bushfires. Mt Res Dev 23:294–295

    Article  Google Scholar 

Download references

Acknowledgments

We thank the New South Wales Office of Environment and Heritage for granting access to the study site and Griffith University for funding this research. We also thank Dr. Clare Morrison and Dr. Susanna Venn for their comments on drafts of this manuscript.

Author information

Authors and Affiliations

  1. Griffith School of Environment, Environmental Futures Research Institute, Griffith University, Parklands Drive, Southport, Gold Coast, QLD, 4222, Australia

    Mark Ballantyne & Catherine Marina Pickering

Authors
  1. Mark Ballantyne
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Catherine Marina Pickering
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark Ballantyne.

Additional information

Communicated by Danna J. Leaman.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10531_2015_910_MOESM1_ESM.pdf

Supplementary material 1 (PDF 305 kb). Supplementary Material 1: Differences in the raw average trait values per species for all species found in and outside of Epacris gunnii canopies in Windswept Feldmark. Growth forms according to Costin et al. (2000), species names according to PlantNET (http://plantnet.rbgsyd.nsw.gov.au/floraonline.htm), family names according to Angiosperm Phylogeny Group III System and life form according to the Raunkiær system (1934) taken from Barrow (1968). Abbreviations for Growth Form (GF): H herb, C cushion, S shrub, G graminoid, L lichen, M moss, CM clubmoss. Species marked with * were only found in the survey of overall composition and not in the quadrat survey and hence were not used in analyses of functional composition. Carex cephalotes, Hypogymnia lugubris, Polytrichum juniperum and Lycopodium fastigiatum excluded from analyses due to rarity, or non-vascular. Supplementary Material 2: Differences in the frequency (number of quadrats) and average cover (%) for all species in and outside of Epacris gunnii canopies in Windswept Feldmark. Growth forms according to Costin et al. 2000, species names according to PlantNET (http://plantnet.rbgsyd.nsw.gov.au/floraonline.htm), family names according to APG III System and life form according to Raunkiær system (1934) taken from Barrow (1968). Abbreviations for growth form (GF): H herb, C cushion, S shrub, G graminoid, L lichen, M moss, CM clubmoss. Species marked with * were only found in the survey of overall composition and not in the quadrat survey

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ballantyne, M., Pickering, C.M. Shrub facilitation is an important driver of alpine plant community diversity and functional composition. Biodivers Conserv 24, 1859–1875 (2015). https://doi.org/10.1007/s10531-015-0910-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-015-0910-z

Keywords

Search

Navigation