Abstract
Conceptual models of how interactions with native species influence invasions emphasize competition, but recent evidence suggests facilitation can promote invasion in stressful environments. However, how nurse-plants with contrasting growth-forms and distribution interact with invaders remains unexplored, although it could offer insights on nurse/exotic interaction mechanisms. We asked whether shrub and cushion nurses differed in their effects on the exotic Rumex acetosella in sites at four elevations in the high tropical Andes (4100–4400 m), shrubs dominating the lowest sites and cushions the highest sites. During the dry season, we measured soil organic matter (SOM) and water content (SWC) under the shrub Hypericum laricifolium, the cushion Azorella julianii, and adjacent areas outside. We compared Rumex’s performance under each situation, measuring midday leaf temperatures (Tleaf), vapor pressure deficit (VPD), minimum water potentials (Ψmin) and leaf nitrogen (Nleaf) and compared the number, size and proportion of fruiting ramets within sampling rings in each situation. SOM and SWC were higher at all elevations under cushions, then under shrubs and lower outside. Rumex’s density was generally reduced under shrubs but increased on cushions. However, both nurses had positive effects along the gradient on Rumex’s size, reproduction, water balance and Nleaf, shrubs having stronger effects on Tleaf and VPD and cushions on Nleaf. Our results indicate that alternating nurses influenced an invader’s physiological performance to different extents via contrasting effects on shading and soil resources, leading to mixed competitive/facilitative effects of shrubs on the exotic’s demography, while cushions had more consistent facilitative effects across elevations.
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References
Abreu Z, Llambí LD, Sarmiento L (2009) Sensitivity of soil restoration indicators during páramo succession in the high tropical Andes: chronosequence and permanent plot approaches. Restor Ecol 17(5):619–628
Alexander JM, Kueffer C, Daehler CC et al (2011) Assembly of nonnative floras along elevational gradients explained by directional ecological filtering. Proc Natl Acad Sci USA 108:656–661. https://doi.org/10.1073/pnas.1013136108
Alexander JM, Lembrechts JJ, Cavieres LA et al (2016) Plant invasions into mountains and alpine ecosystems: current status and future challenges. Alpine Bot 126:89–103. https://doi.org/10.1007/s00035-016-0172-8
Anderson MJ, Gorley RN, Clarke K (2008) PERMANOVA + for PRIMER: Guide to software and statistical methods. PRIMER-E Ltd., Plymouth
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. https://doi.org/10.1111/j.1654-1103.2011.01333.x
Arévalo JR, Delgado JD, Otto R et al (2005) Distribution of alien vs. native plant species in roadside communities along an altitudinal gradient in Tenerife and Gran Canaria (Canary Islands). Perspect Plant Ecol Evol Syst 7:185–202. https://doi.org/10.1016/j.ppees.2005.09.003
Armas C, Pugnaire FI (2005) Plant interactions govern population dynamics in a semi-arid plant community. J Ecol 93:978–989. https://doi.org/10.1111/j.1365-2745.2005.01033.x
Badano EI, Villarroel E, Bustamante RO et al (2007) Ecosystem engineering facilitates invasions by exotic plants in high-Andean ecosystems. J Ecol 95:682–688. https://doi.org/10.1111/j.1365-2745.2007.01262.x
Bertness MD, Callaway RM (1994) Positive interactions in communities. Trends Ecol Evol 9(5):191–193
Briceño B, Morillo G (2002) Catálogo abreviado de las plantas con flores de los páramos de Venezuela. Parte I. Dicotiledóneas (Magnoliopsida). Acta Bot Venez 25:1–46
Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125. https://doi.org/10.1016/S0169-5347(02)00045-9
Bulleri F, Bruno JF, Benedetti-Cecchi L (2008) Beyond competition: incorporating positive interactions between species to predict ecosystem invasibility. PLoS Biol 6:e162. https://doi.org/10.1371/journal.pbio.0060162
Buytaert W, Vuille M, Dewulf A, Urrutia R, Karmalkar A, Célleri R (2010) Uncertainties in climate change projections and regional downscaling in the tropical Andes: implications for water resources management. Hydrol Earth Syst Sci 14:1247–1258
Cáceres Y, Llambí LD, Rada F (2015) Shrubs as foundation species in a high tropical alpine ecosystem: a multi-scale analysis of plant spatial interactions. Plant Ecol Divers 8:147–161. https://doi.org/10.1080/17550874.2014.960173
Callaway RM, Pugnaire FI (1999) Facilitation in plant communities. In: Pugnaire RM, Valladares FI (eds) Handbook of functional plant ecology. Marcel Dekker, New York, pp 623–648
Carboni M, Guéguen M, Barros C et al (2018) Simulating plant invasion dynamics in mountain ecosystems under global change scenarios. Glob Change Biol 24:e289–e302. https://doi.org/10.1111/gcb.13879
Cavieres LA, Badano EI (2009) Do facilitative interactions increase species richness at the entire community level? J Ecol 97:1181–1191. https://doi.org/10.1111/j.1365-2745.2009.01579.x
Cavieres LA, Quiroz CL, Molina-Montenegro MA et al (2005) Nurse effect of the native cushion plant Azorella monantha on the invasive non-native Taraxacum officinale in the high-Andes of central Chile. Perspect Plant Ecol Evol Syst 7:217–226. https://doi.org/10.1016/j.ppees.2005.09.002
Cavieres LA, Badano EI, Sierra-Almeida A et al (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. https://doi.org/10.1111/j.1469-8137.2005.01573.x
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. https://doi.org/10.1111/j.1365-2435.2007.01338.x
Chen J-G, He X-F, Wang S-W et al (2019) Cushion and shrub ecosystem engineers contribute differently to diversity and functions in alpine ecosystems. J Veg Sci 30:362–374. https://doi.org/10.1111/jvs.12725
Cuesta F, Muriel P, Llambí LD et al (2017) Latitudinal and altitudinal patterns of plant community diversity on mountain summits across the tropical Andes. Ecography 40:1381–1394. https://doi.org/10.1111/ecog.02567
Cuesta F, Tovar C, Llambí LD et al (2019) Thermal niche traits of high alpine plant species and communities across the tropical Andes and their vulnerability to global warming. J Biogeogr 47(2):408–420. https://doi.org/10.1111/jbi.13759
Daehler CC (2005) Upper-montane plant invasions in the Hawaiian Islands: patterns and opportunities. Perspect Plant Ecol Evol Syst 7:203–216. https://doi.org/10.1016/j.ppees.2005.08.002
Ellison AM (2019) Foundation species, non-trophic interactions, and the value of being common. IScience 13:254–268. https://doi.org/10.1016/j.isci.2019.02.020
Escarré J, Houssard C (1989) Variations de populations de Rumex acetosella L. le long d’une succession secondaire: I: allocation de biomasse. Acta Oecol 10:3–19
Gallien L, Mazel F, Lavergne S et al (2015) Contrasting the effects of environment, dispersal and biotic interactions to explain the distribution of invasive plants in alpine communities. Biol Invas 17:1407–1423. https://doi.org/10.1007/s10530-014-0803-1
Giladi I, Segoli M, Ungar ED (2013) Shrubs and herbaceous seed flow in a semi-arid landscape: dual functioning of shrubs as trap and barrier. J Ecol 101:97–106. https://doi.org/10.1111/1365-2745.12019
Greig-Smith P (1983) Quantitative plant ecology, 3rd edn. Blackwell Scientific Publications, Oxford
Holmgren M, Scheffer M, Huston MA (1997) The interplay of facilitation and competition in plant communities. Ecology 78:1966–1975. https://doi.org/10.1890/0012-9658(1997)078%5b1966:TIOFAC%5d2.0.CO;2
Holzapfel C, Tielbörger K, Parag HA et al (2006) Annual plant–shrub interactions along an aridity gradient. Basic Appl Ecol 7:268–279. https://doi.org/10.1016/j.baae.2005.08.003
Hupp N, Llambí LD, Ramírez L, Callaway RM (2017) Alpine cushion plants have species-specific effects on microhabitat and community structure in the tropical Andes. J Veg Sci 28:928–938. https://doi.org/10.1111/jvs.12553
Jaimes V, Sarmiento L (2002) Regeneración de la vegetación de páramo después de un disturbio agrícola en la Cordillera Oriental de Colombia. Ecotropicos 15:61–74
Lambers H, Chapin FS, Pons TL (1998) Plant physiological ecology. Springer, New York
Llambí LD, Fontaine M, Rada F et al (2003) Ecophysiology of dominant plant species during old-field succession in a high tropical Andean ecosystem. Arctic Antarctic Alpine Res 35:447–453. https://doi.org/10.1657/1523-0430(2003)035%5b0447:EODPSD%5d2.0.CO;2
Llambí LD, Hupp N, Saez A, Callaway R (2018) Reciprocal interactions between a facilitator, natives and exotics in tropical alpine plant communities. Perspect Plant Ecol Evol Syst 30:82–88. https://doi.org/10.1016/j.ppees.2017.05.002
Mack RN, Simberloff D, Lonsdale WM et al (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710. https://doi.org/10.1890/1051-0761(2000)010%5b0689:BICEGC%5d2.0.CO;2
Mitchell CE, Agrawal AA, Bever JD et al (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740. https://doi.org/10.1111/j.1461-0248.2006.00908.x
Monasterio M (1980) Las formaciones vegetales de los páramos de Venezuela. In: Monasterio M (ed) Estudios Ecológicos en los Páramos Andinos. Editorial de la Universidad de Los Andes, Mérida, pp 93–158
Mora MA, Llambí LD, Ramírez L (2019) Giant stem rosettes have strong facilitation effects on alpine plant communities in the tropical Andes. Plant Ecol Divers 12(6):593–606. https://doi.org/10.1080/17550874.2018.1507055
Nentwig W (2007) Biological invasions: why it matters. In: Nentwig W (ed) Biological invasions. Springer, Berlin, pp 1–9
Pauchard A, Kueffer C, Dietz H et al (2009) Ain’t no mountain high enough: plant invasions reaching new elevations. Front Ecol Environ 7:479–486. https://doi.org/10.1890/080072
Pauchard A, Milbau A, Albihn A et al (2016) Non-native and native organisms moving into high elevation and high latitude ecosystems in an era of climate change: new challenges for ecology and conservation. Biol Invas 18:345–353. https://doi.org/10.1007/s10530-015-1025-x
Pearcy RW, Ehleringer JR, Money HA, Rundell PW (1989) Plant physiological ecology: field methods and instrumentation. Chapman and Hall, New York, p 457
Pérez FL (1995) Plant-induced spatial patterns of surface soil properties near caulescent Andean rosettes. Geoderma 68:101–121. https://doi.org/10.1016/0016-7061(95)00028-M
Pugnaire FI, Armas C, Valladares F (2004) Soil as a mediator in plant-plant interactions in a semi-arid community. J Veg Sci 15:85–92. https://doi.org/10.1111/j.1654-1103.2004.tb02240.x
Rada F, Azócar A, García-Nuñez C (2019) Plant functional diversity in a tropical Andean páramo. Plant Ecol Divers 12(6):539–554
Ramírez LA, Rada F, Llambí LD (2015) Linking patterns and processes through ecosystem engineering: effects of shrubs on microhabitat and water status of associated plants in the high tropical Andes. Plant Ecol 216:213–225. https://doi.org/10.1007/s11258-014-0429-5
Ramsay P, Oxley E (1997) The growth form composition of plant communities in the Ecuadorian páramos. Plant Ecol 131:173–192
Reich PB, Walters MB, Ellsworth D (1997) From tropics to tundra: global convergence in plant functioning. Proc Nat Acad Sci USA 94:13730–13734
Rodríguez M, Acevedo-Novoa D, Machado D, Ablan M, Dugarte W, Davila F (2019) Ecohydrology of the Venezuelan páramo: water balance of a high Andean watershed. Plant Ecol Divers 12(6):573–591
Salgado-Labouriau ML, Schubert C, Valastro S (1977) Paleoecological analysis of a Late Quaternary terrace from Mucubaji, Venezuelan Andes. J Biogeogr 4:313–325
Sandoya V, Pauchard A, Cavieres L (2017) Natives and non-natives plants show different responses to elevation and disturbance on the tropical high Andes of Ecuador. Ecol Evol 7:7909–7919. https://doi.org/10.1002/ece3.3270
Sarmiento L, Llambi LD, Escalona A, Márquez N (2003) Vegetation patterns, regeneration rates and divergence in an old-field succession of the high tropical Andes. Plant Ecol 166:63–74. https://doi.org/10.1023/A:1023262724696
Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9:912–919. https://doi.org/10.1111/j.1461-0248.2006.00939.x
Simberloff D, Martin J-L, Genovesi P et al (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66. https://doi.org/10.1016/j.tree.2012.07.013
Stohlgren TJ, Jarnevich C, Chong GW, Evangelista PH (2006) Scale and plant invasions: a theory of biotic acceptance. Preslia 78:405–426
Theurillat J-P, Guisan A (2001) Potential impact of climate change on vegetation in the European Alps: a review. Clim Change 50:77–109. https://doi.org/10.1023/A:1010632015572
van Kleunen M, Bossdorf Dawson W (2018) The ecology and evolution of alien plants. Annu Rev Ecol Evol Syst 49:25–47. https://doi.org/10.1146/annurev-ecolsys-110617-062654
Acknowledgements
We thank AQUItaine MOBilité (mobility scholarship from the Ministry of Higher Education and Research, France, 33513) for covering travel expenses for AD and the team at ICAE, Universidad de Los Andes, for support during fieldwork. We also wish to thank the detailed comments and suggestions by three anonymous referees, which greatly improved the manuscript.
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Llambí, L.D., Durbecq, A., Cáceres-Mago, K. et al. Interactions between nurse-plants and an exotic invader along a tropical alpine elevation gradient: growth-form matters. Alp Botany 130, 59–73 (2020). https://doi.org/10.1007/s00035-020-00235-6
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DOI: https://doi.org/10.1007/s00035-020-00235-6