Skip to main content

Advertisement

Log in

Linking patterns and processes through ecosystem engineering: effects of shrubs on microhabitat and water status of associated plants in the high tropical Andes

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

Studies on alpine and semi-arid environments indicate that plants that act as ecosystem engineers improve microhabitat conditions and modify local plant abundance and diversity. However, few studies have linked these patterns with the physiological responses of associated species. We analyze the role of a dominant shrub (Hypericum laricifolium) as an ecosystem engineer in páramo ecosystems at two altitudes (3,715 and 4,300 m) in the Venezuelan Andes. Superficial soil temperatures, soil water content, and organic matter were compared under the crown and outside. We selected the species with positive and negative spatial relations with the shrub and compared their midday leaf water potentials and turgor loss points in individuals growing under shrubs and outside. Results show that H. laricifolium dampened temperature oscillations and increased soil water and organic matter contents, the effect being more pronounced at the drier, lower elevation site. While positively associated forbs showed an improvement in their water status when growing under the crown, the species with the lowest water potentials and higher water-stress tolerance were grasses with a negative spatial relation with the shrub; this was consistent at both elevations. Moreover, the effect of the shrub on the water status and abundance of the exotic herb Rumex acetosella changed from positive in the drier site to negative in the more mesic site. Our results provide mechanistic evidence for interpreting spatial association patterns between nurse plants and other species in the alpine tropics. We propose that stress-resistance strategies (tolerance vs. avoidance) and origin (native vs. exotic) influence interactions with ecosystem engineers.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adler L (2003) Host species affects herbivory, pollination and reproduction in experiments with parasitic Castilleja. Ecology 84:2083–2091

    Article  Google Scholar 

  • Aguiar MR, Sala OE (1994) Competition, facilitation, seed distribution and the origin of patches in a Patagonian steppe. Oikos 70:26–34

    Article  Google Scholar 

  • Alvizu P (2004) Complejidad y respuesta funcional de la vegetación de páramo a lo largo de gradientes altitudinales. Dissertation, Universidad de los Andes

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth

    Google Scholar 

  • Anthelme F, Dangles O (2012) Plant–plant interactions in tropical alpine environments. Perspect Plant Ecol Evol Syst 14(5):363–372

    Article  Google Scholar 

  • Anthelme F, Buendia B, Mazoyer C, Dangles O (2011) Unexpected mechanisms sustain the stress gradient hypothesis in a tropical alpine environment. J Veg Sci 23(1):62–72

    Article  Google Scholar 

  • Armas C, Ordiales R, Pugnaire FI (2004) Measuring plant interactions: a new comparative index. Ecology 85(10):2682–2686

    Article  Google Scholar 

  • Azócar A, Rada F (2006) Ecofisiología de plantas de páramo. LITORAMA, Mérida

    Google Scholar 

  • Badano EI, Cavieres LA (2006) Ecosystem engineering across ecosystems: do engineer species sharing common features have generalized or idiosyncratic effects on species diversity? J Biogeogr 33:304–313

    Article  Google Scholar 

  • 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 115:369–385

    Article  Google Scholar 

  • Badano EI, Villarroel E, Bustamante RO, Marquet PA, Cavieres LA (2007) Ecosystem engineering facilitates invasions by exotic plants in high-Andean ecosystems. J Ecol 95:682–688

    Article  Google Scholar 

  • Bertness MD, Callaway RM (1994) Positive interactions in communities. TREE 9(5):191–193

    CAS  PubMed  Google Scholar 

  • 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). http://www.scielo.org.ve/scielo.php?script=sci_arttext&pid=S0084-59062002000100001&lng=es&nrm=iso

  • Cáceres Y (2011) Relaciones espaciales y mecanismos de interacción entre un arbusto dominante (Hypericum laricifolium Juss) y otras especies de plantas en el páramo Altiandino. Dissertation, Universidad de los Andes

  • Cáceres Y, Llambí LD, Rada F (2014) Shrubs as foundation species in a high tropical mountain ecosystem: a multi-scale analysis of plant spatial interactions. Plant Ecol Divers, pp 1–15

  • Callaway RM (1995) Positive interactions among plants. Bot Rev 61(4):306–349

    Article  Google Scholar 

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

    Google Scholar 

  • Callaway RM, Pugnaire FI (1999) Facilitation in plant communities. In: Pugnaire FI, Valladares F (eds) Handbook of functional plant ecology. Marcel Dekker, pp 623–648

  • Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78(7):1958–1965

    Article  Google Scholar 

  • Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham R, Aschehoug ET, Armas C, Kikodze D, Cook BJ (2002) Positive interactions among alpine plants increase with stress. Nature 417(6891):844–848

    Article  CAS  PubMed  Google Scholar 

  • Cavieres LA, Arroyo MTK, Peñaloza A, Molina-Montenegro MA, Torres C (2002) Nurse effect of Bolax gummifera cushion plants in the alpine vegetation of the Chilean Patagonian Andes. J Veg Sci 13(4):547–554

    Google Scholar 

  • Cavieres LA, Quiroz CL, Molina-Montenegro MA, Muñoz AA, Pauchard A (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(3):217–226

    Article  Google Scholar 

  • 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 Phytol 169(1):59–69

    Article  PubMed  Google Scholar 

  • Cavieres LA, Badano EI, Sierra-Almeida A, Molina-Montenegro MA (2007) Microclimatic modifications of cushion plants and their consequences for seedling survival of native and non-native herbaceous species in the High Andes of Central Chile. Arct Antarct Alp Res 39(2):229–236

    Article  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(1):148–156

    Google Scholar 

  • Ellison AM, Bank MS, Clinton BD et al (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3(9):479–486

    Article  Google Scholar 

  • Estrada C, Monasterio M (1991) Comportamiento reproductivo de una roseta gigante, Espeletia spicata Sch. Bip (Compositae) in the desert paramo. Ecotrópicos 4(1):1–17

    Google Scholar 

  • Fagua JC, Gonzalez VH (2007) Growth rates, reproductive phenology, and pollination ecology of Espeletia grandiflora (Asteraceae), a giant Andean caulescent rosette. Plant Biol 9:127–135

    Article  CAS  PubMed  Google Scholar 

  • Farji-Brener AG, Chinchilla FA, Magrach A, Romero V, Ríos M, Velilla M, Serrano JM, Amador-Vargas S (2009) SHORT COMMUNICATION Slope orientation enhances the nurse effect of a paramo shrub, Hypericum irazuense (Hypericaceae) in Costa Rica. J Trop Ecol 25:331–335

    Article  Google Scholar 

  • Franco-Pizaña JG, Fulbright TE, Gardiner DT, Tipton AR (1996) Shrub emergence and seedling growth in microenvironments created by Prosopis glandulosa. J Veg Sci 7(2):257–264

    Article  Google Scholar 

  • Goldstein G, Meinzer FC, Monasterio M (1985) Physiological and mechanical factors in relation to size-dependent mortality in an Andean giant rosette species. Acta Oecol (Oecol Plant) 6(3):263–275

    Google Scholar 

  • Goldstein G, Meinzer FC, Rada F (1994) Environmental biology of a tropical treeline species, Polylepis sericea. In: Rundel PW, Smith AP, Meinzer FC (eds) Tropical alpine environments: plant form and function. Cambridge University Press, Cambridge

    Google Scholar 

  • Greig-Smith P (1983) Quantitative plant ecology. Blackwells, Oxford

    Google Scholar 

  • 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. Perspect Plant Ecol Evol Syst 12(1):9–19

    Article  Google Scholar 

  • He Q, Bertness MD, Altieri AH (2013) Global shifts towards positive species interactions with increasing environmental stress. Ecol Lett 16(5):695–706

    Article  PubMed  Google Scholar 

  • Holmgren M, Scheffer M, Huston MA (1997) The interplay of facilitation and competition in plant communities. Ecology 78(7):1966–1975

    Article  Google Scholar 

  • Holzapfel C, Mahall BE (1999) Bidirectional facilitation and interference between shrubs and annuals in the Mojave desert. Ecology 80(5):1747–1761

    Article  Google Scholar 

  • Holzapfel C, Tielbörger K, Parag HA, Kigel J, Sternberg M (2006) Annual plant-shrub interactions along an aridity gradient. Basic Appl Ecol 7:268–279

    Article  Google Scholar 

  • Jackson RB, Caldwell MM (1993) Geostatistical patterns of soil heterogeneity around individual perennial plants. J Ecol 81:683–692

    Article  Google Scholar 

  • Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78(7):1946–1957

    Article  Google Scholar 

  • Kelly RH, Burke IC, Lauenroth WK (1996) Soil organic matter and nutrient availability responses to reduced plant inputs in shortgrass steppe. Ecology 77(8):2516–2527

    Article  Google Scholar 

  • Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems; with 47 tables. Springer, Berlin

    Book  Google Scholar 

  • Larcher W (1995) Physiological plant ecology: ecophysiology and stress physiology of functional groups. Springer, Berlin

    Book  Google Scholar 

  • Llambí LD, Fontaine M, Rada F, Saugier B, Sarmiento L (2003) Ecophysiology of dominant plant species during old-field succession in a high tropical Andean ecosystem. Arct Antarct Alp Res 35(4):447–453

    Article  Google Scholar 

  • Maestre FT, Bautista S, Cortina J (2003) Positive, negative, and net effects in grass-shrub interactions in Mediterranean semiarid grasslands. Ecology 84(12):3186–3197

    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 

  • Malagón D (1982) Evolución de los suelos en el páramo andino. CIDIAT, Mérida

    Google Scholar 

  • McIntire EJB, Fajardo A (2014) Facilitation as a ubiquitous driver of biodiversity. New Phytol 201(2):403–416

    Article  Google Scholar 

  • Meinzer FC, Goldstein G, Rada F (1994) Paramo microclimate and leaf thermal balance of Andean giant rosette plants. In: Rundel PW, Smith AP, Meinzer FC (eds) Tropical alpine environments: plant form and function. Cambridge University Press, Cambridge

    Google Scholar 

  • Michalet R (2007) Highlighting the multiple drivers of change in interactions along stress gradients. New Phytol 173(1):3–6

  • Monasterio M (1980a) Los páramos andinos como región natural. Características biogeográficas generales y afinidad con otras regiones andinas. In: Monasterio M (ed) Estudios ecológicos en los páramos andinos. Universidad de Los Andes, Mérida, pp 15–27

    Google Scholar 

  • Monasterio M (1980b) Las formaciones vegetales de los páramos de Venezuela. In: Monasterio M (ed) Estudios ecológicos en los páramos andinos. Universidad de Los Andes, Mérida, pp 93–158

    Google Scholar 

  • Monasterio M, Lamotte M (1989) Les populations d´Espeletia timotensis dans le Páramo Désertico des Andes du Venezuela. Rev Ecol-Terre Vie 44:301–327

    Google Scholar 

  • Pagés JP, Michalet R (2006) Contrasted responses of two understorey species to direct and indirect effects of a canopy gap. Plant Ecol 187(2):179–187

    Article  Google Scholar 

  • Pariente S (2000) Spatial patterns of soil moisture as affected by shrubs, in different climatic conditions. Environ Monit Assess 73(3):237–251

    Article  Google Scholar 

  • Pearcy RW, Ehleringer J, Mooney HA, Rundel PW (1989) Plant physiological ecology: field methods and instrumentation. Chapman and Hall, London

    Book  Google Scholar 

  • Pérez FL (1989) Some effects of giant Andean stem-rosettes on ground microclimate, and their ecological significance. Int J Biometeorol 33:131–135

    Article  Google Scholar 

  • Pérez FL (1992) The influence of organic matter addition by caulescent Andean rosettes on superficial soil properties. Geoderma 54:151–171

    Article  Google Scholar 

  • Pfitsch WA (1988) Microenvironment and the distribution of two species of Draba (Brassicaceae) in a venezuelan paramo. Arct Antarct Alp Res 20(3):333–341

    Article  Google Scholar 

  • Pugnaire FI, Armas C, Valladares F (2004) Soil as a mediator in plant-plant interactions in a semi-arid community. J Veg Sci 15(1):85–92

    Article  Google Scholar 

  • Rada F, García-Nuñez C, Rangel S (2011) Microclimate and regeneration patterns of Polylepis Sericea in a treeline forest of the Venezuelan Andes. Ecotrópicos 24:113–122

    Google Scholar 

  • Ramírez L (2013) Interacciones entre un arbusto dominante (Hypericum laricifolium. juss) y otras especies de plantas en el páramo andino y altiandino. Dissertation, Universidad de los Andes

  • Sarmiento G (1986) Ecologically crucial features of climate in high tropical mountains. In: Vuilleumier F, Monasterio M (eds) High Altitude Tropical Biogeography. Oxford University Press, Oxford, pp 11–45

    Google Scholar 

  • Sarmiento L (2006) Grazing impact on vegetation structure and plant species richness in an old-field succession of the Venezuelan Páramos. In: Spehn E. M, Liberman M, Körner C (eds) Land use change and mountain biodiversity, Taylor and Francis, Basel (Switzerland) and La Paz (Bolivia), pp 119–136

  • Sarmiento L, Llambí LD, Escalona A, Marquez N (2003) Vegetation patterns, regeneration rates and divergence in an old-field succession of the high tropical Andes. Plant Ecol 166:63–74

    Article  Google Scholar 

  • Schlesinger WH, Raikes JA, Hartley AE, Cross AF (1996) On the spatial pattern of soil nutrients in desert ecosystems. Ecology 77(2):364–374

    Article  Google Scholar 

  • Schöb C, Butterfield BJ, Pugnaires FI (2012) Foundation species influence trait-based community assembly. New Phytol 196(3):824–834

    Article  PubMed  Google Scholar 

  • Schöb C, Prieto I, Armas C, Pugnaire FI (2014) Consequences of facilitation: one plant’s benefit is another plant’s cost. Funct Ecol 8(2):500–508

    Article  Google Scholar 

  • Sklenář P (2009) Presence of cushion plants increases community diversity in the high equatorial Andes. Flora 204(4):270–277

    Article  Google Scholar 

  • Smith A (1981) Growth and population dynamics of Espeletia (Compositae) in the Venezuelan Andes, vol 48. Smithsonian Institution Press, Washington

  • Valiente-Banuet A, Bolongaro-Crevenna A, Briones O, Ezcurra E, Rosas M, Nuñez H, Barnard G, Vazquez E (1991) Spatial relationships between cacti and nurse shrubs in a semi-arid environment in central Mexico. J Veg Sci 2:15–20

    Article  Google Scholar 

  • Vila M, Weiner J (2004) Are invasive plant species better competitors than native plant species?–evidence from pair-wise experiments. Oikos 105(2):229–238

    Article  Google Scholar 

Download references

Acknowledgments

We wish to thank C. García, T. Schwarzkopf, M. Fariñas and two anonymous referees for their insightful comments and suggestions and the technical staff at ICAE for their help during field and laboratory work (N. Marquez, W. Dugarte, Z. Méndez). This work was financed by the CDCHTA at Universidad de Los Andes (project E-1769-12-01-EM).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lirey A. Ramírez.

Additional information

Communicated by C. Holzapfel.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ramírez, L.A., Rada, F. & Llambí, L.D. 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 (2015). https://doi.org/10.1007/s11258-014-0429-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-014-0429-5

Keywords

Navigation