Functional traits of nurse plants impact recruitment based on life form of beneficiary plants

Sandra M. Gelviz-Gelvez1,2, Felipe Barragán3, Oswaldo Téllez-Valdés1, Horacio Paz, Ricardo Álvarez4
1Laboratorio de Recursos Naturales, UBIPRO, Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México, Tlalnepantla, Estado de México, Mexico
2Instituto de Investigación de Zonas Desérticas, Universidad Autónoma de San Luis Potosí, San Luis Potosí, Mexico
3CONAHCYT-IPICYT División de Ciencias Ambientales, San Luis Potosí, Mexico
4CONAHCYT-Laboratorio Regional para el Estudio y Conservación del Germoplasma, Centro de Investigación Científica de Yucatán A.C, Mérida, Mexico

Tóm tắt

Arid and semi-arid ecosystems are widely distributed around the world, covering about 60% of the earth’s land area. This type of ecosystem has low resilience and high fragmentation caused by human activities related to land use changes to agricultural uses. It has been seen that one of the mechanisms that can help recover the structure and functioning of this type of ecosystem is facilitative interaction. It has been documented that in these environments, the greatest recruitment and establishment of seedlings occur under the cover of a nurse plant. This has led us to investigate whether the life forms of the benefited plants have any relationship with this type of interaction, since the presence and distribution of beneficiaries of particular life forms may result from the evolution of the facilitating interaction. In total, we registered 16 nurse species in the sampling sites, and underneath the canopies of these species, we recorded approximately 250 individuals benefiting from these plants. The majority (51%) were succulent plants, followed by shrubs comprising 27.5%. The functional attributes of the nurse plants that were most strongly associated with the succulent life form were height (H) and canopy density (CD) (Axis 1 of the PCA), as well as leaf area (LA) and specific leaf area (SLA) (Axis 2). These relationships may be due to the fact that succulents seek out nurse plants that have ample canopy cover for the best protection. These findings may help in the selection of effective nurse species for restoring functional diversity in degraded drylands.

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Aiba SI, Kohyama T (1997) Crown architecture and life-history traits of 14 tree species in a warm-temperate rain forest: significance of spatial heterogeneity. J Ecol 85:611–624. https://doi.org/10.2307/2960532 Álvarez-Espino RX (2008) Efecto de la fragmentación sobre el nodricismo en las terrazas aluviales de Zapotitlán de las Salinas, Puebla. Master’s thesis. Universidad Nacional Autónoma de México Archer S (1989) Have southern Texas savannas been converted to woodlands in recent history? Am Nat 134:545–561 Belsky AJ, Canham CD (1994) Forest gaps and isolated forest trees. Bioscience 44:77–84. https://doi.org/10.2307/1312205 Belsky AJ, Amundson RG, Duxbury JM, Riha SJ, Ali AR, Mwonga SM (1989) The effects of trees on their physical, chemical and biological environments in a semi-arid savanna in Kenya. J Appl Eco 26:1005–1024 Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193 Brooker RW, Maestre FT, Callaway RM, Lortie CL, Cavieres LA, Kunstler G et al (2008) Facilitation in plant communities: the past, the present, and the future. J Ecol 96:18–34. https://doi.org/10.1111/j.1365-2745.2007.01295.x Bush J, Van Auken O (1987) Light requirements for growth of Prosopis glandulosa seedlings. Southw Naturalist 32:469–473 Butterfield BJ, Callaway RM (2013) A functional comparative approach to facilitation and its context dependence. Funct Ecol 27:907–917 Butterfield BJ, Betancourt JL, Turner RM, Briggs JM (2010) Facilitation drives 65 years of vegetation change in the Sonoran Desert. Ecology 91:1132–1139 Callaway RM (1992) Effect of shrubs on recruitment of Quercus douglasii and Quercus lobata in California. Ecology 73:2118–2128 Callaway RM (1995) Positive interactions among plants. Bot Rev 61:306–349 Castro J, Zamora R, Hódar JA, Gómez JM (2002) Use of shrubs as nurse plants: a new technique for reforestation in Mediterranean mountains. Restor Ecol 10:297–305 Chave J (2006) Medición de densidad de madera en árboles tropicales manual de campo. France: Sixth Framework Programme Pan-Amazonia7 Cody ML (1991) Niche theory and plant growth form. Vegetation 97:39–55 Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aus J Bot 51:335–380 Crutsinger GM, Strauss SY, Rudgers JA (2010) Genetic variation within a dominant shrub species determines plant species colonization in a coastal dune ecosystem. Ecology 91:1237–1243 Day TA, Wright RG (1989) Positive plant spatial association with Eriogonum ovalifolium in primary succession on cinder cones: seed-trapping nurse plants. Vegetation 80:37–45 Dıiaz S, Cabido M (2001) Vive la différence: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655 Drezner TD (2007) An analysis of winter temperature and dew point under the canopy of a common Sonoran Desert nurse and the implications for positive plant interactions. J Arid Environ 69:554–568. https://doi.org/10.1016/j.jaridenv.2006.11.003 Estrella B, Diego F (2010) Determinación y caracterización de tipos funcionales de plantas (TFPs) en bosques secundarios dentro de un gradiente altitudinal y su relación con variables bioclimáticas. Master’s thesis, CATIE, Turialba (Costa Rica) Flores J, Jurado E (2003) Are nurse-protégé interactions more common among plants from arid environments? J Veg Sci 14:911–916 Flores-Martinez A, Ezcurra E, Sanchez-Colon S (1994) Effect of Neobuxbaumia tetetzo on growth and fecundity of its nurse plant Mimosa luisana. J Ecol 82:325–330 Franco AC, Nobel PS (1988) Interactions between seedlings of agave deserti and the nurse plant Hilaria rigida. Ecology 69:1731–1740 Funk JL, Cleland EE, Suding KN, Zavaleta ES (2008) Restoration through reassembly: plant traits and invasion resistance. Trends Ecol Evol 23:695–703. https://doi.org/10.1016/j.tree.2008.07.013 García E (2006) Efecto de la estructura de la copa en la partición de lluvia de tres especies arbustivas en clima semiárido. Dissertation, University of Almería. Garnier E, Shipley B, Roumet C, Laurent G (2001) A standardized protocol for the determination of specific leaf area and leaf dry matter content. Funct Ecol 15:688–695 Godínez-Álvarez H, Ríos-Casanova L, Pérez F (2005) Characteristics of seedling establishment of Stenocereus stellatus (Cactaceae) in the Tehuacán Valley. Mexico Southw Naturalist 50:375–407 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 Gómez-Aparicio L, Gómez JM, Zamora R, Boettinger JL (2005) Canopy vs. soil effects of shrubs facilitating tree seedlings in Mediterranean montane ecosystems. J Veg Sci 16:191–198 Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA (2001) Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126:457–461 Hunt MA, Murray KE, Battaglia M, Mathers NJ (2007) Determination of specific leaf area of some commercially useful sub-tropical hardwood species. Austral for 70:158–166 Kitajima K (1996) Ecophysiology of tropical tree seedlings. In: Mulkey SS, Chazdon RL, Smith AP (eds) Tropical forest plant ecophysiology. Chapman and Hall, New York, pp 559–597 Larrea AD (2007) Síndrome nodriza y ecología de la regeneración de cactus columnares en un enclave semiárido andino. Dissertation, Universidad de Los Andes Lohbeck M, Lebrija-Trejos E, Martínez-Ramos M, Meave J, Poorter L, Bongers F (2015) Functional trait strategies of trees in dry and wet tropical forests are similar but differ in their consequences for succession. PLoS ONE 10(4):e0123741. https://doi.org/10.1371/journal.pone.0123741 López RP, Valdivia S, Sanjinés N, De la Quintana D (2007) The role of nurse plants in the establishment of shrub seedlings in the semi-arid subtropical Andes. Oecologia 152:779–790 López-Ramiro P, Valdivia S, Sanjinés N, De la Quintana D (2007) The role of nurse plants in the establishment of shrub seedlings in the semi-arid subtropical Andes. Oecologia 152:779–790 Maestre FT, Cortina J (2005) Remnant shrubs in Mediterranean semi-arid steppes: effects of shrub size, abiotic factors and species identity on understory richness and occurrence. Acta Oecol 27:161–169 Mandujano M, Montaña C, Eguiarte LE (1996) Reproductive ecology and inbreeding depression in Opuntia rastrera (Cactaceae) in the Chihuahuan Desert: why are sexually derived recruitments so rare? Am J Bot 83:63–70 Meinzer FC (2003) Functional convergence in plant responses to the environment. Oecologia 134:1–11 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. Ecol Lett 14:433–443 Miguel-Talonia C, Téllez-Valdés O, Murguía-Romero M (2014) Las cactáceas del Valle de Tehuacán-Cuicatlán, México: estimación de la calidad del muestreo. Rev Mex Biodivers 85:436–444 Montiel S, Montaña C (2000) Vertebrate frugivory and seed dispersal of a Chihuahuan Desert cactus. Plant Ecol 146:221–229 Montiel S, Montaña C (2003) Seed bank dynamics of the desert cactus Opuntia rastrera in two habitats from the Chihuahuan Desert. Plant Ecol 166:241–248 Moro MJ, Pugnaire FI, Haase P, Puigdefábregas J (1997) Effect of the canopy of Retama sphaerocarpa on its understory in a semiarid environment. Funct Ecol 11:425–431 Nobel PS (1980) Morphology, nurse plants, and minimum apical temperatures for young Carnegiea gigantea. Bot Gaz 141:188–191 Ordoñez JC, Van Bodegom PM, Witte JPM, Wright IJ, Reich PB, Aerts R (2009) A global study of relationships between leaf traits, climate and soil measures of nutrient fertility. Glob Ecol Biogeogr 18:137–149 Padien DJ, Lajtha K (1992) Plant spatial pattern and nutrient distribution in pinyon-juniper woodlands along an elevational gradient in northern New Mexico. Int J Plant Sci 153:425–433 Padilla FM, Pugnaire FI (2006) The role of nurse plants in the restoration of degraded environments. Front Ecol Environ 4:196–202 Parker V, Muller CH (1982) Vegetational and environmental changes beneath isolated live oak trees (Quercus agrifolia) in a California annual grassland. Am Midl Nat 107:69–81 Poorter L, Bongers F (2006) Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87:1733–1743 Poorter L, McDonald I, Alarcón A, Fichtler E, Licona JC, Peña-Claros M, Sterck F, Villegas Z, Sass-Klaassen U (2010) The importance of wood traits and hydraulic conductance for the performance and life history strategies of 42 rainforest tree species. New Phytol 185:481–492 R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna Rowe N, Speck T (2005) Plant growth forms: an ecological and evolutionary perspective. New Phytol 166:61–72 Rozendaal DMA, Hurtado VH, Poorter L (2006) Plasticity in leaf traits of 38 tropical tree species in response to light; relationships with light demand and adult stature. Funct Ecol 20:207–216 Schlesinger WH, Raies JA, Hartley AE, Cross AF (1996) On the spatial pattern of soil nutrients in desert ecosystems. Ecology 77:364–374 Schöb C, Butterfield BJ, Pugnaire FI (2012) Foundation species influence trait-based community assembly. New Phytol 196:824–834 Scholes RJ, Archer SR (1997) Tree-grass interactions in savannas. Ann Rev Ecol Syst 28:517–544 Suzán-Azpiri H, Sosa VJ (2006) Comparative performance of the giant cardon (Pachycereus pringlei) seedlings under two leguminous nurse plant species. J Arid Environ 65:351–362 Swenson NG, Enquist BJ (2008) The relationship between stem and branch wood specific gravity and the ability of each measure to predict leaf area. Am J Bot 95:516–519 Téllez-Valdés O, Dávila P (2011) Informe final del Proyecto HK040 Evaluación de conservación de especies de Cactaceae en la Reserva de la Biosfera Tehuacán-Cuicatlán Tewksbury JJ, Lloyd JD (2001) Positive interactions under nurse-plants: spatial scale, stress gradients and benefactor size. Oecologia 127:425–434 Tielbörger K, Kadmon R (2000) Temporal environmental variation tips the balance between facilitation and interference in desert plants. Ecology 81:1544–1553 Valiente-Banuet A, Ezcurra E (1991) Shade as a cause of the association between the cactus Neobuxbaumia tetetzo and the nurse plant Mimosa luisana in the Tehuacan Valley, Mexico. J Ecol 76:961–971 Valiente-Banuet A, Verdú M (2007) Facilitation can increase the phylogenetic diversity of plant communities. Ecol Lett 10:1029–1036 Valiente-Banuet A, Verdú M (2008) Temporal shifts from facilitation to competition occur between closely related taxa. J Ecol 96:489–494 Valiente-Banuet A, Bolongaro-Crevenna A, Briones O, Ezcurra E, Rosas M, Nuñez M, 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 Valiente-Banuet A, Rojas-Martinez A, Casa A, Arizmendi MC, Dávila P (1997) Pollination biology of two winter-blooming giant columnar cacti in the Tehuacán Valley, central Mexico. J Arid Environ 37:331–341 Valiente-Banuet A, Casas A, Alcántara A, Dávila P, Flores-Hernández N, del Coro AM, Villaseñor JL, Ramírez JO (2000) La vegetación del valle de Tehuacán-Cuicatlán. Bot Sci 67:25–74 Valiente-Banuet A et al (2006) Modern Quaternary plant lineages promote diversity through facilitation of ancient Tertiary lineages. PNAS 103:16812–16817 Vera FW, Bakker ES, Olff H (2006) Large herbivores: missing partners of western European light-demanding tree and shrub species? In: Danell K, Bergström R, Duncan P, Pastor J (eds) Large herbivore ecology, ecosystem dynamics and conservation (conservation biology). Cambridge University Press, Cambridge, pp 203–231 Verdú M, Gómez JM, Valiente-Banuet A, Schöb C (2021) Facilitation and plant phenotypic evolution. Trends Plant Sci 26:913–923 Vetaas Ole R (1992) Micro-site effects of trees and shrubs in dry savannas. J Veg Sci 3:337–344 Weltzin JK, Coughenour MB (1990) Savanna tree influence on understory vegetation and soil nutrients in northwestern Kenya. J Veg Sci 1:325–334 Westoby M (1998) A leaf-height-seed (LHS) plant ecology strategy scheme. Plant Soil 199:213–227