Oecologia (2016) 181:533–541 DOI 10.1007/s00442-016-3586-5 COMMUNITY ECOLOGY – ORIGINAL RESEARCH Fungal phylogenetic diversity drives plant facilitation Alicia Montesinos-Navarro1,2 · J. G. Segarra-Moragues1,3 · A. Valiente-Banuet2,4 · M. Verdú1 Received: 21 May 2015 / Accepted: 8 February 2016 / Published online: 25 February 2016 © Springer-Verlag Berlin Heidelberg 2016 Abstract Plant–plant facilitation is a crucial ecological when plant facilitative interactions persist than when they process, as many plant species (facilitated) require the pres- do not persist. However, persistent and non-persistent facil- ence of an established individual (nurse) to recruit. Some itative interactions did not differ in the phylogenetic diver- plant facilitative interactions disappear during the ontoge- sity of mutualistic fungi added by the facilitated species netic development of the facilitated plant but others persist, to the shared rhizosphere. Finally, the fungal phylogenetic even when the two plants are adults. We test whether the diversity added by the nurse to the shared rhizosphere did persistence of plant facilitative interactions is explained by not differ between persistent and non-persistent interac- the phylogenetic diversity of mutualistic and non-mutual- tions. This study suggests that considering the fungal asso- istic fungi that the nurse and the facilitated species add to ciates of the plant species involved in facilitative interac- the shared rhizosphere. We classify plant facilitative inter- tions can shed light on the mechanisms of persistence for actions as persistent and non-persistent interactions and plant–plant interactions. quantify the phylogenetic diversity of mutualistic and non- mutualistic fungi added by the plant species to the shared Keywords Community assembly · Aboveground– rhizosphere. Our results show that the facilitated species belowground · Phylogenetic structure · Plant facilitation · add less phylogenetic diversity of non-mutualistic fungi Fungal multifunctionality Communicated by Edith B. Allen. Introduction Electronic supplementary material The online version of this article (doi:10.1007/s00442-016-3586-5) contains supplementary The role of biotic interactions as drivers of community material, which is available to authorized users. assembly has traditionally interested ecologists, who have provided multiple examples of how interacting guilds can * Alicia Montesinos‑Navarro reciprocally shape their species assemblages (Janzen 1970; [email protected] Connell 1971; Packer and Clay 2000; Wolfe et al. 2005; 1 Centro de Investigaciones sobre Desertificación (CIDE, Cahill et al. 2008; Waterman et al. 2011; Montesinos-Nav- CSIC-UV-GV), Carretera de Moncada‑Náquera Km 4.5, arro et al. 2015). In the case of plant communities, plant 46113 Moncada, Valencia, Spain species composition can influence the assembly of mutual- 2 Departamento de Ecología de la Biodiversidad, Instituto de istic and non-mutualistic partners (Thrall et al. 2007; Enci- Ecología, Universidad Nacional Autónoma de México, A.P. nas-Viso et al. 2012), which in turn can influence plant– 70-275, C.P. 04510 Mexico, D.F., Mexico plant interactions through indirect effects (Janzen 1970; 3 Departamento de Biología Vegetal, Facultad de Ciencias Connell 1971; Van der Putten et al. 2001; Montesinos-Nav- Biológicas, Universitat de València, Avda. Dr. Moliner, 50, 46100 Burjassot, Valencia, Spain arro et al. 2012a). When interactions between mutualistic and non-mutualistic plant partners occur, the outcome of 4 Centro de Ciencias de la Complejidad, Ciudad Universitaria, Universidad Nacional Autónoma de México, 04510 Mexico, plant–plant interactions and their persistence may be diffi- D.F., Mexico cult to predict. 1 3 534 Oecologia (2016) 181:533–541 Plant facilitation is a crucial process structuring com- calculate the relative fungal phylogenetic diversity added munity assemblages (Valiente-Banuet and Verdú 2008) by the nurse and the facilitated plant species in 60 pair-wise and maintaining biodiversity (Valiente-Banuet et al. 2006; plant–plant interactions. We tested whether persistent and Valiente-Banuet and Verdú 2007), especially in semiarid non-persistent interactions differ in the fungal phyloge- environments. Plant facilitation is a positive plant–plant netic diversity added by the nurse and the facilitated spe- interaction in which a nurse species provides another facili- cies. We expect that in persistent interactions, the nurse and tated species with a regeneration niche without incurring facilitated species will add more mutualistic and less non- any disadvantage to the nurse (Callaway 2007), which mutualistic diversity to the shared rhizosphere than in non- sometimes benefits both plants (Sortibrán et al. 2014). Plant persistent interactions. facilitative interactions show certain specificity, resulting in some plant–plant pairs prevailing over others (Verdú et al. 2010). Two processes can result in the avoidance or Materials and methods non-persistence of a plant facilitative interaction. On one hand, the microclimate provided by a nurse can match the Study site recruitment requirements of a subset of facilitated species in the community, but not all of them (Verdú et al. 2010). This work was performed in a natural community in the On the other hand, the benefits of the association can shift semiarid valley of Zapotitlán, in the state of Puebla, Mex- to competition along the ontogeny of the facilitated plant ico (18°20N, 97°28W) (Valiente-Banuet and Verdú 2008; (Valiente-Banuet and Verdú 2008; Armas and Pugnaire Verdú et al. 2010; Montesinos-Navarro et al. 2012b). The 2009; Incerti et al. 2013; Rolo et al. 2013). However, when vegetation in this area is a xeric shrubland dominated by the benefits of plant facilitative interactions persist over the columnar cactus Neobuxbaumia tetetzo (J.M. Coult.) time, there will be spatial associations between the adult Backeb, Agave spp. and different species belonging to individuals of the nurse and facilitated species (Valiente- the families Fabaceae, Malpighiaceae, Verbenaceae and Banuet and Verdú 2008). Asteraceae. The strength of facilitative interactions increases between plant species which have distinct arbuscular myc- Plant–plant facilitation orrhizal fungi, probably reflecting a diverse functional- ity in the rhizosphere (Montesinos-Navarro et al. 2012a). The interactions studied involved six nurse species [Aca- However, it is usually difficult to assess the functional cia constricta Benth., Caesalpinia melanadenia (Rose) profile of the fungal community because few fungal traits Standl., Eysenhardtia polystachya (Ortega) Sarg., Mimosa with ecological relevance are known for most fungal taxa. luisana Bragndegee, Mascagnia seleriana Loes., Senna When there is little functional information, the use of phy- wislizeni (A. Gray) H.S. Irwin & Barneby] and ten facili- logenetic diversity can be convenient as the evolutionary tated species [Agave karwinskii Zucc., Caesalpinia mela- relatedness between taxa is a good proxy of functional trait nadenia, Coryphantha pallida Britton & Rose, E. poly- similarity (Cadotte et al. 2008); phylogenetic relationships stachya, Justicia mexicana Rose, Mammillaria mystax have been suggested to broadly reflect species functional Mart., Mammillaria collina J.A. Purpus, N. tetetzo, Ruellia diversity. hirsutoglandulosa (Oerst.) Hemsl., and S. wislizeni]. Some Fungal functional diversity influences plant communi- species can be facilitated by a nurse, but act also as a nurse ties. Mycorrhizal fungal richness and phylogenetic diversity of other species (Valiente-Banuet and Verdú 2013). Sixty have been shown to promote plant coexistence and increase potential interactions were considered, including also plant biomass (Van der Heijden et al. 1998; Maherali and those in which the same plant species can act as a nurse Klironomos 2007; Wagg et al. 2011). However, non-mutu- and as a facilitated plant (auto-facilitation). Different indi- alistic fungi, even if they are not strictly considered as path- viduals of each species were considered according to their ogens, may compete for space with mutualistic fungi in the relative abundance in the community (Table S4). There is plant root (Filion et al. 1999; Bodker et al. 2002; Roger accumulated evidence in this system to support that plant– et al. 2013; Thonar et al. 2014). In this sense, a higher func- plant associations are driven by facilitation (Valiente-Ban- tional (and phylogenetic) diversity of non-mutualistic fungi uet and Verdú 2007, 2008; Verdú et al. 2010; Verdú and might reduce the available niche for mutualistic fungi, Valiente-Banuet 2011), including experimental evidence potentially reducing plant performance and coexistence. In for some species in the community (Castillo et al. 2010). this study we hypothesize that the persistence of plant facil- Plant–plant facilitation matrices from Valiente-Banuet and itative interactions is influenced by the phylogenetic diver- Verdú (2008) and Verdú et al. (2010) were used to charac- sity of mutualistic and non-mutualistic fungi added by the terize plant–plant interaction persistence. In these studies, facilitated and nurse species to the shared rhizosphere. We the number of seedlings growing beneath the canopies of 1 3 Oecologia (2016) 181:533–541 535 other species and in the bare ground were counted along for space in the plant roots (e.g. Filion et al. 1999; Bodker four transects of 1,000 m in three different sites. This et al. 2002; Roger et al. 2013; Thonar