An Overview on Epiphytism As a Direct Mechanism of Facilitation in Tropical Forests

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An Overview on Epiphytism As a Direct Mechanism of Facilitation in Tropical Forests Tropical Ecology 59(1): 1–9, 2018 ISSN 0564-3295 © International Society for Tropical Ecology www.tropecol.com An overview on epiphytism as a direct mechanism of facilitation in tropical forests TALITHA MAYUMI FRANCISCO1*, MÁRIO LUÍS GARBIN2, CAMILA DE TOLEDO CASTANHO3 & CARLOS RÁMON RUIZ-MIRANDA1 1Programa de Pós-Graduação em Ecologia e Recursos Naturais, Laboratório de Ciências Ambientais, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Avenida Alberto Lamego, 2000, Parque Califórnia, 28035-200, Campos dos Goytacazes, RJ, Brazil 2Programa de Pós-Graduação em Ecologia de Ecossistemas, Laboratório de Ecologia Vegetal, Universidade Vila Velha, Rua Comissário José Dantas de Melo, s/n, Boa Vista, 29102-770, Vila Velha, ES, Brazil 3Departamento de Ciências Ambientais, Universidade Federal de São Paulo, Rua Prof. Artur Riedel, 275, Jd. Eldorado, 09972-270, Diadema, SP, Brazil Abstract: Direct facilitation is characterized by the positive effect of one individual on the other through changes in abiotic conditions and the creation of novel habitats. We aimed to present a systematic review of the literature about direct facilitation in tropical forests, emphasizing knowledge gaps and suggesting future lines of inquiry. We asked: (1) What is the existing literature about direct facilitation in tropical forests? (2) What kind of methodological approach (experimental or observational) has been more used? (3) What kind of study, pairwise species or community level, are more common? (4) What vegetative habits are more common between facilitators and facilitated species? (5) What hypotheses are more commonly tested? (6) How often epiphytism has been approached as facilitation? Based on literature search, we found thirty-five studies examining direct facilitation in plants mainly in the Neotropics (69%). The number of observational and experimental studies was similar. Most studies were based on pairwise comparisons of species. Trees were the most common nurse plants representing 51% of the studies, followed by shrubs (20%). This was the same for facilitated plants: trees corresponded to 48% and shrubs to 21%. The most common facilitation mechanism in tropical forest was the improvement of aboveground microclimate conditions (43%). Epiphytism is still marginally explored (11%, only 4 out of 35 studies) as a direct mechanism of facilitation. Given that about nine per cent of the world vascular flora are epiphytes that demand facilitators to survive, it is timely to widen the scope of field studies about facilitation towards such direct mechanisms. Key words: Commensalism, Neotropical, plant community, plant-plant interaction, positive interaction, systematic review. Introduction Walker 1997; Holmgren et al. 1997). The balance between the positive and negative effects that one Interactions between plants are positive (e.g., individual plant causes on the other in growth, facilitation) or negative (e.g., competition) and they survival or reproduction, is the basis for such simultaneously play key roles in the organization distinction (Bertness & Callaway 1994). For and functioning of plant communities (Callaway & instance, Anthelme et al. (2011) studied the effect of *Corresponding Author; e-mail: [email protected] 2 DIRECT FACILITATION IN TROPICAL FORESTS the grass Setaria sphacelata (Poaceae) on palm tree instance, the shade provided by the canopy of trees seedlings in cloud forests of Ecuador. The shade and shrubs can protect plants from extreme provided by the grass considerably reduced above temperatures, winds, solar radiation, reducing and belowground water stress. This effect water loss, and increasing soil moisture to other counterbalanced the negative effects of competition, plant species, thus promoting microclimate resulting in a positive effect of grass on palm conditions (Callaway 1995; Callaway 2007). seedlings. Although poorly documented, facilitator plants also Facilitation between plants may be thus defined directly modulate the availability of resources to as a positive, non-trophic, interaction, between other organisms, creating new habitats at which physiologically independent plants, which benefits many species depend on (Jones et al. 1997). at least one of the organisms involved (species or Especially in tropical forests, trees can be individuals) (Brooker et al. 2008). It can occur when facilitators by providing habitat through structural the presence of a facilitator modifies local micro- support for various taxa (e.g., nonvascular environment more favorable to other (facilitated) epiphytes such as lichens and mosses, vascular plants (Brooker et al. 2008; Bruno et al. 2003; epiphytes such as ferns, orchids, bromeliads, aroids, Callaway 1997), improving reproduction, growth climbing plants, among others) allowing the and survival of at least one of the involved establishment and survival of these groups (Burns organisms (Callaway 2007). Facilitation can result 2007; Garbin et al. 2012; McIntire & Fajardo 2014). in positive, neutral or negative effects for the In this way, direct interactions can occur in plant facilitator plants (Bronstein 2009; Callaway 2007). communities and have an important role in species Therefore, facilitative interactions between species coexistence (Lang et al. 2012) influencing the may occur through mutualism, commensalism or structure (Filazzola & Lortie 2014) and promoting parasitism (Bronstein 2009; Callaway 2007; Lin et diversity in plant communities (Garbin et al. 2012; al. 2012). Commensalism between plants is Hacker & Gaines 1997; McIntire & Fajardo 2014). demonstrated by epiphytism (Burns 2007; Flores- While most known examples of facilitation in plants Palacios 2016). It comprises those plant species that come from systems with stressful environmental use trees (phorophytes) as structural support. The conditions (e.g., salt marsh, arid and semi-arid phorophytes are facilitators for providing a vital environments, deserts, and alpine environments, space above the forest floor for the establishment of see Bronstein 2009), facilitation may also be epiphytes and the facilitated plants generally (or important in many other ecosystems, particularly supposedly) has a neutral effect on phorophytes. in the tropics. However, there are relatively few This is a reasonable case of facilitation (Ewel & studies in these environments (Bonanomi et al. Hiremath 2005; McIntire & Fajardo 2014). These 2011; Castanho et al. 2015). facilitated plants need the support of phorophytes We aimed to prepare a systematic review about to survive, but not nutrients and water that are direct facilitation in tropical forests, emphasizing provided by moist air or rainwater (Benzing 1990; knowledge gaps and directing future research. We Burns 2007). Importantly, there is a large array of asked: (1) What is the existing literature about studies about epiphytism in tropical systems and direct facilitation in tropical forests? (2) What kind they have not been synthesized yet under the scope of methodological approach (i.e., experimental or of facilitation theory. observational) has been more used? (3) What kind Facilitation has a key role in maintaining and of study, pairwise species or community level, are promoting the diversity of plant communities more common? (4) What vegetative habits (trees, (Hacker & Gaines 1997; McIntire & Farjado 2014). shrubs, herbs, climbers) are more common among These positive effects occur through a wide variety facilitators and facilitated species? (5) Which of direct mechanisms (see Callaway 1995; Callaway hypotheses are more commonly tested? (6) How 2007) caused by facilitator species in changing often epiphytism (as a commensal +/0 interaction) conditions and resources favoring facilitated species has been approached as facilitation? The role of (Bertness & Callaway 1994; Brooker et al. 2008; epiphyte-phorophyte interactions as a key McIntire & Farjado 2014). The direct mechanism is facilitative process, especially in tropical forests, in characterized by the effect of one species over promoting and maintaining species diversity has another, i.e., it does not require another, third, been seldom studied. We argue that the inclusion species (Callaway 1995; Callaway 2007). For of epiphytism into facilitation theory expands the FRANCISCO et al. 3 Fig. 1. Flow diagram describing the search protocol and the articles included for the systematic review. Adapted from Moher et al. (2009). See text for criteria used for exclusions. scope of positive interactions adding an important made in the topic field “topic terms" of the database vertical dimension to the mechanism. that searches for words in the title, abstract, keywords, articles and keywords. Articles in all Methods languages were included in this search. The review included a personal database with additional Literature research method references (Fig. 1). A literature review was conducted including From ISI, 109 research articles were found. For research articles published and indexed between the first criterion (Fig. 1), an initial screening of 1945-2015 that examined and provided evidence titles, abstracts and keywords was conducted, and about direct facilitation between plants in tropical the articles were excluded if: (1) they comprised forests. The literature was consulted using the ISI literature reviews, 2) the interacting organisms database Web of Science® on November 4, 2015 were not plants (e.g., animal-plant interactions), (3) using a combination of three groups of terms: (1) they were related to indirect
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