Role of spatial and environmental factors in structuring vascular epiphyte communities in two neotropical ecosystems

Highlights

• Space was important in determining the structure of epiphytic communities.

• Neutral and niche-based processes act simultaneously on the epiphyte community.

• The importance of different environmental components differed between communities.

• Phorophyte size is central to promote the epiphyte richness and diversity.

Abstract

The great heterogeneity of tropical systems challenges our understanding of how niche and neutral processes structure epiphyte communities. Dispersal, phorophyte identity and the environmental conditions created by phorophytes are the main determinants of vascular epiphyte structure and diversity. However, these forces comprise multiple causal factors that need to be decomposed to address the complex patterns of independent and confounded effects acting upon epiphyte communities. We tested the hypothesis that the environment created by phorophytes (size, bark characteristics, microenvironmental conditions, and substrate type) is more important than phorophyte species identity and space in determining the structure of epiphyte communities, with phorophyte size being a major determinant within the environmental component. We also expected larger phorophytes to exhibit greater epiphyte richness and diversity. The study was carried out on an inselberg within a semi-deciduous montane forest and a cloud forest in southeastern Brazil. Partial redundancy analysis was used to hierarchically decompose the relative abundances of vascular epiphytes into three components: association with particular phorophyte species, the environment created by phorophytes, and space (Moran’s eigenvector maps). Linear models were used to analyze the relationship between epiphytic diversity and richness with size descriptors. We show that neutral and niche-based processes act simultaneously on the dynamics of vascular epiphyte species, but distinctly on the inselberg and cloud forest. The potential for an epiphyte to occupy all favorable phorophytes was larger in the cloud forest due to the higher connectivity offered by trees. Abundance, richness and diversity of epiphytes increased with phorophyte size, probably due to an increase in the area, time of colonization or increase in microhabitat heterogeneity within phorophytes. Larger phorophytes are a major determinant of local environmental conditions and the spatial organization of epiphytes, as they promote their abundance and maintain their diversity in tropical systems.

Introduction

Vascular epiphytes use trees as structural support and represent 9% of all vascular plant species in the world (Zotz, 2016). A variety of non-mutually exclusive factors explain the diversity and coexistence of this diverse group of plants. From a neutral perspective, the distributions and diversity of epiphyte communities can be explained by random events of local dispersal, births and deaths (Wolf, 2005; Zotz and Schultz, 2008; Cascante-Marín et al., 2009). They can also be explained by niche-based processes involving specific adaptations of vascular epiphytes to environmental conditions (Zotz and Schultz, 2008; Dislich and Mantovani, 2016). In tropical forests, few studies have evaluated the role of dispersal limitation and microclimatic conditions created by phorophytes on epiphyte community organization (Zotz and Schultz, 2008; Dislich and Mantovani, 2016). Moreover, due to the high habitat heterogeneity of tropical plant communities (Scarano, 2002; Chave, 2008), it is necessary to broaden the scope of these assessments to lesser-known habitat types to better understand how epiphytic communities are organized in space.

Important factors that explain the organization of vascular epiphytes include neutral processes, such as limited dispersal (Wolf, 2005; Zotz and Schultz, 2008), and niche-based processes that considers environmental variables as the main structuring force of communities. The latter include characteristics of phorophytes such as architecture, growth rate, size, age and identity of the phorophyte, physical and chemical characteristics of the bark, trunk height, crown branch inclination (Zotz and Schultz, 2008; Zhao et al., 2015; Marí et al., 2016; Hayward et al., 2017), and branch fall (Hietz, 1997; Sarmento Cabral et al., 2015). However, arguably the most important factor is tree size (Zhao et al., 2015; Hayward et al., 2017). Large phorophytes (in height or diameter), have larger surface areas that are exposed to seed rain over a long time period, providing more opportunities for colonization (Zhao et al., 2015; Woods, 2017). Larger phorophytes with rougher bark are more favorable for epiphyte establishment (Sáyago et al., 2013; Zhao et al., 2015) because rough bark may promote the establishment of taxa such as Bryophyta (mosses). A substrate composed of mosses has the capacity to retain more moisture, favoring the establishment and survival of later colonizing vascular epiphyte species (Tremblay et al., 1998; Zhao et al., 2015). In this way, phorophyte size is a complex factor that can integrate several ecological characteristics and can be very important in determining the structure of epiphyte communities (Sáyago et al., 2013). Other important factors that have been shown to affect epiphyte communities include edaphic characteristics (Boelter et al., 2014), environmental conditions (e.g. humidity, temperature, wind and radiation) (Werner, 2011), association with non-vascular epiphytes (mosses and lichens) (Callaway et al., 2001; Zhao et al., 2015), climate change (Benzing, 1998), and disturbances (Hietz et al., 2006; Nadkarni and Kohl, 2018).

Evidence suggests that dispersal limitation, determined by spatial processes, along with environments created by phorophytes, and phorophyte identity are also important process explaining the distribution of vascular epiphytes (Wolf, 2005; Zotz and Schultz, 2008; Wagner et al., 2015). However, neutral and niche-based processes comprise multiple causal factors that need to be decomposed to address the complex patterns of independent and confounded effects acting on epiphyte communities. Understanding the simultaneous interaction of niche and neutral processes is particularly important considering the growing interest in analyzing the combined influence of these processes (Guèze et al., 2013; Matthews and Whittaker, 2014).

In this study, we aimed to identify the relative importance of phorophyte identity, environmental characteristics created by phorophytes and space in explaining the relative abundances and diversity of vascular epiphytes in tropical plant communities (inselberg and cloud forest). The inselberg’s vegetation represents xeric ecosystems, isolated in the landscape and historically neglected in studies of vascular epiphytes compared to forest ecosystems. Understanding the simultaneous interaction of niche and neutral processes in explaining how epiphyte communities are organized in contrasting ecosystems can improve our understanding of the functioning and conservation measures in these ecosystems and their epiphyte communities. Phorophyte identity tests the distribution patterns of epiphytes caused by association with specific phorophytes. The environment is determined by the substrate provided by phorophytes as well as microenvironmental factors (e.g. size, bark type, illumination index, among others). Space is related to dispersal processes (dispersal limitation), which are important for testing the role of neutral factors in explaining spatial patterns in biological communities (Hubbell, 2001). We tested the hypothesis that environmental conditions created by phorophytes are more important in determining the structure of epiphytic communities than spatial structures and phorophyte species identities. When partitioning such environmental components, size-related properties should be more important than bark characteristics, illumination index and substrate type. We also expected larger phorophytes to exhibit higher epiphytic richness and diversity.