Abstract
Abiotic and biotic factors structure species assembly in ecosystems both horizontally and vertically. However, the way community composition changes along comparable horizontal and vertical distances in complex three-dimensional habitats, and the factors driving these patterns, remain poorly understood. By sampling ant assemblages at comparable vertical and horizontal spatial scales in a tropical rain forest, we compared observed patterns with those predicted according to environmental filtering by microclimate and microhabitat structure. We found that although dissimilarity between ant assemblages increased with vertical distance, the dissimilarity was higher horizontally but was independent of distance. The pronounced horizontal and vertical structuring of ant assemblages across short distances is likely explained by a combination of microclimate and microhabitat connectivity. Our results demonstrate the importance of considering three-dimensional spatial variation in local assemblages and reveal how highly diverse communities can be supported by complex habitats.
Keywords : community ecology, distance-decay, habitat complexity, microclimate, species turnover, vertical stratification
IntroductionThis turnover of ecological communities occurs in both vertical and horizontal dimensions (Sreekar et al. 2017), which can be explained by both biotic and abiotic factors, as well as their interactions (Cottenie 2005). The relative importance of these processes in determining community composition varies with spatial scale (Nekola and McGill 2014). At small spatial scales, turnover between communities is mostly explained by heterogeneity in habitat (Kitching et al. 2013, Basham et al. 2018, Sreekar et al. 2020). Vertical stratification is increasingly recognised as one of the key ecological mechanisms in structuring species distributions and diversity patterns. Habitats with high vertical complexity, such as forests, often house more species than habitats with low structural complexity (Oliveira and Scheffers 2019). Vertical stratification of communities has been documented for a range of habitats, from deep ocean to tropical forest, and is largely driven by variation in abiotic conditions and resources (Venegas‐Li et al. 2018, Sheehan et al. 2019, Jorda et al. 2020). For example, in pelagic ecosystems, distance from insolation at the water surface drives vertical stratification (Li et al. 2020), whereas in terrestrial ecosystems shifts in vegetation structure with height can be important (Jarron et al. 2020). Although species turnover in relation to horizontal distance has been examined at large spatial scales (Chesters et al. 2019), it is often considered to be negligible at small scales, and therefore has rarely been incorporated into studies of vertical stratification (Roisin et al. 2006, Weiss et al. 2016). However, in complex ecosystems with high three-dimensional structural heterogeneity, such as coral reefs and tropical rain forests, abiotic and biotic factors can vary greatly at small horizontal and vertical scales (Reaka-Kudla 1997), which may drive small scale variation in community composition (Davies and Asner 2014). Although numerous studies have investigated how species diversity changes with horizontal and vertical distance, few have assessed both dimensions simultaneously at comparable spatial scales (Wermelinger et al. 2007). Tropical rain forest is one of the most structurally complex and biologically diverse habitats on earth (Ehrlich and Wilson 1991). In this habitat, the heterogenous environment from the ground to the canopy generates high microclimatic and structural complexity (Scheffers et al. 2013, Nakamura et al. 2017). First, microclimate, including air temperature, humidity and light intensity, can vary significantly along both vertical and horizontal dimensions and shape community composition through environmental filtering (Parker 1995, Scheffers et al. 2017). With increasing height, air temperature tends to monotonically increase while relative humidity tends to monotonically decrease due to the interplay between solar radiation and canopy buffering (Scheffers et al. 2013). Horizontally, microclimate can vary between open and shaded areas such as forest gaps and closed canopy forest (Fetcher et al. 1985, Parker 1995, Scheffers et al. 2017), although any monotonic changes clearly cannot persist over longer distances. For example, maximum air temperature can vary by as much as 2.2˚C between the ground and 20 m above the forest floor in the canopy (Scheffers et al. 2013), while differences in maximum air temperature between shaded areas and forest gaps can exceed 8˚C (Brown 1993; Kaspari et al., 2015; Stark et al. 2017). Second, influenced by the changes in abiotic conditions, various nutrient resources are distributed unevenly from ground to the canopy (Davidson 1997, Malhi et al. 2011), which may also influence community composition. Species distributions can be limited by key resources, such as food, habitat and supporting vegetation structure including tree size and leaf area (Dáttilo et al. 2014, Klimes 2017, Plowman et al. 2019). Finally, microhabitat connectivity can also play an important role in shaping community composition in rain forest (Ramette and Tiedje 2007, Adams et al. 2019). Physical structures such as lianas, can form links along which organisms can travel (Bélisle 2005, Adams et al. 2017), when horizontal gaps in the canopy would otherwise isolate them, leading to high horizontal turnover in community composition (Adams et al. 2017, Adams et al. 2019). For non-flying arboreal organisms with limited ability to move, vertical movement is likely to be easier than horizontal movement when connectivity between trees is low (Adams et al. 2017). In addition, the interaction between resource availability and connectivity can also influence the importance of competition in driving species turnover (Matthiessen et al. 2010, Parr and Gibb 2010). Of the few studies considering variation in composition in both horizontal and vertical dimensions in tropical rain forest, patterns documented are idiosyncratic and tend to be taxon-dependent (Basham et al. 2018, Antoniazzi et al. 2021). The relevant scale when investigating spatial patterns of beta diversity can be dependent on the behavioural, morphological and physiological traits of the study organism and the variation in the habitat (Soininen et al. 2018). For amphibians in Madagascar, distance-decay was only found in the canopy and understory but not on the ground, which may be explained by limited habitat connectivity in the canopy (Basham et al. 2018). Conversely, distance-decay has been detected only in ground assemblages but not in canopy assemblages for ants in secondary forest in Mexico, which may relate to the higher dispersal capacity and larger territories of canopy ants, as well as higher microhabitat heterogeneity at the ground level (Antoniazzi et al. 2021). Nevertheless, how beta diversity of rain forest fauna changes at comparable horizontal and vertical distances remains largely unknown (Dial et al. 2004a, Nakamura et al. 2017), partly due to the technical challenges in conducting sampling across replicated horizontal positions for a range of vertical heights (Dial et al. 2004a).
Tropical arboreal ants are abundant and ecologically important, and are therefore an ideal study system to examine vertical and horizontal turnover in tropical forest (Yusah et al. 2018). The distribution and activity of ants in tropical forests are sensitive to microclimate variation (Kaspari 1993, Perfecto and Vandermeer 1996). The key resources ants rely on change with height in the canopy (Kaspari and Yanoviak 2001), and hence environmental filtering is expected to be important in determining ant community turnover. Furthermore, movement of flightless worker ants are likely limited by canopy connectivity (Adams et al. 2019). A large-scale experiment has demonstrated that the species richness, composition, and beta diversity of ants significantly changes after lianas, which provide both connectivity and nesting resources for arboreal ants, are removed (Adams et al. 2019).
Using traverse techniques, we surveyed arboreal ants at small spatial scale from the ground to the canopy at different horizontal positions in tropical rain forest in Sabah, Malaysia, which is home to both the world’s tallest tropical trees and extremely high arthropod biodiversity (Shenkin et al. 2019). We tested how pairwise dissimilarity of ant assemblages across different vertical and horizontal positions related to spatial distance, microclimate and microhabitat structure. Specifically, we test two hypotheses that are not necessarily mutually exclusive (Fig. 1):
Environmental filtering will generate turnover of ant species (and therefore beta diversity) at small scales due to changes in microclimate and canopy structure. This will occur both vertically (e.g. ground-to-canopy temperature gradients) and horizontally (e.g. open vs closed areas temperature differences).
Habitat heterogeneity (connectivity) will create greater horizontal turnover of assemblages (and therefore beta diversity) than vertical turnover at small scale, as vertical tree architecture (trunks) provides connectivity for crawling ant workers.