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 decreased resource availability in the upper canopy, environmental filtering by microclimate and microhabitat structure, presence of competition in the form of ant mosaics, and structural connectivity. We found although dissimilarity between ant assemblages increased with vertical distance, the dissimilarity was higher horizontally but was independent of distance in this dimension. Moreover, there was not a more rapid increase in horizontal distance-dissimilarity at greater heights in the canopy, as would be predicted if large competitive ant colonies drove these patterns. 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
IntroductionVariation in community composition in space is 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 large spatial scales, turnover between communities is generally driven by dispersal limitation and environmental filtering (i.e. the process where abiotic factors such as climatic gradients prevent species from establishing or persisting in a particular area) (Tuomisto et al. 2003, Qian and Ricklefs 2007, Sreekar et al. 2020). Whereas at small spatial scales, turnover between communities is mostly explained by heterogeneity in habitat, and distance effects can be less important (Kitching et al. 2013, Basham et al. 2018, Sreekar et al. 2020). In addition, biotic factors such as changes in resource availability and interspecific competition can also drive community turnover across multiple spatial scales (Zellweger et al. 2017). This turnover of ecological communities occurs in both vertical and horizontal dimensions (Sreekar et al. 2017). Vertical stratification generated by vegetation height is increasingly recognised as one of the key ecological mechanisms in structuring species distributions and diversity patterns at large spatial scales (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 structured by variation in abiotic conditions and resources (Venegas‐Li et al. 2018, Sheehan et al. 2019, Jorda 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 cause short distance 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 a structurally complex habitat that supports most biologically diverse terrestrial habitat 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). Vertically, due to the interplay between the solar radiation and canopy buffering, air temperature tends to monotonically increase with vertical height while relative humidity tends to monotonically decrease with vertical height (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 height in the canopy (Scheffers et al. 2013), while the maximum air temperature variation between shaded areas and forest gaps can reach 8˚C (Brown 1993). Second, influenced by the changes in abiotic conditions, various nutrient resources, including net primary productivity, carbohydrates and nitrogen, are distributed unevenly from ground to the canopy (Davidson 1997, Malhi et al. 2011), which may also influence the species distributions. Species distribution 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). If there is variation in only the amount of these resources, but not their composition, then this mechanism potentially only drives reductions in abundance and richness, but does not necessarily lead to changes in composition. 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 (e.g. vines) can form links along which organisms can travel (Bélisle 2005, Adams et al. 2017), and horizontal gaps in the canopy can isolate them, leading to high horizontal turnover in community composition (Adams et al. 2017, Adams et al. 2019). For non-flying arboreal ectotherms with limited mobile ability, it could be easier for them to move vertically rather than horizontally when there is lack of connectivity between trees (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 ground level (Antoniazzi et al. 2021). 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 therefore ideal to examine vertical and horizontal turnover in tropical forest (Yusah et al. 2018). The diversity distribution and activity of tropical ants are sensitive to microclimate variation in forest (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, flightless worker ants are likely limited by canopy connectivity (Adam 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 nest resource for arboreal ants, are removed (Adams et al. 2019). Moreover, “ant mosaic” patterns have been observed in canopy ants in many tropical forest sites, with segregation of numerically dominant and subdominant species that establish large colonies and territories (Majer 1993, Davidson et al. 2007, Sanders et al. 2007, Yusah et al. 2018, Dejean et al. 2019). If the territories of dominant ant species (and their species-specific subordinates) are large, then horizontal turnover is expected to be low at short distances in the upper canopy, but then become much greater at the distances which span multiple dominant territories. Conversely, in the lower canopy where the dominant ant species that form mosaics are less abundant, a slower increase in turnover with horizontal distances is predicted. As such, we may expect different horizontal distance-decay patterns from the ground to the canopy if there is strong “ant mosaic” effect on ant assemblage turnover in forest canopies.
Using traverse techniques, we surveyed arboreal ants at fine spatial scale from ground to the canopy at different horizontal positions in tropical rain forest in Sabah, Malaysia. Sabah is home to both the world’s tallest tropical trees and 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. We further partition the dissimilarity into richness difference (nestedness) and replacement (turnover). Specifically, we test a series of hypotheses (that are not necessarily mutually exclusive):
  1. Environmental filtering will generate turnover of ant species both vertically and horizontally and that as a result, this turnover will be correlated with variables important for ants, such as microclimate and canopy structure.
  2. If connectivity is important, then horizontal turnover of assemblages should be greater than vertical turnover of assemblages at comparable spatial scales, since vertical tree architecture can provide connectivity for crawling ant workers.
  3. Ant mosaics will result in rapid horizontal turnover as scale increases beyond that of the typical range of dominant or subdominant ant territory. This pattern is expected to be stronger in the high canopy, where ant mosaics are present, but weaker in the lower canopy, where turnover should increase more gradually.