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.