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):
- 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.
- 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.
- 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.