4 Discussion
We observed different patterns in species assemblage distribution over vertical and horizontal gradients in a complex habitat. The high local diversity of arboreal ants can be explained by high environmental and habitat heterogeneity along both horizontal and vertical dimensions. The replacement of individuals and species, rather than their loss is the major component of total assemblage dissimilarity both vertically and horizontally, indicating a potential environmental filtering process in maintaining high biodiversity across small spatial scales (Baselga 2010). We found consistently greater horizontal turnover in ant assemblages than that observed at comparable vertical distances. However, increase in turnover with distance was only detected vertically, but not horizontally, with the high species turnover between horizontal positions being independent of distance. The observed patterns are likely associated with continuous directional changes in environment (i.e., microclimate) and resources vertically, and stochastic variation in environment and resource, as well as poor connectivity horizontally.
We found the spatial distribution of ant assemblages was associated with heterogeneity in air temperature and relative humidity within the three-dimensional structure of the forest. The spatial distribution pattern of microclimate variables in our study plot is in line with other studies: air temperature increased with height above ground, while relative humidity decreased (Davis et al. 2019, De Frenne et al. 2019). Horizontal variation in microclimate was also high but without directional change, presumably relating to variation in vegetation structure within and between trees (Fetcher et al. 1985, Scheffers et al. 2017). Such non-directional horizontal variation in microclimate may contribute to the high turnover of ant assemblages and lack of distance-decay pattern in this dimension at the scales we sampled. Given that turnover at very short horizontal distances was already nearly maximal, it would not have been possible for turnover to then be even greater with increasing horizontal distance. Tropical arboreal ants show thermal adaptation to their vertical habitat use through their physiology (Kaspari et al. 2015), morphology (Law et al. 2020) and nesting site selection (Plowman et al. 2019). The high variance in microclimate generates diverse thermal niches for ant species with different thermal tolerances, and hence can facilitate co-existence of multiple species at small spatial scales (Lessard et al. 2009). For tiny ectotherms like ants, fine-scale environmental heterogeneity can play an essential role in defining their distributions, probably due to the small foraging range and small body size of ants, and the thermal diversity of the environment (Ribas and Schoereder 2007, Fayle et al. 2010, Klimes et al. 2012, Kaspari et al. 2015, Bütikofer et al. 2020). The association between microclimate pattern and ant assemblage composition may not only result from direct effects through environmental preferences of ant species, but can also be a consequence of indirect biotic effects, for example if microclimate influences ant food availability. However, the relative importance of direct and indirect microclimate influences on ant assemblage composition remains to be investigated.
In addition to microclimate, biotic influences such as resource limitation and vegetation structure may also contribute to the high horizontal turnover observed. The decline in ant richness and abundance with height in the canopy could be due to reduction in leaf area which limits foraging range and nest site availability (Adams et al. 2019, Plowman et al. 2019). However, partitioning analyses of vertical pairwise dissimilarity demonstrated that the changes in ant assemblages was mostly driven by the turnover of the assemblage rather than the nestedness of assemblage, which implicated that environmental filtering, rather than resource limitation is a more plausible explanation (i.e. different resources, rather than just less of the same resources). Ant assemblage composition can be affected by vegetation structure such as tree size, number of branches, and cavity diversity (Powell et al. 2011, Yusah and Foster 2016, Adams et al. 2019, Plowman et al. 2019). Hence, we can expect distinct ant communities to be hosted by different individual trees and that the distance between trees per se might not be driving assemblage dissimilarity. The lack of distance effects on high horizontal turnover arboreal ants in our study is consistent with that found in canopy ant assemblages across greater horizontal distances (100-700 m) in rain forest of Mexico, whereas a distance-decay pattern was observed in ground ant assemblages (Antoniazzi et al. 2021). For social insects like ants where workers are wingless, vertical movement of workers within the colony tree can be less challenging than movement between trees, especially without vegetation connections such as lianas (Yusah and Foster 2016, Adams et al. 2019), which may be lessened in Asian versus American tropics (Dial et al. 2004a). Such barriers between individual trees could make each tree canopy function as an island within the forest (Southwood and Kennedy 1983, Adams et al. 2017).
We did not find any evidence to support the existence of ant mosaics at the scales sampled, since turnover was not higher in the upper canopy, where ant mosaics are more likely to influence community structure (Ribeiro et al. 2013, Yusah et al. 2018). However, previous work conducted close to our study site has found evidence for segregation between species in the high canopy (Yusah et al. 2018). This could be because our horizontal sampling grain was 20 m, and hence most adjacent horizontal samples might already fall in different territories, on different trees, with the exception of species with very large territories such as Dinomyrmex gigas (Pfeiffer and Linsenmair 2001). This is supported by the high horizontal turnover in species composition that we observed, regardless of distance across all heights in the canopy.
Our findings offer important insights into the way in which biodiversity is maintained at fine scales in complex three-dimensional habitats. The high species richness discovered within the 130 m long by 70 m high vertical plot in our study site represents a high proportion of ant diversity at larger scales. The number of species that we detected using precision fogging across vertical strata among 11 trees reached about 40% of the number of species sampled in a similar forest habitat elsewhere in Sabah from 99 trees (Floren et al. 2014). This finding of a relatively large proportion of regional biodiversity being sampled from small plots within rain forest is in line with patterns for herbivorous insects (Novotny et al. 2007), birds (Huang and Catterall 2021) and butterflies (Daily and Ehrlich 1995), and is likely driven by high structural complexity at small scales. The high turnover of the ant assemblages across short horizontal and vertical distances explains how a high proportion of local biodiversity of arthropods can be detected by comprehensive sampling of the ground and canopy at small spatial scales (Basset et al. 2012). While previous studies have pointed out the importance of including both canopy and understory communities when examining assemblage composition at large spatial scales (Ashton et al. 2016), our results suggest that comprehensive sampling covering multiple horizontal and vertical planes may allow detection of a large proportion of certain species that utilize multiple dimensions of the space, even when sampling a relative small area of the habitat. Future sampling across multiple vertical and horizontal replicates at microhabitat scales for various taxa, particularly for groups that are sensitive to microclimate and with limited dispersal abilities such as non-flying arthropods, are needed to test the generality of high community dissimilarity over small horizontal distances.
Our study highlights the great conservation value of primary tropical rain forest in supporting high diversity of arboreal arthropods. Compared with disturbed forest, primary tropical rain forest exhibits higher complexity in vegetation structure, greater level of vertical stratification and larger vertical distances due to the presence of taller trees (Klimes et al. 2012, Liu et al. 2016). For instance, in oil palm plantation, which has displaced large areas of forest in tropical Asia (Fitzherbert et al. 2008), canopy ant species richness is 52% lower compared with primary rain forest, possibly due to the simplification of canopy structure (Fayle et al. 2010). The observed high beta diversity supported by vertical forest layers in our study indicates a potential risk of biodiversity loss among arboreal insects with the reduction of these important vertical niches through logging and conversion to plantation. The heterogeneity in microclimates of rain forest may also increase the climate change resilience of tropical species by providing them high microclimate heterogeneity to track their optimal climatic niche for activity (Scheffers et al. 2013, Pincebourde and Suppo 2016).