interspecific variations in movement trajectories
The segregation of small mammals in tropical assemblages along vertical strata and/or by body size is considered to favour coexistence in species-rich communities (e.g. Charles-Dominique et al. 1981; Janson & Emmons 1991; Malcolm 1995; Voss & Emmons 1996; Bakker & Kelt 2000; Cunha & Vieira 2002). Although most studies have been conducted up to now in the neotropics and less is known about small mammal assemblages in the forests of South-east Asia, similar patterns in substrate use have been suggested for the neo- and the palaeotropics because of general constraints in climbing ability and adaptations to the arboreal/scansorial habitat (Emmons 1995).
Our results demonstrate that small Bornean mammals, which are mostly characterized as terrestrial/scansorial, differ in their movement trajectories with regard to several structural habitat features. Conversely, we found no differences in structural path properties that might indicate differences in movement patterns of species that differ in habitat use or morphometric features, despite the increase in step lengths with body size. Our results contrast with a study on small-scale movement strategies of American martens that were associated with structural features (Nams & Burgeois 2004). The small-scale movement pattern should differ from movements on larger scales as a response to resource distribution, which might more likely represent large-scale effects of habitat variability (e.g. Johnson et al. 2002; Ramos-Fernández et al. 2004; Soléet al. 2005).
Overall, our results revealed for the local assemblages on Borneo five groups of small mammals in relation to habitat use: (1) terrestrial species (M. rajah, M. surifer); (2) species that were mostly active on the ground but occasionally reached the upper canopy (L. sabanus); (3) terrestrial species with frequent scansorial activity (T. tana, T. longipes); (4) scansorial species that were not active in the canopy (T. gracilis, S. lowii); and, finally (5) arboreal species that occasionally approached the ground (N. cremoriventer, T. minor). We confirmed occasional arboreal activity of L. sabanus, although this species spends proportionally much more time on the ground than the scansorial species S. lowii and T. gracilis.
The general activity patterns were similar to those noted for mammal assemblages in the neotropics (see Charles-Dominique et al. 1981; Voss & Emmons 1996; Cunha & Vieira 2002). However, in contrast to studies at neotropical sites, climbing activity of small mammals was not related to body size but rather to morphometric measures (HF/HB and T/HB), indicating that species of variable sizes are adapted to cursorial vs. arboreal activity. Although some convergences of small mammals have been reported for neo- and palaeotropic assemblages (see Emmons 1995), patterns in body-size distribution cannot necessarily expected to be equivalent. It has been suggested that arboreal vertebrates in the neotropics are in general smaller than palaeotropical vertebrates because canopy structure is reported to be more fragile in the neotropics (Cristoffer 1987). Differences in morphological modifications such as gliding that occurs predominantly in the palaeotropics or prehensile tails that are prevalent in the neotropics may in turn affect accessibility and use of vegetation structures (Emmons & Gentry 1983). On the other hand, studies on neotropical assemblages of small mammals that contained only few species usually included also some larger bodied, mostly terrestrial didelphids, such as Didelphis spp. or Metachirus spp. (body mass > 500 g and 1 kg, respectively; references above) that might have biased the conclusions on body size distribution drawn from these assemblages.
Interestingly, habitat segregation was weak between the two species pairs based on similarities in morphology: Maxomys rajah and M. surifer as well as T. longipes and T. tana. However, as both species pairs exhibit paraphyletic relationships (Ruedas & Kirsch 1997; Han, Sheldon & Stuebing 2000), similarities in morphological appearance and body size represent convergent adaptations to their similar life styles and ecological niches. In contrast, the two smaller treeshrews T. gracilis and T. minor, which also exhibited substantial convergence in body size and morphology (Han et al. 2000), used distinct habitats along the vertical axis. Whereas T. gracilis was confined to the scansorial layer, T. minor was active in the upper canopy with occasional descents to the ground.
The two larger treeshrews T. longipes and T. tana, which have been mainly described as terrestrial based on field observations (Emmons 2000) and morphological traits (Sargis 2001), revealed greater climbing activity than terrestrial spiny rats, with half of all of their tracks reaching heights of 1 m or higher. Although both species were similar with regard to their movement trajectories, the higher scansorial activity of T. tana was not expected because it had been reported to actively dig in the leaf litter and soil for foraging, whereas the prey of T. longipes is probably located more on the surface of the forest floor (Emmons 2000). Therefore, with regard to our findings, orientated movement and foraging of these species may take place in different microhabitats and utilization of resource patches and interpatch movement may be independent of each other.
If rain forest mammals partition resources along the vertical axis, the finding that closely related species share a similar habitat is of much interest. The described patterns demonstrate that many factors determine assemblage structure and resource partitioning, where morphological characteristics are as important as further unknown factors, such as possible energetic constraints along the vertical axis. Further, if habitat heterogeneity and scaling effects differ between different strata, we would expect more pronounced effects of vertical habitat partitioning on the overall movement strategy contrary to our results on this single investigated scale of orientated paths.
movement patterns in logged vs. unlogged forest
One reason that species occur in particular sets of habitats is that they are adapted to specific ecological conditions. Therefore, the potential of a species to cope with environmental variability is an important determinant in species distribution from a local to regional scale and throughout its geographical range, particularly in the heterogeneous rain forest environment. We found little evidence that any of the investigated species was restricted to a single set of habitat type and structure. Our comparisons of movement trajectories of small mammals between logged and unlogged forests clearly showed that highly modified forest structures in logged forests affected the movement trajectories of all species. The observed shifts in movement trajectories might result from the altered structure per se, changes in vertical partitioning of resources (e.g. Cunha & Vieira 2002) or differences in spatial orientation and environmental perception by the respective species because of the altered habitat structure (e.g. Grobety & Schenk 1992; Jacobs & Shiflett 1999). Contrary to our expectations, we found no evidence that pathways were adjusted to possible shifts in habitat heterogeneity and variability, as overall movement strategies were found to be similar in logged and unlogged forests. This weak effect of physical habitat differentiation on pathway structures reinforces the conclusion of a rather fixed movement strategy for the examined scale, as we found no differences across species or populations in different forest types.
As the response of individual species to habitat alteration was very variable, the effects of changes in habitat structure on small mammal assemblages are difficult to interpret when only single species are examined. Our results show convincingly that one needs to address the entire set of focal species for a given habitat type to reach a valid conclusion. Some general shifts in habitat use become evident when we consider the most drastic habitat change with regard to disturbance, here the reduction of canopy space and structure caused by the extraction of emergent trees in logged forests. As a consequence, arboreal species and biomass may shift from the canopy to the ground in logged forests (Malcolm 1997; Struhsaker 1997). Furthermore, differences in branch dimension and structure may alter connectivity and thus movement tracks of animals (Malcolm 1995). The predicted shifts in vertical movement patterns in response to habitat differences between understorey and canopy of logged vs. unlogged forest were less evident as we encountered terrestrial and scansorial species in logged forest with denser undergrowth and a higher variety of supportive structures at almost equal proportions. Probably, species might quickly change between two neighbouring habitat layers (here ground vs. understorey supports) and habitat differences such as microclimate between these layers might affect the species less than expected, leading to a continuous gradient in habitat use rather than a strict terrestrial–arboreal dichotomy.
A general difference of movement trajectories between the two habitat types was only found for the diameter of supportive structures, which declined in logged forests. It needs to be noted that this general pattern refers to an overall difference in branch diameters rather than to particular preferences of small mammals for particular supportive structures. There were, for example, fewer large logs or thick arboreal branches in logged forests, whereas the abundance of thin supports increased in the understorey particularly because of the fast growing and highly abundant climbing bamboo with diameters between 1 and 3 cm that is frequently used for climbing by various species of small mammals (pers. obs.). Smaller climbing mammals might profit from thin supports because of less body mass (Lemelin 1999; Cunha & Vieira 2002), although Charles-Dominique et al. (1981) did not find a relationship between the diameter of supports and body sizes in an assemblage of mammals in the neotropics. However, the potential consequences of thinner supports in logged forests for individual species or the entire assemblage remain unclear. For example, L. sabanus, the largest focal species, frequently used thin supports (c. 20% of used supports = 2 cm) and showed increased climbing activity in logged forests, whereas the climbing activity of the much smaller N. cremoriventer was reduced in logged forests, although this species showed in general a clear preference for small diameters (Table 3). This observed variability might not be independent of other features, such as texture or the interconnectivity of supports. No general trend was found for the proportion of movements in dense undergrowth, although all species faced denser undergrowth in logged forests. Only T. tana and L. sabanus moved longer distances in dense undergrowth in logged forests. Diurnal treeshrews might profit from dense ground cover as a strategy for predator avoidance (Emmons 2000) as they generally move greater distances in dense undergrowth than nocturnal rats. Although this strategy has been suggested for several tropical small mammals (e.g. Emmons 2000; Lambert & Adler 2000; Vernes 2003) it needs to be tested with behavioural experiments and with further information with respect to associated structural, abiotic and biotic habitat features. Little is known about such differences between logged and unlogged forests. Studies comparing small mammals in undisturbed forests and tree-fall gaps therein indicate that various factors such as resource availability or protection from predators may differ in their impact on syntopic small mammals and the pay-off for them to move in densely covered gaps (Beck et al. 2004).
The arguments so far led us to the conclusion that any particular habitat change such as structural differences between logged and unlogged forests is closely linked to other habitat variables that might have either synergistic or reciprocal effects on small mammal movement, depending on the specific combination of intrinsic and environmental factors. Therefore, changes in movement trajectories between forest habitats must be analysed in a multivariate approach. Our analysis suggests that specific movement patterns differ between logged and unlogged forest whereby variables related to climbing activity play a dominant role (see Fig. 5). We did not detect any trends in shifts of movement patterns with regard to body size, taxonomic grouping or vertical stratification. Further, no parallel trends were seen in the shift of movement trajectories for congeneric species pairs such as M. rajah and M. surifer or T. longipes and T. tana despite their strong convergence in morphology and habitat use.
These results highlight the importance of qualitative habitat alterations and their impact on small forest-dwelling mammals. Fortunately, most of the common species such as those in our study were able to persist in logged forest habitats. However, preliminary data from our study as well as other studies suggest that more specialized species that are rare in logged forest react negatively to environmental variability (e.g. Henein, Wegner & Merriam 1998; Purvis et al. 2000; Wells, pers. obs.). The results presented here are preliminary in that neither the ultimate reasons for changes in movement trajectories nor the consequences for foraging success, individual survival and population establishment can be given because of the lack of knowledge regarding the ecology of the species, in particular the rarer ones. However, first data on how species react in their movement patterns to habitat disturbance provide a promising approach for a better understanding of interspecific variation in adaptability to altered ecological conditions, determining decline or persistence of tropical rain forest mammals in local assemblages. The observed inconsistency in the species’ responses to logging cautions the approach to extrapolate results obtained from a few species to a whole assemblage, underlining the importance of species-based approaches in understanding the effects of habitat degradation on speciose assemblages.