Elephant (Loxodonta africana) footprints as habitat for aquatic macroinvertebrate communities in Kibale National Park, south-west Uganda

Introduction

East Africa exhibits one of the largest and most outstanding concentrations of mammals (Gordon & Barbero, 2008). Kibale National Park, located in western Uganda, has several different biotopes, enabling high concentrations of various of these mammals, such as primates, carnivores, ungulates and elephants (Wanyama et al., 2009).

The African elephant is one of the most extraordinary animals in that region (Clarke & Bertin, 1989; Kingdom, 1989). Despite being very attractive and thrilling to tourists (Naughton, Rose & Treves, 1999; Briggs & Roberts, 2010), elephant damage to crops has led to ‘animosity, fear and detest’ among those sharing their lands with them (Naughton, Rose & Treves, 1999). Ivory poaching, which has become a large-scale illegal industry in a number of African countries, has been recognized as the main threat to elephant preservation in Africa (Clarke & Bertin, 1989; Kingdom, 1989; Naughton, Rose & Treves, 1999; Chiyo & Cochrane, 2005; Chiyo et al., 2005).

Elephants are large-scale ecosystem engineers and considered as major sediment disturbers (see Haynes, 2012 and references therein). They also play a role in the dispersal of tree seeds (Cochrane, 2003; Babweteera & Brown, 2010) and in the creation and maintenance of forest gaps (Struhsaker, Lwanga & Kasenene, 1996; Paul et al., 2004; Zanne & Chapman, 2005). Vanschoenwinkel et al. (2011) recently found out that elephants are effective vectors for the dispersal of aquatic organisms. These notwithstanding, the ecological importance of elephants as ecosystem engineers in Africa's different landscapes is not yet fully understood.

Additionally, elephants create water-filled footprints which can act as temporary habitats for aquatic macroinvertebrates. In this work, we accessed the aquatic diversity in such habitats, a matter that has not been subject to scientific studies so far, although elephant footprints have been mentioned as breeding habitats for mosquito larvae (e.g. Dutta et al., 2010). To understand the ecology of these footprints, we studied the natural diversity of their invertebrate inhabitants and the influence of ecological factors on their community composition. We believe both abiotic, such as age of the footprint or percentage of sunlit water surface, and biotic factors, such as predator/prey interactions, may influence the aquatic macroinvertebrate diversity and composition. To assess the initial colonization process of newly formed ponds, we created artificial footprints. We hypothesized that distance from the nearest water source and the surrounding habitat affects the colonization process of these ephemeral waterbodies.

Methods

Study area

Kibale National Park, with an area of 766 km², is located in south-west Uganda and consists of a medium altitude (1110-1590 m), tropical rainforest interspersed with swamp areas, grassland, degraded and regenerating forests (Chiyo & Cochrane, 2005; Chiyo et al., 2005). This study was carried out near Makerere University Biological Field Station (MUBFS) along the western swamp trail (Fig. 1). Due to a steep terrain in the area, most habitats have flowing water, although it might be a mere trickle through a swamp. True stagnant pools and puddles are rare and usually the result of activities of large mammals.

Results

Natural footprints

A total of 2751 specimens taken from 30 natural footprints were collected. The 61 detected taxa were assigned to 27 families or orders. The most diverse families were Hydrophilidae (13 taxa) and Dytiscidae (9 taxa), whereas the highest abundances were found in Culicidae (1044), Dytiscidae (641), Hydrophilidae (495) and Chironomidae (187). A detailed table of taxa is provided in the (Table S1).

The results of the abiotic factors are summarized in the (Table S2). Whilst the bulk CPOM was made up of dead tree leaves, in some old footprints, living amphibious vegetation was abundantly growing into the water from the outside.

The CCA (Fig. 2) suggests that all ecological factors assessed here might have an influence on community composition and species occurrence in elephant footprints. The analysis shows that age and organic matter, which are strongly correlated (r = 0.84, r²=0.71), are important variables in the colonization patterns of numerous footprints. Most species exhibit a positive correlation with age and CPOM content. Another cluster of footprints and species is positively correlated to substrate and conductivity of the water. Volume does not show a strong gradient, but some species are positively correlated to high volume. Additionally, communities of some footprints might be influenced by low canopy cover.

When comparing footprints by their age in terms of α-diversity (measured by the Shannon index H), old footprints show the highest values and footprints of medium age show the lowest (anova: F = 5.26, P = 0.01182) (Fig. 3). Old footprints have an α-diversity significantly higher than medium-aged footprints (Tukey′s HSD, P = 0.011). No significant differences occur between old and young and between young and medium footprints (Tukey′s HSD, P = 0.171 and P = 0.85, respectively).

Old footprints have the highest species richness, followed by the young and medium footprints, although no significant differences were found (anova: F = 2.09, P = 0.14). On the other hand, medium-aged footprints show higher total number of individuals, again with no significant differences (anova: F = 0.965, P = 0.36) (Fig. 3).

The ANOSIM revealed differences in community composition between the age classes young and old (R = 0.36, P < 0.05) and between medium and old footprints (R = 043, P < 0.01). No differences were found between age classes young and medium (R = -0.07, P = 1) (Bonferroni-corrected P-values).

The Pearson correlation coefficient of -0.18 suggests a very weak negative relationship between predator and prey abundance (Fig. 4). The coefficient of determination (r²) of 0.0324 shows that 3.24% of the data points are explained by the model. According to the general linear model, the prey abundance is not significantly correlated with the number of predators in a footprint (F = 0.9, P = 0.35).

Artificial footprints

A total of 410 specimens assigned to 21 different taxa and morphospecies (10 families) were sampled in the artificial footprints. A detailed table of taxa is provided in the (Table S1). Abiotic factors are summarized in the (Table S2).

Diversity (measured by the Shannon index H) was significantly higher in footprints in B distance than in C distance (Tukey′s HSD: P = 0.04). No significant differences occurred between A and B as well as A and C distances (Tukey′s HSD: P = 0.35 and 0.42, respectively). The number of taxa (species richness) was significantly higher in A and B distances than in C distances (Tukey's HSD: P = 0.011 and 0.011, respectively), whereas no significant difference occurred between A and B distances (Tukey's HSD: P = 1). The absolute abundance of footprints in A distance seems to be higher than in B distance, although not statistically significant. Statistically significant differences in abundance occur between distances A and C (Tukey's HSD: P = 0.008) (Fig. 5).

We used Jaccard similarity coefficient to assess the β-diversity between sites in different distances to the stream. Similarity between footprints at sites A and B, A and C, and B and C was 0.33, 0.45 and 0.25, respectively. The analysis of similarities could not detect any differences in community composition between groups of footprints in different distances (ANOSIM: R = 0.05, P = 0.28).

The Bray–Curtis dissimilarity dendrogram (Fig. 6) shows a low overall similarity of communities in natural as well as in artificial footprints. A separation of natural and artificial footprint communities is evident (ANOSIM: R = 0.46, P < 0.01). Furthermore, it reveals a tendency of artificial footprint communities to be increasingly similar to natural footprint communities with decreasing distance to the stream.

Discussion

Here, we most likely present the first study of elephant footprints as habitats for aquatic invertebrates. This is a preliminary study conducted with a limited sample size over a short time period. Nevertheless, the results are noticeable and should eventually be taken up in a larger study design.

The elephant footprints create suitable habitats for over 62 taxa from various aquatic groups, ranging from mosquito larvae to tadpoles. To truly assess the composition of such communities, a full identification of organisms would be necessary. As many of the tropical macroinvertebrates are yet unknown to science (Godfray, Lewis & Memmott, 1999), the need for taxonomical studies is hereby advocated. Nevertheless, the allocation to morphospecies allows a description of the invertebrate communities based on diversity indices that reveal a high species richness and some degree of variability between footprint communities in relation to the environmental factors sampled. It should be noted that the actual species richness is surely higher than recorded here because of omitting organisms below 2 mm body size due to the sampling method.

As far as natural footprints are concerned, we can see that there are several environmental factors that may affect the species composition of an elephant footprint. The CPOM content of footprints has a positive correlation with age, as leaves are trapped and plants grow in them over time. These two factors seem to influence a rather large group of organisms and are probably key factors in the forming of distinctive communities in old footprints. Tadpoles should receive special attention here because, although not being part of the invertebrate community, they also benefit from ‘ponds’ created by elephants, but were only present in old footprints. Tadpoles do function as food for larger invertebrates, such as coleopteran or dragonfly larvae. The latter were found in several footprints, with larvae from the Libellulidae found in footprints of all age classes, whilst larvae of Coenagrionidae were only found in older footprints, as they need submerged vegetation for oviposition. These findings suggest that there is a succession in the species composition of a footprint over time and that these footprints may also play important long-term roles in several aquatic species, such as frogs. The CCA suggests that conductivity and substrate also affect the species composition of these habitats, although these factors cannot be separated here and their actual significance in this context remains rather obscure. In general, hardness of the bottom substrate of a pond can influence the type of organisms present; for instance, the capacity to burrow eggs or to hide from predators may change with this factor (McCafferty, 1998). Consequently, species composition of a footprint may change according to substrate properties. Conductivity of the water varied greatly among the footprints sampled, even within footprints of the same cluster (from 55 to 949 μS cm⁻¹). We infer that the deposit of elephant excretions in the footprints may be the cause for such differences. Presence of more or less ions in the water may, again, favour different types of organisms, such as Culicidae larvae (Rychla, Benndorf & Buczyński, 2011). Other variables seem to have a lesser influence on their own. Nevertheless, they seem to interact with each other in shaping the species composition of the footprints and should be taken into account in further studies.

According to Macarthur & Wilson (1967), we would expect that distance to the nearest water source, that is the source of aquatic organisms, would play a major role in defining aquatic macroinvertebrate communities. However, most of the footprints are grouped in clusters/tracks and could act as stepping stones of dispersion among all other surrounding footprints. Time also seems to be a crucial factor for the establishment of species within a footprint as we could observe a succession in the species composition dependent on the footprint's age.

Although not significant in most cases, the comparison of natural footprints diversity measurements according to their age (Figure 3) suggests that old footprints embrace more species and show higher levels of α-diversity, whilst holding a smaller number of individuals. Younger footprints are still in the initial stage of colonization and have been accessible for dispersers for a shorter time period. If a footprint is colonized by r-strategists which lay many eggs in the absence of predators, the number of individuals can be much higher (although being represented by few species). In time, species composition will change and biotic interactions will intensify due to higher degrees of competition and predation (Townsend, 1991). This is underlined by our observation that species diversity and number of predators such as dragonfly larvae increased with age of the footprints, whilst the number of individuals decreased. A general change of communities with increasing age is shown by ANOSIM. Comparison of species richness and number of individuals, however, reveals no significant differences. The succession of footprint communities should be subject to further studies.

Besides abiotic factors such as the ones we sampled, biotic factors such as predator–prey interactions are equally crucial in defining communities of small water bodies (Fincke, Yanoviak & Hanschu, 1997; Urban, 2007; Chase, Burgett & Biro, 2010). Although we did not take predator–prey interactions into consideration when designing the methodology, we observed the tendency that the presence of predators has a negative effect on prey abundance (Figure 5). This may also be a result of ageing (i.e. duration) of the pond, as suggested by Schneider & Frost (1996), in their study about habitat duration and community structure. A closer and more specific look into biotic factors such as predator–prey interactions would foster our understanding of the community dynamics and colonization process.

We hypothesized that distance to the stream can affect the colonization process. In our artificial footprint experiment, we tried to control every other ecological variable to see how the colonization process is influenced by the distance to the nearest source of aquatic organisms.

The colonization progressed unexpectedly fast. On the first day, we already registered water beetles inhabiting several footprints and occasionally spider webs that covered parts of the surface. After five days, the 18 footprints were inhabited by 410 individuals. One trigger for the fast colonization of new footprints, whether man or elephant made may be the absence of predators. Key predators in the elephant footprints are dragonfly larvae from the Libellulidae family. Adult male dragonflies (Hadrothemis coacta, Palpopleura portia and Tetrathemis camerunensis) have been frequently observed to hold a water-filled footprint as a territory. Also the artificial footprints were quickly found by dragonflies and occupied as territories. Being strong predators to other invertebrates and also to their own relatives, there is a struggle to place eggs as the first ‘top predator’ in a waterbody (Clausnitzer & Lindeboom, 2002; Suhling, Martens & Marais, 2009).

According to Macarthur & Wilson (1967), we compared α-diversity among three sets of distances. We expected that the closer the footprint is to the water source, the higher the diversity. Although we could indeed observe a significantly higher number of species in the footprints nearer to the stream (A and B distances), we found that diversity was highest in the intermediate distances, which contradicts our predictions. Jaccard similarity coefficient also shows that there were bigger differences in species composition between footprints of sites B and C than between sites A and C. We may infer that these results are explained by a low number of replicates in our study. It should be taken into account that, due to the short time span of exposure, the colonization events which occur by chance could have a high influence on species composition. Nevertheless, we can still see a trend towards our predictions as the diversity, species richness and abundance in C footprints were lowest. This trend is also supported by the Bray–Curtis dissimilarity which shows that the communities of the artificial footprints that are closer to the stream tend to be more similar to natural footprint communities than the artificial footprints in greater distance to the open water course.

Conclusively, we could show that elephant footprints play an important role as habitats for aquatic communities. We recommend repeating this study with more replicates over a longer period of time, also considering oxygen levels (Osborne et al., 2001) and biotic interactions in food webs (Urban, 2007; Chase, Burgett & Biro, 2010). Considering a wider range of habitats as well as replicating, this study during wet seasons might reveal totally different communities (Godfray, Lewis & Memmott, 1999).

The elephant has already been proven to have several functions in tropical rainforests. Besides being a seed disperser, maintaining the landscape heterogeneity by creating gaps and being crucial in nutrient cycling, we are now closer to perceive yet another role for this ecosystem engineer. The fast colonization process highlights the suitability of the footprints as stepping stone habitats for the dispersal of aquatic macroinvertebrates over larger distances. This function might be especially pronounced in the rainy season, when water-filled footprints are certainly more numerous especially on higher terrain outside the swampy areas. Without elephants, the number of small and stagnant water bodies, forming a network through the Kibale Forest, would be next to zero. The steep relief in most parts of the area results in streams and muddy parts with some water currents largely preventing the formation of stagnant pools. This fact strongly suggests that the aquatic macroinvertebrate fauna depends on water-filled footprints as habitat and as a refuge during dry periods. In forest conservation practice, the elephant should be considered as an important ecosystem engineer, creating habitats for numerous aquatic species, especially from the insect class.