Spillover of organisms from rainforests affects local diversity of land-snail communities in the Akagera savanna in Rwanda

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Spillover of organisms from rainforests affects local diversity of land-snail communities in the Akagera savanna in Rwanda Torsten Wronskia, Prosper Umuntunundib, Ann Apioc, Bernhard Hausdorfd,∗ a

School of Natural Sciences and Psychology, Faculty of Science, Liverpool John Moores University, James Parsons Building, Byrom Street, Liverpool, L3 3AF, UK Faculty of Science, Department of Biology, Mabarara University of Science and Technology, P.O. Box 1410, Mbarara, Uganda c College of Agriculture, Animal Sciences and Veterinary Medicine, Department of Wildlife and Aquatic Management, University of Rwanda, PO Box 57, Nyagatare, Rwanda d Zoological Museum, Center of Natural History, Universität Hamburg, Martin-Luther-King-Platz 3, 20146, Hamburg, Germany b

A R T I C LE I N FO

A B S T R A C T

Keywords: East Africa Ecotone Gastropoda Metacommunity

We investigated how local and landscape variables influence the structure and richness of land-snail communities in a savanna ecosystem. The land-snail species richness in the Akagera savanna in Rwanda is smaller than in nearby rainforests. Generalized linear models indicated that the diversity of land-snail communities in the savanna is most strongly affected by a landscape variable, the distance from the escarpment where remnants of the former rainforests persist. The number and abundance of rare species decline more strongly with increasing distance from the escarpment than that of the frequent species that are supposedly better adapted to the drier habitats in the savanna. Actually, the number and abundance of rare species are also more strongly dependent on precipitation and the distance from the next stream than that of the frequent species. This indicates that the snail fauna of the Akagera savanna represents a metacommunity that depends on the spillover of immigrants from the richer fauna of the adjacent rainforests. Streams are probably the most important pathways for dispersal of landsnails. Given the low dispersal abilities of land-snails the spatial scale of the influence of the rainforests on the savanna is surprising.

1. Introduction In East-central Africa, rainforests extend from the Albertine Rift Valley eastwards. With increasing aridity they are replaced by evergreen and semi-evergreen bushland and thicket (Kindt et al., 2014), which cover large parts of eastern Rwanda, southwestern Uganda and adjacent parts of Tanzania. The distribution of the vegetation types is dynamic. During Pleistocene glacials the forests were restricted to refugia along the Albertine Rift (Hamilton, 1976; Grubb, 2001; Maley, 2001). The postglacial climate change resulted in an expansion of the rainforests eastwards. How this dynamic influences the structure and diversity of local animal and plant communities is still poorly understood. In previous studies (Wronski and Hausdorf, 2008; Boxnick et al., 2015), we could show that the richness and the structure of land-snail communities in the rainforests of the Albertine Rift reflect this dynamic. The species richness of the rainforests is decreasing eastwards with increasing distance from putative East Congolian forest refugia. The ranges of species are significantly clustered and nested and range size

∗

increases with increasing distance from the refugia. However, it remains unknown how the diversity and structure of communities changes across the ecotone from rainforest to savanna. Because it was estimated that about 83% of the land-snail fauna in East Africa is restricted to evergreen forests (Verdcourt, 1972), landsnail surveys of the two past decades have predominantly focussed on the evergreen forest remnants (Tattersfield, 1996, 1998; Emberton et al., 1997; Tattersfield et al., 2001, 2006; Warui et al., 2001; Seddon et al., 2005; Wronski and Hausdorf, 2008, 2010; Boxnick et al., 2015; Wronski et al., 2016). However, these studies are informative for only a small part of the region. Evergreen forests currently cover only around 6% of the terrestrial surface in East Africa and their area is still decreasing (Pfeifer et al., 2012). By contrast, the land-snail communities in the savannas of Africa remained almost unexplored. van Bruggen (1978) and Fontaine et al. (2007) described the land-snail fauna of savanna in southern and western Africa as poor. van Bruggen (1978) stated that the savanna fauna includes mainly ecologically tolerant forest taxa or species derived from forest taxa, and Fontaine et al. (2007) found no land-snail fauna that is specific to savanna habitats.

Corresponding author. E-mail address: [email protected] (B. Hausdorf).

https://doi.org/10.1016/j.jaridenv.2018.09.002 Received 23 February 2018; Received in revised form 26 July 2018; Accepted 3 September 2018 0140-1963/ © 2018 Elsevier Ltd. All rights reserved.

Please cite this article as: Wronski, T., Journal of Arid Environments, https://doi.org/10.1016/j.jaridenv.2018.09.002

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explaining these patterns. 2. Methods 2.1. Sampling We investigated the land-snail fauna in 102 plots, each 20 × 20 m, along two transect belts (2.5 × 42.5 km) across the Akagera savanna in Rwanda (Fig. 1; Supplementary Data Table S1). All plots include at least some natural savanna vegetation with indigenous thickets or trees. The transects were positioned so that they run through four (northern transect) or five (southern transect) different zones of conservationpolitical history reaching from the international border with Tanzania or the wetlands inside the current Akagera National Park in the east to the international border with Uganda or the Byumba Escarpment in the west. The northern transect crosses the gallery forest along the lower course of the Muvumba River, whereas there is no forest close to the southern transect. The two transects allowed to look for regional differences within the Akagera savanna. The geographic coordinates of the plots were determined using a GPS. Sampling plots were located within 34 quadrants (each measuring 2.5 × 2.5 km) along the two transect belts across the Akagera savanna. All living slugs and snails as well as their empty shells were collected from the vegetation and the ground for one person-hour at each plot. Additionally, samples from the woody vegetation (shrubs and young trees) and litter samples were taken at each plot. Understorey vegetation was beaten over plastic sheets and falling leaves, twigs and fine material were bagged. About 5 l of leaf litter and surface soil were also sampled into plastic bags. Samples from woody vegetation and the litter samples were sun-dried, fractioned by sieving and sorted. All individuals were counted. Most specimens were found in the dried litter and soil samples. It is difficult to distinguish specimens that died during the sampling, drying and sorting of the samples from fresh shells. It is unlikely that counting all individuals caused a bias affecting the results because the soil is acidic (pH 5.7–6.7, mean 6.0) so that empty shells dissolve and do not accumulate over longer periods. The material is kept in the Zoological Museum at the University of Hamburg, Germany.

Fig. 1. Location of the 102 surveyed plots (black dots) along two transect belts in the Akagera savanna in northeastern Rwanda. The gallery forest along the lower Muvumba River is indicated in green. Along the Rwanda-Uganda border only fragments of the gallery forest remained. Dotted lines, current and former borders of the Akagera National Park and the Mutara Game Reserve. Darker shades of grey indicate increasing altitude. Insert shows the location of the study area in Africa. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

However, it remains unknown whether this is generally true. Thus, quantitative surveys of land-snail faunas in savanna habitats are urgently needed. Without knowledge of the diversity of land-snail communities in savannas and the factors determining it, the effects of the increasing human impact on savanna ecosystems and the land-snail fauna herein cannot be evaluated. We conducted a first quantitative study of the land-snail communities in an East African savanna ecosystem. We studied the Akagera savanna in the Nyagatare District of northeastern Rwanda (Fig. 1), of which the area west of the Akagera National Park is often referred to as the Mutara rangelands. The Akagera savanna extends into the Ankole grasslands in southwestern Uganda and the Kagera Region in Tanzania. The woody vegetation is dominated by Senegalia senegal, Senegalia polycantha, and Combretum species, while grasslands are mostly composed of gramineous species such as Bracharia sp., Hyparrhenia filipendula and Sporobolus pyramidalis (Vande weghe 1990). The Akagera savanna in Rwanda can be divided into zones of different conservationpolitical history. The westernmost part of the Akagera savanna, west of the Muvumba River, comprising open grasslands and savanna, which are predominantly used for grazing cattle, was never protected. In 1934 large parts of the Akagera savanna east of the Muvumba River were protected as Mutara Game Reserve and Akagera National Park (Vande weghe 1990). Between 1973 and 1990 the western parts of the Mutara Game Reserve (Fig. 1) were opened for development projects, livestock breeding and the army (Vande weghe 1990). Following the civil war and genocide (1991–1995), the remaining Mutara Game Reserve and the western half of Akagera National Park were also degazetted, reducing the protected area from an initial surface area of 2,800 km2 to about 1,120 km2 (Williams and Ntayombya 1999, 2001; Vande weghe and Vande weghe, 2011). Occurrence and abundance patterns of species may be affected by local as well as landscape variables (Blevins and With, 2011; Turner and Gardner, 2015; Mendes et al., 2017). We studied species richness and abundance patterns of the land-snail communities in the Akagera savanna near the ecotone between rainforest and savanna and investigated the relative importance of local versus landscape variables in

2.2. Species identification The sampled specimens were sorted into morphospecies, classified into genera and subsequently compared with all species of the respective genus known from Rwanda or neighbouring countries, mainly based on compilations by Pilsbry (1919) and Verdcourt (2006). Identifications were based on original descriptions or, if available, on revisions (see Boxnick et al., 2015). 2.3. Estimates of species richness and Shannon diversity For comparisons between the Akagera savanna and forests along the Albertine Rift and the adjacent Lake Victoria forest belt (data from Wronski and Hausdorf, 2008, 2010; Boxnick et al., 2015; Wronski et al., 2016; Umuntunundi et al., 2017), we used the iChao1 estimator (Chao and Chiu, 2016) for species richness (more accurately a lower bound for species richness) and the estimator for Shannon entropy/diversity proposed by Chao et al. (2013). Both estimators were calculated using SpadeR Online (Chao et al., 2015). 2.4. Local and landscape variables putatively affecting species richness and abundance As potential local determinants of species richness and abundance we recorded the depth of leaf litter, the soil pH and annual precipitation. The depth of leaf litter was measured five times in each sampling plot. The pH of the uppermost soil layer at each plot was acquired from the SoilGrids250m map (http://www.isric.org/content/soilgrids; Hengl 2

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Table 1 Comparison of land-snail species diversities and abundances in the Akagera savanna with the gallery forest along the Muvumba and the investigated forests in the Lake Victoria forest belt (Mpanga and Mabira) and the northern Albertine Rift (remaining forests). Area

Forest area (km2)

Mean elevation (m)

Number of plots

Number of species

Median number of species per plot

Median number of individuals per plot

Estimated species richness

Estimated Shannon diversity

Akagera savanna Muvumbaa Nyungweb Mgahingac Echuyac Bwindic Kalinzuc Kasyoha-Kitumic Maramagamboc

7 970 34 35 321 137 390 443

1391 1339 2253 2570 2295 1870 1428 1256 988

102 24 50 6 4 5 5 5 4

45 34 102 57 57 66 56 46 44

7 14 14 21 27 13 29 29 23

87.5 411.5 55 171.5 157.5 50 203 228 378.5

45.5 36.0 107.7 65.4 68.4 69.6 60.0 49.6 56.3

11.7 14.1 42.1 25.2 25.9 35.9 25.7 21.3 20.9

Kibalec Rwenzorid Semlikic Matiric Bugomac Budongoc Mpangac Mabirac

558 1500 220 54 401 825 5 300

1330 2345 687 1285 1073 1108 1214 1260

5 40 3 4 4 5 5 5

68 91 45 33 54 60 40 44

36 10 26 16.5 32 31 19 24

485 40.5 296 207 345 299 155 235

77.3 100.9 54.7 36.1 58.4 71.6 47.9 75.4

25.9 23.4 22.5 9.9 24.6 22.4 16.1 16.8

a b c d

Data from Umuntunundi et al. (2017). Data from Boxnick et al. (2015). Data from Wronski and Hausdorf (2008, 2010). Data from Wronski et al. (2016).

was computed with the function envfit. Significance of the fit was tested based on 9999 permutations.

et al., 2017) and the annual precipitation was obtained from the WorldClim database (http://www.worldclim.org; c. 1 km2 resolution; Hijmans et al., 2005). As landscape variables, the nearest distances of each plot to the Byumba escarpment, representing the former natural boundary between rainforest and savanna (Vande weghe 1990; Kindt et al., 2014), to the next stream and to the gallery forest along the lower course of the Muvumba River were established. Additionally, the proportion of fields (grassland transformed to subsistence agriculture) and the elevational range in the surroundings of the plots were determined. The distances to the Byumba escarpment, to the next stream and to the gallery forest at the Muvumba River were measured using Google Earth. As a measure of habitat degradation and destruction, the proportion of fields in each quadrant (2.5 × 2.5 km; see above) was used. We determined the proportion of fields by walking along a 3.5 km transect line in each quadrant and measuring the length walked either in fields or in seminatural grassland. The minimum and maximum elevation in the surrounding of each plot within a radius of 5 km were determined using ArcGis (ESRI, Redlands). The difference between minimum and maximum elevation was used as a measure for the relief in the surrounding of the plots. The values of all mentioned variables are listed in Supplementary Data Table S1. We analysed the influence of these putative explanatory variables on species richness and abundance in the plots using generalized linear models, which were calculated with the function glm of the ‘stats’ package for R (R Core Team, 2016). To correct for over-dispersion, we used a Quasipoisson error structure. The final model was constructed manually by removing all non-significant terms starting from a model including linear terms of all variables.

3. Results 3.1. Species richness and composition of the land snail fauna of the Akagera savanna In total, 14,005 land-snails were collected in 102 plots located across the Akagera savanna (Fig. 1) and assigned to 45 species (Supplementary Data Table S2). The number of individuals per plot varied between 1 and 1018 (median 87.5). Species richness per plot ranged from 1 to 16 (median 7). The most species-rich families were Achatinidae (including subulinids) (8 species), Streptaxidae (8 species) and Urocyclidae (4 species), representing 44% of all recorded species. Thirty-one (69%) of the species were previously collected in Ugandan rainforest reserves (Wronski and Hausdorf, 2008, 2010; Wronski et al., 2016) and 11 (24%) in the Nyungwe Forest National Park in Rwanda (Boxnick et al., 2015). Twenty-two (49%) of the species were found in the gallery forests along the Muvumba River in the Akagera savanna (Umuntunundi et al., 2017). Thirteen (29%) of the species found in the Akagera savanna were not recorded in the rainforests of Rwanda or Uganda surveyed by Wronski and Hausdorf (2008, 2010), Boxnick et al. (2015) and Wronski et al. (2016). Some of those might be especially adapted to savanna vegetation. The species that are most characteristic for the savanna were Nothapalinus kempi (Preston, 1912), which was with 4976 sampled specimens the most abundant species overall, and Streptostele babaulti Germain, 1919, of which 726 specimens were recorded in total, each from 70 of the 102 plots. Gittenedouardia cf. prestoni (Connolly, 1925), Gastrocopta klunzingeri (Jickeli, 1873) and Halolimnohelix eulotaeformis (Preston, 1914) were also present in more than 10% of the plots and were not recorded in the rainforest surveys. The estimated land-snail species richness of the Akagera savanna is lower than that of any of the investigated rainforests in the Albertine Rift except Matiri forest, but higher than that of the gallery forest along the Muvumba River in the Akagera savanna (Table 1). The Shannon diversity of the Akagera savanna is also lower than that of any of the investigated rainforests in the Albertine Rift except Matiri forest. It is even lower than that of the gallery forest along the Muvumba River in the Akagera savanna (Table 1). This means that only a few very

2.5. Environmental variables putatively affecting community composition We assessed the importance of the environmental variables for determining the distribution of species and the composition of assemblages by fitting them onto an ordination plot using the ‘vegan’ package (Oksanen et al., 2017) for R (R Core Team, 2016). The ecological similarities between species and between assemblages were explored by a nonmetric multidimensional scaling (NMDS) of quantitative Kulczýnski distances (Faith et al., 1987) between the abundance data, using the function metaMDS. The goodness of fit of the environmental variables 3

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increasing distance from the Byumba escarpment up to a distance of c. 30 km. Between 30 and 40 km the species number increased in both transects, but decreased again in the zone around 40 km east of the Byumba escarpment in the Akagera National Park. For a better understanding of the processes determining species richness and abundance in the Akagera savanna, we distinguished frequent and rare species. Species found in about 10% or more of the sampled plots (10 or more) were classified as frequent; all other species as rare (see Supplementary Data Table S2). Twenty-seven (= 60%) of the recorded 45 species were rare. The richness of both groups is most strongly correlated with the distance from the Byumba escarpment (Table 2). However, the number of rare species decreased with increasing distance from the escarpment more strongly than the number of frequent species. The second most important predictor for richness of rare species was the distance from the next stream. This variable did not significantly affect the richness of the frequent species. The richness of both frequent and rare species significantly increased with annual precipitation, but the number of rare species decreased more strongly with decreasing precipitation than the number of frequent species. In addition, the number of frequent species slightly decreased with increasing relief in the surroundings of the plots. The variables determining abundance differ even more strongly between frequent and rare species (Table 2). The abundance of frequent species increased significantly with the depth of leaf litter and with decreasing distance from the gallery forest along the Muvumba River. Both variables had no significant effect on the abundance of rare species. Just as the richness, the abundance of rare species decreased most strongly with increasing distance from the Byumba escarpment. Furthermore, it increased with increasing proportion of fields and with increasing precipitation and decreased with increasing distance from the next stream and increasing relief in the surroundings of the plots. Since the dispersal capacity of land snails depends on body size, we also distinguished small (major shell dimension ≤ 5 mm) and large species (major shell dimension > 5 mm). The two recorded slug species were not considered in these analyses. The number of small species decreased most strongly with increasing distance from the Byumba escarpment, whereas the number of larger species decreased significantly, but less strongly with increasing distance from the gallery forest along the Muvumba River (Table 2). The same trends hold also for the abundances of small and large species, respectively. We analysed the data from the two transects separately to check for regional differences within the Akagera savanna (Table 3). The results of the modelling based on the two transects differ from each other and from those based on the complete dataset. The variable that has the most consistent influence on the species richness and abundance in the northern transect is the distance from the gallery forest at the Muvumba River. The number and abundance of all species as well those of the frequent species decrease with increasing distance from the gallery forest at the Muvumba River. Moreover, total species richness and the number and abundance of rare species increase with increasing annual precipitation. In contrast, distance from the Byumba escarpment is the most important variable in the southern transect. The numbers of all species, of frequent species and of rare species decrease with increasing distance from the Byumba escarpment. Whereas abundance of the rare species decreases also with increasing distance from the Byumba escarpment, total abundance and abundance of the frequent species increase with increasing distance from the Byumba escarpment.

abundant species are dominant in the snail assemblages of the Akagera savanna. There were minor differences in the sampling strategy between the compared studies. Whereas the plots in forests were sampled for two person-hours (Wronski and Hausdorf, 2008, 2010; Boxnick et al., 2015; Wronski et al., 2016), the plots in the gallery forest along the Muvumba River (Umuntunundi et al., 2017) and in the Akagera savanna were sampled for only one person-hour. Instead, the understorey was sampled by beating branches of young trees and shrubs in the gallery forest along the Muvumba River and in the Akagera savanna, a sampling method that was not applied in the mature forests with little understorey. In all studies, the vast large majority of individuals and species were acquired from standardized 5 l soil and litter samples. Thus, the differences between the diversity estimates in the savanna, gallery forest and mature forests can hardly be ascribed to the minor differences in the sampling strategy. 3.2. Environmental variables putatively affecting species richness and abundance Habitat destruction as measured by the proportion of fields varied between different zones of conservation-political history. A regression considering all plots showed that habitat destruction was not significantly lower in the western part of the former Mutara Game Reserve (Fig. 1) that was opened for development projects, livestock breeding and the army between 1973 and 1990 than in the area that was never protected (p = 0.072). By contrast, habitat destruction was significantly lower in the eastern part of the former Mutara Game Reserve (p = 0.004), in the part of the Akagera National Park degazetted in 1997 (p < 0.001) and in the current Akagera National Park (p < 0.001). Habitat destruction was not included in the final generalized linear models describing the relationships between land-snail species richness and the recorded environmental variables. If only the northern transect is considered, the proportion of fields was lower in the part of the Akagera National Park degazetted in 1997 (p < 0.001) than in the area that was never protected, but there were no significant differences between the latter zone and the two zones of the former Mutara Game Reserve. In the southern transect the differences between different zones of conservation-political history correspond to those considering the whole dataset. A regression of soil pH against the distance from the escarpment considering all plots did not reveal a relationship (p = 0.447). Soil pH was also not included in the final generalized linear models describing the relationships between land-snail species richness and abundance and the recorded environmental variables. If the two transects are analysed separately, two different relationships between pH and the distance from the escarpment emerged. In the northern transect pH decreased significantly with increasing distance from the escarpment (p < 0.001), whereas it increased in the southern transect (p < 0.001). The modelling approach based on the complete dataset indicated that species richness in the Akagera savanna strongly decreases with increasing distance from the Byumba escarpment (Table 2). Furthermore, species richness increased with annual precipitation and with decreasing distance from the next stream and slightly decreased with higher relief in the surroundings of the plots. The depth of leaf litter had no significant influence on species richness, but was the most significant variable affecting the abundance of land-snails (Table 2). The abundance of land-snails also increased with increasing proportion of fields and decreasing distance from the gallery forest at the Muvumba River. Using another approach to visualize the relationship between species richness and distance from the Byumba escarpment, we also counted the total species numbers in groups of 9–10 neighbouring plots as a function of the distance from the Byumba escarpment in the two transects (Fig. 2). In both transects the species richness decreased with

3.3. Environmental variables putatively affecting community composition In the NMDS, plot 95, at which only a single species was found, turned out to be an outlier. Thus, we excluded this plot from the analyses of community composition. The distance from the Byumba escarpment and the elevational range within 5 km were the only tested environmental variables that significantly affected the community 4

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Table 2 Results of the modelling of the influence of environmental variables on species richness and abundance in the plots in the Akagera savanna (N = 102). Only significant variables are listed. β = estimated regression parameter. Environmental variables

Depth of leaf litter Annual precipitation log(distance from Byumba escarpment) log(distance from next stream) log(distance from Muvumba gallery forest) Proportion fields Elevational range within 5 km

Species richness

Species abundance

Species richness (frequent species)

Species abundance (frequent species)

Species richness (rare species)

Species abundance (rare species)

β

P

β

P

β

P

β

P

β

P

β

P

0.135

0.008

0.141

0.004

0.010 −0.263

< 0.001 < 0.001

0.007 −0.153

0.004 0.009

0.021 −0.626

< 0.001 < 0.001

0.088 −1.422

< 0.001 < 0.001

−0.315

< 0.001

−0.621

0.011

1.999 −0.011

0.037 0.026

−0.076 0.005 −0.254

0.021

0.871

0.014

−0.002 0.001

Environmental variables

Depth of leaf litter Annual precipitation log(distance from Byumba escarpment) log(distance from next stream) log(distance from Muvumba gallery forest) Proportion fields Elevational range within 5 km

−0.286

−0.002

0.006

< 0.001

Species richness (small species)

Species abundance (small species)

Species richness (large species)

Species abundance (large species)

β

β

P

β

P

β

P

0.156

0.040

0.075 0.008

0.002 < 0.001

0.117

0.025

−0.617

0.002

−0.226

< 0.001

−0.353

< 0.001

P

−0.481

< 0.001

0.249

0.001

−0.002

0.003

2010; Boxnick et al., 2015; Wronski et al., 2016). At first sight, the number of 45 recorded land-snail species suggests that species richness in the Akagera savanna is higher than might have been expected. However, the low Shannon diversity indicated that many of the recorded species are rare and that the savanna habitat is dominated by a few abundant species. This already poses the question whether the numerous rare species found in the savanna are represented there by self-maintaining populations.

4.2. Spillover from rainforests affects local diversity in the savanna The analysis of the complete dataset indicated that the richness of land-snail communities in the Akagera savanna is most strongly affected by a landscape variable, i.e. the distance from the Byumba escarpment (Table 2), which marks the natural boundary between rainforest and savanna (Vande weghe 1990; Kindt et al., 2014). Today the Byumba escarpment is largely deforested, but there are still patches of forest at the slopes of the hills which may be sufficient to support relict populations of the rainforest fauna. The decrease of land-snail species richness in the Akagera savanna with increasing distance from the forests at the Byumba escarpment points to a role of these forest populations as sources of immigrants. Land snails disperse mainly passively (Dörge et al., 1999) and their passive dispersal ability decreases with increasing body size (Vagvolgyi, 1976; Hausdorf, 2000; Hausdorf and Hennig, 2003). We found differences in the distribution patterns between small and large size snail species that are in agreement with the hypothesis that dispersal from source areas plays an important role in the distribution of land snail species richness in the Akagera savanna. Both, small and large snails are affected by the distance from potential source areas. The number of small species decreases strongly with increasing distance from the forests at the Byumba escarpment, whereas the number of larger species decreased significantly, but less strongly with increasing distance from the gallery forest along the Muvumba River (Table 2). That the number

Fig. 2. Species numbers in zones (including 9–10 plots) in the Akagera savanna as a function of the distance from the Byumba escarpment in the two transects.

composition (Table 4).

4. Discussion 4.1. Species richness of the savanna in comparison to the rainforests along the Albertine Rift In accordance with the findings of van Bruggen (1978) and Fontaine et al. (2007) in southern and western Africa, the first quantitative survey of the land-snail fauna in the savannas of East Africa confirmed that species richness and Shannon diversity are lower than those of most of the adjacent rainforests (Table 1; Wronski and Hausdorf, 2008, 5

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Table 3 Results of the modelling of the influence of environmental variables on species richness and abundance in the plots in (A) the northern transect (N = 45) and (B) the southern transect (N = 57) through the Akagera savanna. Only significant variables are listed. β = estimated regression parameter. Environmental variables

A Depth of leaf litter Annual precipitation log(distance from next stream) log(distance from Muvumba gallery forest) B Depth of leaf litter pH log(distance from Byumba escarpment) Proportion fields

Species richness

Species abundance

Species richness (frequent species)

Species abundance (frequent species)

Species richness (rare species)

Species abundance (rare species)

β

P

β

P

β

β

P

β

P

β

P

2.850

0.007

2.724

0.009

3.657

< 0.001 2.370

0.023

2.646

0.012

4.058 −4.856

< 0.001 < 0.001

4.043 −3.721

< 0.001 < 0.001

−2.759

0.009

−2.838

0.007

−2.935

0.005

2.039 −8.085

0.046 < 0.001

−3.247

−2.510

0.002

0.015

40.893

< 0.001

6.185

0.016

P

−2.086

−2.074

0.043

0.043

Depth of leaf litter Annual precipitation log(distance from Byumba escarpment) log(distance from next stream) log(distance from Muvumba gallery forest) Proportion fields Elevational range within 5 km

Fit on NMDS R2

P

0.003 0.023 0.063 0.040 0.001 0.045 0.111

0.841 0.353 0.043 0.152 0.935 0.097 0.007

< 0.001

0.040 0.014 0.001

communities in the savanna form a metacommunity (Leibold et al., 2004), the diversity of which is maintained by a mass-effect, i.e. a spillover of immigrants from the adjacent rainforest remnants. In accordance with the cross-habitat spillover hypothesis, the landscapemoderated spillover of organisms across habitats influences landscapewide community structure (Tscharntke et al., 2012). Usually such spillover processes are studied at smaller spatial scales, often between fragments of natural habitats and human-modified landscapes (Blitzer et al., 2012; Estavillo et al., 2013; Schneider et al., 2016). Our study demonstrates that such spillover processes are also important in determining diversity patterns at larger spatial scales across ecotones between adjacent biomes. An alternative or, perhaps, complementary explanation for the increase of species richness towards the escarpment might be the input of minerals, especially calcium, which is essential for snails, from the nearby hills. This would also represent a spillover process. There are no measurements of calcium concentrations from the soils of the Akagera savanna. However, the calcium concentration is usually correlated to the pH. The pH of the soils in the Akagera savanna is not significantly correlated with the distance from the escarpment. Thus, input of calcium from the hills is unlikely to explain the decrease of snail species richness with increasing distance from the escarpment. Moreover, the hypothesis that snail populations in the forest remnants of the Byumba escarpment act as sources that influence the richness of the adjacent savanna is corroborated by separate analyses of frequent and rare species. The frequent species are supposed to be well adapted to the drier conditions in the savanna so that they can survive at many patches. By contrast, the rare species are less well adapted to the dry conditions and may be represented in the savanna mainly by sink populations, which depend on immigration from populations at more favourable sites in the forest remnants in the west. In accordance with this hypothesis, the richness and abundance of the rare species decrease faster with increasing distance from the Byumba escarpment than that of the frequent species. The assumption that the rare species are actually not as dry adapted as the frequent species is corroborated by the much stronger decrease of their richness and abundance with decreasing annual precipitation and with increasing distance from the next stream. However, streams are not only important for providing water, but are also dispersal pathways for land snails (see above). By contrast, the abundance of the frequent species depended only on the depth of the leaf litter and the distance from the gallery forest at the Muvumba River. Leaf litter was also reported to be an important

Table 4 Fit of environmental variables on the NMDS based on quantitative Kulczýnski distances between abundance data of land snail species in 102 surveyed plots in the Akagera savanna in northeastern Rwanda. Environmental variables

20.316

2.107 2.531 −3.401

of small species with better dispersal capacity depended on the distance from the forest remains at the Byumba escarpment that are further away, but supposedly richer than the gallery forest at the lower Muvumba river, whereas the number of larger species depends on the distance from the closer gallery forest, fits the hypothesis that the richness of the habitats in the savanna is affected by the distance from source areas and the richness of such source areas. Whereas most modes of passive transport like dispersal by winds, cattle or birds, that may contribute to the dispersal of land snails across the savanna do not result in directional dispersal, dispersal by streams may result in a directional dispersal away from the escarpment across the savanna (Arter, 1990; Dörge et al., 1999). The generally higher richness of the southern transect compared to the northern transect (Fig. 2), irrespective of the direct distance of the plots from the escarpment, is in accordance with the hypothesis that the NNW running streams represent important pathways for passive transport of snail individuals from the rainforest remnants at the Byumba escarpment to suitable habitat patches in the Akagera savanna. The separate analyses of the two transects through the Akagera savanna indicated that species richness decreased with increasing distance from the Byumba escarpment in the southern transect as in the analysis of the complete dataset, whereas species richness decreased with increasing distance from the gallery forest at the Muvumba River in the northern transect (Table 3). Thus, the separate analyses confirm the strong influence of a landscape variable, namely the distance from nearby forests, on species richness in the savanna. The immigrants disperse into the savanna and either establish new populations or supplement already existing populations. Thus, local 6

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impact on the snail fauna, it would be necessary to quantify the area occupied by favourable patches in the different parts of the Akagera savanna and their connectivity. Snail diversity may not be affected by a decrease of the area suitable for the maintenance of diverse snail communities until the patch size and the connectivity between the patches fall below critical values under which the number of immigrants is no longer large enough to maintain sink populations and to establish new populations with a rate equivalent to the rate with which local populations become extinct in other patches. A more detailed investigation of land-snail communities in the savanna mosaic landscape will be necessary to establish the minimum patch size required for maintaining populations of different land-snail species and the maximum distance allowed between patches to preserve the metapopulation dynamics necessary to maintain a high land-snail diversity. The low diversity of the gallery forest that encompasses the lower course of the Muvumba River (Table 1; Umuntunundi et al., 2017), might be the result of a loss of connectivity to the rainforests at the Byumba escarpment due to deforestation along the upper course of the Muvumba River. Gallery forests may function as corridors for colonization and migration between forest fragments (Verdcourt, 1972; Horáčková et al., 2015) and probably acted as important refugia for tropical forest biotas during arid climatic phases (Meave et al., 1991; Meave and Kellman, 1994). The gallery forest along the lower course of the Muvumba River acts as a source for immigrants, especially of frequent and larger species into the savanna (Table 2), but in the case of the rare species the distance from the gallery forest had no significant impact on the richness or abundance of plots in the adjacent savanna (in addition to the fact that it is the next stream for a part of the plots).

local factor for land-snails in lowland rainforests (Emberton et al., 1997; Wronski et al., 2014), where moisture is not limiting and landsnail species richness depends mainly on the amount of leaf litter that provides shelter and food. Although there is less leaf litter in the savanna compared to forest habitats, it is not the limiting factor for rare species. The limiting variable for these snails in the savanna is rather moisture that constraints foraging and other activities. The abundance of rare species (and all species together) is also positively correlated with the proportion of fields. This correlation is not caused by synanthropic species occurring only in the vicinity of fields, but is probably the result of increased numbers of hygrophilous species persisting e.g. in living fences that separate the fields and reduce wind speed and evaporation. Such habitats may act as refuges as well as corridors for the colonization of suitable habitat patches. In the Akagera savanna both local and landscape variables affect species richness and abundance of local snail communities. However, the general patterns are predominantly determined by landscape variables, especially the distance from the Byumba escarpment and the distance from the gallery forest at the Muvumba River. The inferred metapopulation dynamics help to understand how the forest fauna can disperse stepwise into areas previously occupied by savanna vegetation by an increasing survival of former sink populations when the climate becomes moister. The land snail fauna of the forest remnants at the Byumba escarpment has to be studied in detail to corroborate the hypothesis that these remnants are still rich enough to influence the richness pattern in the adjacent Akagera savanna as indicated by the presented analyses. 4.3. Conservation of savanna diversity demands protection of nearby rainforests remnants

Statement of authorship TW, AA and BH designed the study; PU performed the fieldwork and the sorting of the samples; TW identified the samples; BH analysed the data and drafted the manuscript; all authors contributed to the final version of the manuscript and approved it.

It is also important to understand the metapopulation dynamics for conservation planning. The deforestation of the Byumba escarpment had probably resulted in a loss of source populations. The loss of source populations will also entail a loss of sink populations of the rare hygrophilous species that depend on immigration. Thus, the deforestation of the Byumba escarpment will result (and probably has already resulted) in a reduction of the species richness in the savanna. This process reduces the potential of the savanna fauna to react to climate change. Therefore, the protection of forest remnants close to the savanna is important to preserve the biodiversity in savanna habitats and their evolutionary potential, even if these forest remnants are not as rich as the larger forest remnants further west in the Albertine Rift. Our study did not show a correlation between habitat destruction (as measured by the proportion of fields) and land-snail species richness in the Akagera savanna. The proportion of fields is correlated with the conservation-political history of the different parts of the Akagera savanna. The lack of a correlation of human impact and conservationpolitical history on the richness of the snail fauna indicates that landscape-moderated processes like the spillover of rainforest species into the savanna may override negative local effects of habitat fragmentation on biodiversity. Moreover, human impact, such as the transformation of grasslands into fields, resulted even in increased abundances of rare hygrophilous species, probably due to the erection of living fences. Living fences comprise mainly of Euphorbia tirucalli and Lantana camara, but also harbour a selection of indigenous shrub species, function as wind breaks and, thus, reduce evaporation and erosion. On the other hand the fragmentation of suitable habitat as a result of subsistence agriculture may have negative effects on snail richness in the long run, which, however, were not revealed by our study. This may be owned to our study design. Snail populations can survive in small patches of favourable habitat. Favourable patches may still be present, even if large parts of a landscape are converted into fields and pastures. To ensure that we recorded the snail fauna along the transect belts as complete as possible, we chose sites that we considered favourable for snails (e.g. thicket clumps, living fences). To detect an effect of human

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