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Species richness and abundance of small mammals inside and outside an African national park
Biological Conservation 98 (2001) 251±257
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Species richness and abundance of small mammals inside and outside an African national park T.M. Caro Department of Wildlife, Fish and Conservation Biology and Center for Population Biology, University of California, Davis, CA 95616, USA Received 7 February 2000; received in revised form 1 June 2000; accepted 14 June 2000
Abstract To discover whether management practices designed to protect large mammals are eective in preserving other elements of biodiversity, small mammal traps were set at 12 sites inside a national park in western Tanzania and at 13 sites outside, in an area where people practised agriculture. Over 6145 trapnights spanning both dry and wet seasons, nine species of rodent and insectivore were captured. Average species diversity and measures of abundance were greater outside than inside the Park, particularly during the dry season. These results also held when traps set inside people's houses were excluded from analyses. Mastomys natalensis, Lemniscomys striatus and the human commensal, Rattus rattus, were each found at signi®cantly greater densities outside the protected area. These data on small mammal species' richness and abundance raise questions as to whether large mammals can act as eective umbrellas for conserving small mammal taxa in East Africa. # 2001 Published by Elsevier Science Ltd. All rights reserved. Keywords: Abundance; Diversity; Katavi National Park; Small mammals; Umbrella species
1. Introduction Over the last 150 years protected areas have been set aside from human activities for a variety of reasons including scenic beauty, as hunting reserves, to protect single species, as water catchment areas, or simply because the land is worth little for other purposes (Pressey, 1994). In East Africa, the majority of protected areas were originally set up for sport hunting in the early part of the twentieth century (Selous, 1908; Roosevelt and Heller, 1922). Subsequently, they became national parks or game reserves in the 1950s, 1960s and 1970s (Caro et al., 2000). The fact that protected areas were set aside for preservation of large mammals raises the question of whether large mammal fauna can act as an umbrella for the conservation of other taxonomic groups (Berger 1997; Caro and O'Doherty 1999). For example, it is unknown whether reserves holding high large mammal densities are associated with small terrestrial mammal species richness and abundance as well.
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Evidence tangential to this problem has been collected from comparative surveys of small mammals in relatively undisturbed habitats and from those under various disturbance regimes or in anthropologically altered settings, including fragmented habitats (Laurance and Bierregaard, 1997; Mankin and Warner, 1997). A general theme to emerge from these studies is that rodent abundance increases in mildly disturbed habitats (e.g. Estrada et al., 1994, for a tropical example) including those that have been selectively logged (e.g. IsabiryeBasuta and Kasenene, 1987; Struhsaker, 1997) or subject to ``edge eects'' (Malcolm, 1994, 1997). Although it would be convenient to use studies of mammals in undisturbed and disturbed habitats as a proxy for comparing protected and unprotected areas, it is known that responses vary between species (Diendorfer et al., 1995; Songer et al., 1997; Hayward et al., 1999); responses depend on the length of time since the habitat was altered (Jerey, 1977; Ramirez and Hornocker, 1981) and on the type of disturbance involved (Estrada et al., 1994; FitzGibbon, 1997). Moreover, it is unclear as to how much natural disturbance occurs within protected areas, which again makes extrapolations risky (Stephenson, 1993). Unfortunately, there are very few
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studies to which we can turn when trying to assess the ecacy of contemporary forms of protection for small mammals (but see Decher, 1997). To determine whether protection policies for large mammals are also eective for small mammals, I here provide data on diversity and abundance of small, non-volant mammals inside and outside a national park in western Tanzania. 2. Methods 2.1. The study area The study site was in and immediately south of Katavi National Park, latitude 6 450 to 7 050 S, longitude 30 450 to 31 250 E at the north end of Rukwa Valley in Rukwa Region, western Tanzania (Fig. 1). The study site consisted of two legally designated areas. Katavi National Park consists largely of miombo woodland, a dry deciduous forest characterized by Acacia, Combretum, Grewia, Kigelia, Pterocarpus and Terminalia tree species (Rodgers, 1996) but also encompasses two seasonally inundated ¯oodplains,
Lakes Katavi and Chada (Caro, 1999a,b). No temporary or permanent settlements are allowed aside from Park headquarters and two outlying ranger posts; no livestock, beekeeping, hunting, ®shing or timber extraction are tolerated. These laws are enforced by Tanzania National Park rangers conducting vehicle and foot patrols. The second, Open Area, to the south supports miombo woodland adjacent to the Park boundary and is inhabited by Pimbwe agriculturalists and Sukuma pastoralists. Within 5 km of the Park boundary, one encounters scattered ®elds, cultivated for maize, and an open, seasonally ¯ooded grassy plain where cattle graze periodically. Eventually these give way to three small villages (Mirumba, Manga and Kibaoni). Although people cultivate, graze cattle, collect grass and ®rewood, cut hardwood, keep beehives, and hunt illegally in the Open Area, there are still many trees left and some large mammals use the Open Area on a seasonal basis (Caro, 1999a). The study was conducted in August and September 1998 during the middle of the dry season when food for people was plentiful, and at the beginning of the 1999 wet season in February when crops were still scarce.
Fig. 1. Location of 12 trapgrids (®lled squares) inside west and central portions Katavi National Park and 8 outside it in Usevia Open Area. An additional 5 trapgrids (not marked) were set in Kibaoni itself in people's houses. The village of Sitalike and hamlets of Kibaoni, Manga and Mirumba are shown as ®lled circles. The park boundary is shown as a dotted line, the main dirt road through the park as a dashed line.
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2.2. Trapping To determine species diversity and abundance of small, non-volant mammals, standard Sherman traps (2389 cm) were laid out in a grid 10 m from each other in a 77 array, except when trapping in people's houses where they were placed according to owners' wishes. During the dry season, trapgrids were placed in 9 habitat types representative of the National Park and 9 areas outside that were subject to dierent forms of human use. In the Park, these included dierent sorts of woodland, bushland and wetter open grassland habitats next to the seasonally ¯ooded lakeshores. Outside the Park, these included habitats little used by people, habitats in which trees had been felled to diering extents, land used for dierent forms of cultivation, and villages. In the second round of trapping in the wet season, the same trapgrids were resampled in the Park, save for 3 that could not be reached due to the state of the road. Instead, 3 additional habitats were added. Outside the Park, 7 out of 9 trapgrids were resampled and trapping was conducted at an additional 4 sites in houses and outbuildings because people wanted rodents removed. While the protocol in no way represents a comprehensive sampling of dierent habitats in the two areas (Caro et al., in press a), it does sample representative vegetation types that are protected and those that are subject to human activities in this region of western Tanzania. Traps were always baited with banana following a series of trials in which traps were baited with banana, dried ®sh, braized cooked maize meal, or peanuts and found to yield similar trapping success (see also Delany, 1971). Traps were set between 16.00 and 19.00 hours for a targetted 5 consecutive nights although this was often reduced to 3 when trap success was very low (<1.5% over 3 nights) or if independent circumstances dictated. Curtailing trap eort seemed justi®ed because species and number of animals caught each night changed very little over either 3 or 5 consecutive trapnights. Grids were baited for an average of 156 trapnights inside and 189 trapnights outside the Park in the dry season, and 146 and 157 inside and outside respectively in the wet season. Traps were checked between 06.30 and 09.00 hours the next day, and then closed. Captured animals were placed in a zip-lock plastic bag and weighed using a 300 g Pesola spring balance. Measurements of head plus body length and tail length were taken with calipers. Weight and length data and overall appearance were used to identify animals to the generic level using Kingdon (1997). They were further keyed to the species level using Wilson and Reeder (1993) and Nowak (1999) (see also Gordon and Watson, 1986; Linzey and Kesner, 1997). The animal was then marked with either a blue or red ``sharpie'' (permanent pen) marker on its chest or belly before release; marks remained on the animals for a full 5 days.
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Mammal species richness and abundance were compared on each trapgrid. Species richness was the number of species captured on each grid over the course of a trapping session. Abundance was measured as individuals captured per 100 trapnights, i.e. the number of dierent individual animals caught divided by the number of trapnights 100. Crude measures of vegetation were taken at every trap station on every grid except when traps were set in houses. These were thickness of leaf litter, cover of herbs, cover of shrubs, and extent of tree canopy cover, each of which was scored subjectively on a 6-point scale. For example, if no trees overshadowed a trap it was assigned a canopy score of 0; if the sky was completely obscured by leaves of trees, it was scored as 5. Subsequently, an average of each measure was calculated for the 49 traps on each grid and was entered into analyses to take account of any dierences in vegetation structure inside and outside the Park. Moon phase was taken into consideration when setting trapgrids by matching the time that grids were set inside and outside the Park. As there were no signi®cant eects of moon phase on any measure of trapping success comparing grids set over the 2 weeks spanning the new moon and those spanning the full moon, this variable was dropped from further analysis (see also Caro et al., in press b). 2.3. Analyses First, using parametric statistics, the two outcome measures were compared across trapgrids inside and outside the Park by examining data on all animals collected in the dry season, and then in the wet season. Prior to these comparisons, however, the eects of vegetation on outcome measures were examined. Pearson correlation coecients revealed no signi®cant (P<0.05) associations between average canopy or shrub scores and measures of mammal species richness or abundance, but herb and litter average scores were signi®cantly correlated with individuals/100 trapnights (N=31 trapgrids outside villages and over both seasons, herbs: r=0.546, P=0.002; litter: r=0.399, P=0.026). Herb and litter scores were therefore entered into ANOVAs comparing measures of mammal abundance inside and outside the Park by designating each grid as falling above or below the median score for herb or litter averages. Once entered as covariates, however, they lost signi®cance, nevertheless statistical comparisons with and without these confounding factors are presented in the text. Second, trapping measures for individual species were examined using data taken from both seasons together to increase sample size. In this set of comparisons, there were many instances in which no individuals of a particular species were caught which generated a large
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number of zeroes. This made it impossible to normalize the data using standard procedures so non-parametric statistics were used instead. Prior to comparing measures in the two areas, I examined correlations between canopy, shrub, herb and litter scores with the measure of abundance. Mastomys natalensis abundance was signi®cantly negatively correlated with canopy cover (N=31 trapgrids outside villages and over both seasons, Spearman correlation coecient: individuals/100 trapnights, rs= 0.329, P=0.035; but was signi®cantly positively correlated with herb cover (N=31 trapgrids, rs=0.382, P=0.017). Additionally, Lemniscomys striatus abundance was signi®cantly positively correlated with herb cover (N=31 trapgrids, rs=0.418, P=0.010). Consequently, for inside±outside Park comparisons, I analysed the data for Mastomys by whether average trap station canopy scores fell above and then below the median canopy score, and then again for whether they fell above or below the median herb score. For Lemniscomys, I compared data using above and then below median herb scores. 3. Results Four terrestrial species were trapped inside the Park: a multimammate rat (Mastomys natalensis), a bushveld gerbil (Tatera leucogaster), a pouched mouse (Saccostomus campestris) and the white-toothed shrew (Crocidura hirta) as well as an arboreal rodent, the African dormouse (Graphiurus murinus). Outside the Park, seven species were captured: the same multimammate rat (Mastomys natalensis), the same bushveld gerbil (Tatera leucogaster), the same shrew (Crocidura hirta), a meadow rat (Myomys fumatus), a zebra or striped mouse (Lemniscomys striatus), a native species of Mus, probably the pigmy mouse Mus minutoides, and one exotic, the roof rat (Rattus rattus). Not only were non-volant small mammals more diverse outside the Park but the rate at which new species were captured increased faster outside than inside the Park in the dry season (Fig. 2) suggesting that the number of species that might be caught eventually catch would be greater outside than inside if the study had progressed beyond 6145 trapnights. In the dry season, a signi®cantly greater number of species were caught on grids outside the Park than inside (Ns=9, 9 trapgrids, Xs=1.9, 0.6 species, respectively, F=4.721, P=0.045) and individuals/100 trapnights was signi®cantly greater outside than inside (Ns=9, 9, Xs=15.8, 0.7, respectively, F=6.674, P=0.020; controlling for herb and litter cover: F=4.393, P=0.058). In the wet season, a similar pattern was seen but it was not as marked. There were no signi®cant dierences in number of species caught (Ns=11, 9, Xs=1.7, 1.0 species, respectively, F=2.592, NS) but individuals/100
trapnights was signi®cantly greater outside the Park than inside although not when nonsigni®cant herb and litter covariates were included (Ns=11, 9, Xs=5.8, 1.0 respectively, F=6.331, P=0.022; controlling for herb and litter cover: F=2.082, NS). It could be argued that greater small mammal species richness and abundance outside the Park was driven by trapping in houses where exotics ¯ourish (Senzota, 1982) and where they can achieve very high densities (Leirs et al., 1996). Certainly Rattus rattus was only found in people's houses. Yet when I compared measures of trapping success omitting trapgrids placed in houses, results were replicated in the dry season (number of species, F=4.082, P=0.062; individuals/100 trapnights, F=5.061, P=0.040; controlling for confounding variables: F=4.393, P=0.058) and in the wet season (number of species, F=1.357, NS; individuals/100 trapnights, F=5.872, P=0.031; controlling for confounding variables: F=2.082, NS). Next, data were examined on a species by species basis to determine which were in¯uenced most by protection (Table 1). Mastomys natalensis was found at signi®cantly greater abundances outside the Park than inside as judged from individuals/100 trapnights when canopy cover was low (Mann-Whitney U test, N=8, 8 trapgrids respectively, z= 2.644, P=0.008). Rattus rattus was found at signi®cantly greater abundances outside than inside the Park (N=20, 18 trapgrids respectively, z=2.239, P=0.025) and the same was true for Lemniscomys striatus when herb cover was high (N=5, 10 trapgrids, respectively, z=2.070, P=0.038). Although no other signi®cant dierences were uncovered, it is worth noting that Mus minutoides was never trapped inside the Park and Graphiurus murinus was never trapped outside (Table 1). Only single individuals of Saccostomus campestris and of Myomys fumatus were caught, inside and outside the Park respectively. More generally, across the 9 species, average values of individuals/100 trapnights were signi®cantly greater outside the Park than inside (Wilcoxon matched pairs test, N=9 species, T=3.5, P<0.05). 4. Discussion This study shows that in the miombo belt of south central Africa, small, non-volant mammal species richness is lower inside a national park than in adjacent agricultural areas outside. Signi®cantly more small mammal species were caught on grids outside the Park in the dry season and somewhat more in the wet season. Four strictly terrestrial species were trapped only outside the Park, Lemniscomys striatus, Myomys fumatus, Mus minutoides, and Rattus rattus whereas only one, Saccostomus campestris, was trapped inside but not outside the Park. The rate of captures of new mammal
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Fig. 2. Cumulative number of new species captured inside (®lled triangles) and outside (®lled squares) the park plotted against an increasing number of trapnights in the dry season and wet season.
Table 1 Mean values of measures of species' abundance inside and outside Katavi National Park over dry and wet seasons combined
Mastomys natalensis Lemniscomys striatus Tatera leucogaster Myomys fumatus Saccostomus campestris Crocidura hirta Graphiurus murinus Rattus rattus Mus minutoides
Number of individuals
Individuals/100 trapnights
In
Out
In
Out
7 0 9 0 1 1 5 0 0
316 2 17 1 0 19 0 51 3
0.27 0 0.30 0 0.04 0.04 0.19 0 0
7.34 0.04 0.35 0.02 0 0.39 0 2.04 0.14
species increased more rapidly outside than inside at least during the dry season suggesting that the total number of species might eventually be higher in areas outside protection. While other trapping methods, such as pitfall traps, would probably reveal additional species in the two areas, the design does provide a fair comparison of those small mammals willing to enter a Sherman trap baited with banana.
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Small mammal abundance was very low in Katavi National Park, 0.2/ha in the dry and 0.3/ha in the wet season, compared to 13±75/ha in Sengwa Wildlife Research Area, Zimbabwe (Linzey and Kesner, 1997), 2±17/ha in Liwonde National Park, Malawi (Happold and Happold, 1990) and 9±33/ha in Mozambique (Gliwicz, 1987) (all of which are miombo habitats) and 17± 63/ha in Ruwenzori National Park (Cheeseman and Delany, 1979) and 3±40/ha in Nakuru National Park (other East African albeit savanna parks) although not all these densities were calculated in the same way. Small mammal abundance was lower inside the Park than outside in both dry and wet seasons. Signi®cant results could not be attributed to the presence of commensal exotic species outside since, when trapgrids set in houses and outbuildings were omitted from analyses, abundance was still signi®cantly greater outside the Park. The species chie¯y responsible for the greater small mammal abundance outside the Park were Mastomys natalensis, Lemniscomys striatus and Rattus rattus. Results here con®rm and expand those found in Ghana. Jerey (1977) found that the removal of high forest and its replacement by agriculture and domestic housing resulted in an increase in diversity, numbers and biomass of rodents. She surmised that agricultural practices were bene®cial to rodent fauna although the mechanisms by which this occurred were obscure (see also Christiansen, 1966; Rahm, 1967; Delany, 1971; Isabirye-Basuta and Kasenene, 1987). Again in Ghana, sacred groves outside legally protected reserves had high population densities and supported mammal communities not found elsewhere (Decher and Bahian, 1999). A similar ®nding has been made for thornveld birds outside protected areas in Botswana (Herremans, 1998). Several factors could be responsible for the higher species richness and abundance of the small, non-volant mammal community in the Open Area. First, food availability or quality may be higher outside the Park. Highest species richness at any site was in a garden in the dry season when bananas, mangoes and maize were available. Similarly, density was far higher in a maize ®eld when maize was on the cob than after stalks had been burnt and the ®eld freshly planted; and it was three times as high in a house when maize was stored in grain baskets than when stores were empty in the wet season. Mastomys natalensis breeds during and after the rains (Leirs et al., 1990, 1996) and before the end of the dry season (Taylor and Green, 1976; Christensen, 1993; but see Leirs et al., 1994) which would account for high dry season abundance. Additionally, few small mammals were captured outside the Park at sites where no cultivation occurred. Second, predator abundance might be lower outside the Park. While most mammals found in the Park were also seen by people in the Open Area (A. Msago, personal communication), estimated densities of small diurnal carnivores such as mongooses were lower
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in the Open Area (Caro, 1999a). Relative densities of snakes and raptors are unknown but there were more perching sites for raptors inside the Park which is known to increase predation on Mastomys natalensis (van Gulck et al., 1998). Third, competition between ungulates and rodents could be higher inside the Park. Evidence from Kenya shows that small mammal abundance increased sharply in the year following experimental exclusion of large ungulates (Keesing, 1998, 2000). Certainly large wild mammal densities were signi®cantly lower in the Open Area than in the Park; however, livestock densities were far higher in the Open Area (Caro, 1999a). It is dicult to assess the eects of competition from livestock and wild ungulates without experimentation (e.g. Young et al., 1998). 5. Conclusions This is one of a very few studies that has compared small mammal fauna inside and outside a fully protected area in the tropics (but see Decher and Bahiran, 1999) and has shown that species richness and abundance are higher outside. This could be due to relatively low densities inside this particular park as suggested by comparisons with other protected areas, or to relatively high densities outside con®rming indirect evidence from a wide variety of regions that habitat disturbance promotes small mammal abundance, or to both. Whatever causal factors underly these dierences, these ®ndings address the eectiveness of using species as umbrellas for conservation. Since protected areas in East Africa were set up to conserve large mammal populations, it seems that large bodied species may not act as eective umbrella species for smaller mammals despite having much larger home ranges, and that protected areas are performing a relatively poor service in protecting small mammals in comparison to anthropogenically disturbed habitats. Indeed, multiple-use areas which sanction human settlements and subsistence activities to the detriment of large mammal populations (Caro et al., 1998) could be an important form of protection for small, non-volant mammals. Acknowledgements I thank the Government of Tanzania, particularly the Commission of Science and Technology, Tanzania Wildlife Research Institute and Tanzania National Parks for permissions, the University of California faculty research grant program for funding, and Friends of Conservation and British Airways frequent ¯ier programme for reduced airfares. Research was conducted under a UC Davis Animal Care and Use Protocol. I thank Monique Borgerho Mulder, Kawawa Khalfan,
Ally Kyambile, Julius Nassari and Ayubu Msago for help with logistics; Ron Cole, Doug Kelt and I. Lejora for discussions; Barnabas Caro, Meredith Evans and Brian Paciotti for important help in recording data; John Kabisu, Malashi Kadele, Charles Kapembe, Julius Kassanga, Juma Lusakila, Gisella Mali ya Bwana, Mwalimu Mbasa, Marietta Mkata, Ayubu Msago, Masanilo Ruhemeja and Ivo Selemani for help in the ®eld; and Doug Kelt, Mark Schwartz, Truman Young and anonymous reviewers for comments. References Berger, J., 1997. Population constraints associated with the use of black rhinos as an umbrella species for desert herbivores. Conservation Biology 11, 69±78. Caro, T.M., 1999a. Densities of mammals in partially protected areas: the Katavi ecosystem of western Tanzania. Journal of Applied Ecology 36, 205±217. Caro, T.M., 1999b. Abundance and distribution of mammals in Katavi National Park, Tanzania. African Journal of Ecology 37, 305±313. Caro, T.M., O'Doherty, G., 1999. On the use of surrogate species in conservation biology. Conservation Biology 13, 805±814. Caro, T.M., Pelkey, N., Borner, M., Campbell, K.L.I., Woodworth, B.L., Farm, B.P., Severre, E.L.B., 1998. Consequences of dierent forms of protection for large mammalsin Tanzania: preliminary analyses. African Journal of Ecology 36, 303±320. Caro, T.M., Rejmanek, M., Pelkey, N., 2000. Which mammals bene®t from protection in East Africa? In: Enwistle, A., Dunstone, N. (Eds), Priorities for the Conservation of Mammalian Diversity. Has the Panda had its Day? Cambridge University Press, Cambridge, pp. 221±238. Caro, T.M., Kelly, M.J., Bol, N., Matola, S., in press a. Inventorying mammals at multiple sites: the Maya Mountains of Belize. Journal of Mammalogy. Caro, T.M., Brock, R.E., Kelly, M., in press b. Diversity of mammals in the Bladen Nature Reserve, Belize and factors aecting their trapping success. Zeitschrift fur Saugetierkunde. Cheeseman, C.L., Delany, M.J., 1979. The population dynamics of small rodents in a tropical African grassland. Journal of Zoology 188, 451±475. Christensen, J.T., 1993. The seasonal variation in breeding and growth of Mastomys natalensis (Rodentia: Muridae): evidence for resource limitation. African Journal of Ecology 31, 1±9. Christiansen, A., 1966. Les mammiferes de la foret equatoriale de l'Est du Congo. Annals of the Museum of the Republique Africane Central 8, 149±176. Decher, J., 1997. Conservation, small mammals, and the future of sacred groves in West Africa. Biodiversity and Conservation 6, 1007±1026. Decher, J., Bahrian, L.K., 1999. Diversity and structure of terrestrial small mammal communities in dierent vegetation types in the Accra Plains of Ghana. Journal of Zoology 247, 395±408. Delany, M.J., 1971. The biology of small rodents in Mayanja Forest, Uganda. Journal of Zoology 165, 85±129. Diendorfer, J.F., Slade, N.A., Gaines, M.S., Holt, R.D., 1995. Population dynamics of small mammals in fragmented and continuous old-®eld habitat. In: Lidicker, W.Z. Jr. (Ed.), Landscape Approaches in Mammalian Ecology. University of Minnesota Press, Minneapolis, pp. 175±199. Estrada, A., Coates-Estrada, R., Merritt Jr., D., 1994. Non ¯ying mammals and landscape changes in the tropical rain forest region of Los Tuxtlas, Mexico. Ecography 17, 229±241.
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Conservation of Fragmented Communities. University of Chicago Press, Chicago, pp. 207±221. Mankin, P.C., Warner, R.E., 1997. Mammals of Illinois and the midwest: ecological and conservation issues for human-dominated landscapes. In: Schwartz, M.W. (Ed.), Conservation in Highly Fragmented Landscapes. Chapman and Hall, New York, pp. ±. Nowak, R.M., 1999. Walker's Mammals of the World, Vol. II, 6th Edition. John Hopkins University Press, Baltimore. Pressey, R.L., 1994. Ad hoc reservations: forward or backward steps in developing representative reserve systems. Conservation Biology 8, 662±668. Rahm, U., 1967. Note sur la reproduction des Sciurides et Murides dans la foret equatoriale au Congo. Revue Suisse Zoologie 77, 635± 646. Ramirez Jr., P., Hornocker, M., 1981. Small mammal populations in dierent aged clearcuts in northwestern Montana. Journal of Mammalogy 62, 400±403. Rodgers, W.A., 1996. The miombo woodlands. In: McClanahan, T.R., Young, T.P. (Eds.), East African Ecosystems and their Conservation. Oxford University Press, New York, pp. 299±325. Roosevelt, T., Heller, E., 1922. Life-histories of African Game Animals, John Murray, London. Selous, F., 1908. African Nature Notes and Reminiscences, Macmillan, London. Senzota, R.B.M., 1982. A house rat enters Serengeti. African Journal of Ecology 20, 211±212. Songer, M.A., Lomolino, M.V., Perault, D.R., 1997. Niche dynamics of deer mice in a fragmented, old-growth landscape. Journal of Mammalogy 78, 1027±1039. Stephenson, P.J., 1993. The small mammal fauna of Reserve Speciale d'Analamazaotra, Madagascar: the eects of human disturbance on endemic species diversity. Biodiversity and Conservation 2, 603± 615. Struhsaker, T.T., 1997. Ecology of an African Rain Forest: Logging in Kibale and the Con¯ict between Conservation and Exploitation, University Press of Florida, Gainesville. Taylor, K.D., Green, M.G., 1976. The in¯uence of rainfall on diet and reproduction in four African rodent species. Journal of Zoology 180, 367±389. van Gulck, T., Stoks, R., Verhagen, R., Sabuni, C.A., Mwanjabe, P., Leirs, H., 1998. Short-term eects of avian predation variation on population size and local survival of the multimammate rat, Mastomys natalensis (Rodentia, Muridae). Mammalia 62, 329±339. Wilson, D.E., Reeder, D.M., 1993. Mammal Species of the World, 2nd Edition, Smithsonian University Press, Washington. Young, T.P., Okello, B.D., Kinyua, D., Palmer, T.M., 1998. KLEE: a long-term multi-species herbivore exclusion experiment in Laikipia, Kenya. African Journal of Range and Forage Science 14, 94± 102.
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Species richness and abundance of small mammals inside and outside an African national park T.M. Caro Department of Wildlife, Fish and Conservation Biology and Center for Population Biology, University of California, Davis, CA 95616, USA Received 7 February 2000; received in revised form 1 June 2000; accepted 14 June 2000
Abstract To discover whether management practices designed to protect large mammals are eective in preserving other elements of biodiversity, small mammal traps were set at 12 sites inside a national park in western Tanzania and at 13 sites outside, in an area where people practised agriculture. Over 6145 trapnights spanning both dry and wet seasons, nine species of rodent and insectivore were captured. Average species diversity and measures of abundance were greater outside than inside the Park, particularly during the dry season. These results also held when traps set inside people's houses were excluded from analyses. Mastomys natalensis, Lemniscomys striatus and the human commensal, Rattus rattus, were each found at signi®cantly greater densities outside the protected area. These data on small mammal species' richness and abundance raise questions as to whether large mammals can act as eective umbrellas for conserving small mammal taxa in East Africa. # 2001 Published by Elsevier Science Ltd. All rights reserved. Keywords: Abundance; Diversity; Katavi National Park; Small mammals; Umbrella species
1. Introduction Over the last 150 years protected areas have been set aside from human activities for a variety of reasons including scenic beauty, as hunting reserves, to protect single species, as water catchment areas, or simply because the land is worth little for other purposes (Pressey, 1994). In East Africa, the majority of protected areas were originally set up for sport hunting in the early part of the twentieth century (Selous, 1908; Roosevelt and Heller, 1922). Subsequently, they became national parks or game reserves in the 1950s, 1960s and 1970s (Caro et al., 2000). The fact that protected areas were set aside for preservation of large mammals raises the question of whether large mammal fauna can act as an umbrella for the conservation of other taxonomic groups (Berger 1997; Caro and O'Doherty 1999). For example, it is unknown whether reserves holding high large mammal densities are associated with small terrestrial mammal species richness and abundance as well.
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Evidence tangential to this problem has been collected from comparative surveys of small mammals in relatively undisturbed habitats and from those under various disturbance regimes or in anthropologically altered settings, including fragmented habitats (Laurance and Bierregaard, 1997; Mankin and Warner, 1997). A general theme to emerge from these studies is that rodent abundance increases in mildly disturbed habitats (e.g. Estrada et al., 1994, for a tropical example) including those that have been selectively logged (e.g. IsabiryeBasuta and Kasenene, 1987; Struhsaker, 1997) or subject to ``edge eects'' (Malcolm, 1994, 1997). Although it would be convenient to use studies of mammals in undisturbed and disturbed habitats as a proxy for comparing protected and unprotected areas, it is known that responses vary between species (Diendorfer et al., 1995; Songer et al., 1997; Hayward et al., 1999); responses depend on the length of time since the habitat was altered (Jerey, 1977; Ramirez and Hornocker, 1981) and on the type of disturbance involved (Estrada et al., 1994; FitzGibbon, 1997). Moreover, it is unclear as to how much natural disturbance occurs within protected areas, which again makes extrapolations risky (Stephenson, 1993). Unfortunately, there are very few
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studies to which we can turn when trying to assess the ecacy of contemporary forms of protection for small mammals (but see Decher, 1997). To determine whether protection policies for large mammals are also eective for small mammals, I here provide data on diversity and abundance of small, non-volant mammals inside and outside a national park in western Tanzania. 2. Methods 2.1. The study area The study site was in and immediately south of Katavi National Park, latitude 6 450 to 7 050 S, longitude 30 450 to 31 250 E at the north end of Rukwa Valley in Rukwa Region, western Tanzania (Fig. 1). The study site consisted of two legally designated areas. Katavi National Park consists largely of miombo woodland, a dry deciduous forest characterized by Acacia, Combretum, Grewia, Kigelia, Pterocarpus and Terminalia tree species (Rodgers, 1996) but also encompasses two seasonally inundated ¯oodplains,
Lakes Katavi and Chada (Caro, 1999a,b). No temporary or permanent settlements are allowed aside from Park headquarters and two outlying ranger posts; no livestock, beekeeping, hunting, ®shing or timber extraction are tolerated. These laws are enforced by Tanzania National Park rangers conducting vehicle and foot patrols. The second, Open Area, to the south supports miombo woodland adjacent to the Park boundary and is inhabited by Pimbwe agriculturalists and Sukuma pastoralists. Within 5 km of the Park boundary, one encounters scattered ®elds, cultivated for maize, and an open, seasonally ¯ooded grassy plain where cattle graze periodically. Eventually these give way to three small villages (Mirumba, Manga and Kibaoni). Although people cultivate, graze cattle, collect grass and ®rewood, cut hardwood, keep beehives, and hunt illegally in the Open Area, there are still many trees left and some large mammals use the Open Area on a seasonal basis (Caro, 1999a). The study was conducted in August and September 1998 during the middle of the dry season when food for people was plentiful, and at the beginning of the 1999 wet season in February when crops were still scarce.
Fig. 1. Location of 12 trapgrids (®lled squares) inside west and central portions Katavi National Park and 8 outside it in Usevia Open Area. An additional 5 trapgrids (not marked) were set in Kibaoni itself in people's houses. The village of Sitalike and hamlets of Kibaoni, Manga and Mirumba are shown as ®lled circles. The park boundary is shown as a dotted line, the main dirt road through the park as a dashed line.
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2.2. Trapping To determine species diversity and abundance of small, non-volant mammals, standard Sherman traps (2389 cm) were laid out in a grid 10 m from each other in a 77 array, except when trapping in people's houses where they were placed according to owners' wishes. During the dry season, trapgrids were placed in 9 habitat types representative of the National Park and 9 areas outside that were subject to dierent forms of human use. In the Park, these included dierent sorts of woodland, bushland and wetter open grassland habitats next to the seasonally ¯ooded lakeshores. Outside the Park, these included habitats little used by people, habitats in which trees had been felled to diering extents, land used for dierent forms of cultivation, and villages. In the second round of trapping in the wet season, the same trapgrids were resampled in the Park, save for 3 that could not be reached due to the state of the road. Instead, 3 additional habitats were added. Outside the Park, 7 out of 9 trapgrids were resampled and trapping was conducted at an additional 4 sites in houses and outbuildings because people wanted rodents removed. While the protocol in no way represents a comprehensive sampling of dierent habitats in the two areas (Caro et al., in press a), it does sample representative vegetation types that are protected and those that are subject to human activities in this region of western Tanzania. Traps were always baited with banana following a series of trials in which traps were baited with banana, dried ®sh, braized cooked maize meal, or peanuts and found to yield similar trapping success (see also Delany, 1971). Traps were set between 16.00 and 19.00 hours for a targetted 5 consecutive nights although this was often reduced to 3 when trap success was very low (<1.5% over 3 nights) or if independent circumstances dictated. Curtailing trap eort seemed justi®ed because species and number of animals caught each night changed very little over either 3 or 5 consecutive trapnights. Grids were baited for an average of 156 trapnights inside and 189 trapnights outside the Park in the dry season, and 146 and 157 inside and outside respectively in the wet season. Traps were checked between 06.30 and 09.00 hours the next day, and then closed. Captured animals were placed in a zip-lock plastic bag and weighed using a 300 g Pesola spring balance. Measurements of head plus body length and tail length were taken with calipers. Weight and length data and overall appearance were used to identify animals to the generic level using Kingdon (1997). They were further keyed to the species level using Wilson and Reeder (1993) and Nowak (1999) (see also Gordon and Watson, 1986; Linzey and Kesner, 1997). The animal was then marked with either a blue or red ``sharpie'' (permanent pen) marker on its chest or belly before release; marks remained on the animals for a full 5 days.
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Mammal species richness and abundance were compared on each trapgrid. Species richness was the number of species captured on each grid over the course of a trapping session. Abundance was measured as individuals captured per 100 trapnights, i.e. the number of dierent individual animals caught divided by the number of trapnights 100. Crude measures of vegetation were taken at every trap station on every grid except when traps were set in houses. These were thickness of leaf litter, cover of herbs, cover of shrubs, and extent of tree canopy cover, each of which was scored subjectively on a 6-point scale. For example, if no trees overshadowed a trap it was assigned a canopy score of 0; if the sky was completely obscured by leaves of trees, it was scored as 5. Subsequently, an average of each measure was calculated for the 49 traps on each grid and was entered into analyses to take account of any dierences in vegetation structure inside and outside the Park. Moon phase was taken into consideration when setting trapgrids by matching the time that grids were set inside and outside the Park. As there were no signi®cant eects of moon phase on any measure of trapping success comparing grids set over the 2 weeks spanning the new moon and those spanning the full moon, this variable was dropped from further analysis (see also Caro et al., in press b). 2.3. Analyses First, using parametric statistics, the two outcome measures were compared across trapgrids inside and outside the Park by examining data on all animals collected in the dry season, and then in the wet season. Prior to these comparisons, however, the eects of vegetation on outcome measures were examined. Pearson correlation coecients revealed no signi®cant (P<0.05) associations between average canopy or shrub scores and measures of mammal species richness or abundance, but herb and litter average scores were signi®cantly correlated with individuals/100 trapnights (N=31 trapgrids outside villages and over both seasons, herbs: r=0.546, P=0.002; litter: r=0.399, P=0.026). Herb and litter scores were therefore entered into ANOVAs comparing measures of mammal abundance inside and outside the Park by designating each grid as falling above or below the median score for herb or litter averages. Once entered as covariates, however, they lost signi®cance, nevertheless statistical comparisons with and without these confounding factors are presented in the text. Second, trapping measures for individual species were examined using data taken from both seasons together to increase sample size. In this set of comparisons, there were many instances in which no individuals of a particular species were caught which generated a large
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number of zeroes. This made it impossible to normalize the data using standard procedures so non-parametric statistics were used instead. Prior to comparing measures in the two areas, I examined correlations between canopy, shrub, herb and litter scores with the measure of abundance. Mastomys natalensis abundance was signi®cantly negatively correlated with canopy cover (N=31 trapgrids outside villages and over both seasons, Spearman correlation coecient: individuals/100 trapnights, rs= 0.329, P=0.035; but was signi®cantly positively correlated with herb cover (N=31 trapgrids, rs=0.382, P=0.017). Additionally, Lemniscomys striatus abundance was signi®cantly positively correlated with herb cover (N=31 trapgrids, rs=0.418, P=0.010). Consequently, for inside±outside Park comparisons, I analysed the data for Mastomys by whether average trap station canopy scores fell above and then below the median canopy score, and then again for whether they fell above or below the median herb score. For Lemniscomys, I compared data using above and then below median herb scores. 3. Results Four terrestrial species were trapped inside the Park: a multimammate rat (Mastomys natalensis), a bushveld gerbil (Tatera leucogaster), a pouched mouse (Saccostomus campestris) and the white-toothed shrew (Crocidura hirta) as well as an arboreal rodent, the African dormouse (Graphiurus murinus). Outside the Park, seven species were captured: the same multimammate rat (Mastomys natalensis), the same bushveld gerbil (Tatera leucogaster), the same shrew (Crocidura hirta), a meadow rat (Myomys fumatus), a zebra or striped mouse (Lemniscomys striatus), a native species of Mus, probably the pigmy mouse Mus minutoides, and one exotic, the roof rat (Rattus rattus). Not only were non-volant small mammals more diverse outside the Park but the rate at which new species were captured increased faster outside than inside the Park in the dry season (Fig. 2) suggesting that the number of species that might be caught eventually catch would be greater outside than inside if the study had progressed beyond 6145 trapnights. In the dry season, a signi®cantly greater number of species were caught on grids outside the Park than inside (Ns=9, 9 trapgrids, Xs=1.9, 0.6 species, respectively, F=4.721, P=0.045) and individuals/100 trapnights was signi®cantly greater outside than inside (Ns=9, 9, Xs=15.8, 0.7, respectively, F=6.674, P=0.020; controlling for herb and litter cover: F=4.393, P=0.058). In the wet season, a similar pattern was seen but it was not as marked. There were no signi®cant dierences in number of species caught (Ns=11, 9, Xs=1.7, 1.0 species, respectively, F=2.592, NS) but individuals/100
trapnights was signi®cantly greater outside the Park than inside although not when nonsigni®cant herb and litter covariates were included (Ns=11, 9, Xs=5.8, 1.0 respectively, F=6.331, P=0.022; controlling for herb and litter cover: F=2.082, NS). It could be argued that greater small mammal species richness and abundance outside the Park was driven by trapping in houses where exotics ¯ourish (Senzota, 1982) and where they can achieve very high densities (Leirs et al., 1996). Certainly Rattus rattus was only found in people's houses. Yet when I compared measures of trapping success omitting trapgrids placed in houses, results were replicated in the dry season (number of species, F=4.082, P=0.062; individuals/100 trapnights, F=5.061, P=0.040; controlling for confounding variables: F=4.393, P=0.058) and in the wet season (number of species, F=1.357, NS; individuals/100 trapnights, F=5.872, P=0.031; controlling for confounding variables: F=2.082, NS). Next, data were examined on a species by species basis to determine which were in¯uenced most by protection (Table 1). Mastomys natalensis was found at signi®cantly greater abundances outside the Park than inside as judged from individuals/100 trapnights when canopy cover was low (Mann-Whitney U test, N=8, 8 trapgrids respectively, z= 2.644, P=0.008). Rattus rattus was found at signi®cantly greater abundances outside than inside the Park (N=20, 18 trapgrids respectively, z=2.239, P=0.025) and the same was true for Lemniscomys striatus when herb cover was high (N=5, 10 trapgrids, respectively, z=2.070, P=0.038). Although no other signi®cant dierences were uncovered, it is worth noting that Mus minutoides was never trapped inside the Park and Graphiurus murinus was never trapped outside (Table 1). Only single individuals of Saccostomus campestris and of Myomys fumatus were caught, inside and outside the Park respectively. More generally, across the 9 species, average values of individuals/100 trapnights were signi®cantly greater outside the Park than inside (Wilcoxon matched pairs test, N=9 species, T=3.5, P<0.05). 4. Discussion This study shows that in the miombo belt of south central Africa, small, non-volant mammal species richness is lower inside a national park than in adjacent agricultural areas outside. Signi®cantly more small mammal species were caught on grids outside the Park in the dry season and somewhat more in the wet season. Four strictly terrestrial species were trapped only outside the Park, Lemniscomys striatus, Myomys fumatus, Mus minutoides, and Rattus rattus whereas only one, Saccostomus campestris, was trapped inside but not outside the Park. The rate of captures of new mammal
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Fig. 2. Cumulative number of new species captured inside (®lled triangles) and outside (®lled squares) the park plotted against an increasing number of trapnights in the dry season and wet season.
Table 1 Mean values of measures of species' abundance inside and outside Katavi National Park over dry and wet seasons combined
Mastomys natalensis Lemniscomys striatus Tatera leucogaster Myomys fumatus Saccostomus campestris Crocidura hirta Graphiurus murinus Rattus rattus Mus minutoides
Number of individuals
Individuals/100 trapnights
In
Out
In
Out
7 0 9 0 1 1 5 0 0
316 2 17 1 0 19 0 51 3
0.27 0 0.30 0 0.04 0.04 0.19 0 0
7.34 0.04 0.35 0.02 0 0.39 0 2.04 0.14
species increased more rapidly outside than inside at least during the dry season suggesting that the total number of species might eventually be higher in areas outside protection. While other trapping methods, such as pitfall traps, would probably reveal additional species in the two areas, the design does provide a fair comparison of those small mammals willing to enter a Sherman trap baited with banana.
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Small mammal abundance was very low in Katavi National Park, 0.2/ha in the dry and 0.3/ha in the wet season, compared to 13±75/ha in Sengwa Wildlife Research Area, Zimbabwe (Linzey and Kesner, 1997), 2±17/ha in Liwonde National Park, Malawi (Happold and Happold, 1990) and 9±33/ha in Mozambique (Gliwicz, 1987) (all of which are miombo habitats) and 17± 63/ha in Ruwenzori National Park (Cheeseman and Delany, 1979) and 3±40/ha in Nakuru National Park (other East African albeit savanna parks) although not all these densities were calculated in the same way. Small mammal abundance was lower inside the Park than outside in both dry and wet seasons. Signi®cant results could not be attributed to the presence of commensal exotic species outside since, when trapgrids set in houses and outbuildings were omitted from analyses, abundance was still signi®cantly greater outside the Park. The species chie¯y responsible for the greater small mammal abundance outside the Park were Mastomys natalensis, Lemniscomys striatus and Rattus rattus. Results here con®rm and expand those found in Ghana. Jerey (1977) found that the removal of high forest and its replacement by agriculture and domestic housing resulted in an increase in diversity, numbers and biomass of rodents. She surmised that agricultural practices were bene®cial to rodent fauna although the mechanisms by which this occurred were obscure (see also Christiansen, 1966; Rahm, 1967; Delany, 1971; Isabirye-Basuta and Kasenene, 1987). Again in Ghana, sacred groves outside legally protected reserves had high population densities and supported mammal communities not found elsewhere (Decher and Bahian, 1999). A similar ®nding has been made for thornveld birds outside protected areas in Botswana (Herremans, 1998). Several factors could be responsible for the higher species richness and abundance of the small, non-volant mammal community in the Open Area. First, food availability or quality may be higher outside the Park. Highest species richness at any site was in a garden in the dry season when bananas, mangoes and maize were available. Similarly, density was far higher in a maize ®eld when maize was on the cob than after stalks had been burnt and the ®eld freshly planted; and it was three times as high in a house when maize was stored in grain baskets than when stores were empty in the wet season. Mastomys natalensis breeds during and after the rains (Leirs et al., 1990, 1996) and before the end of the dry season (Taylor and Green, 1976; Christensen, 1993; but see Leirs et al., 1994) which would account for high dry season abundance. Additionally, few small mammals were captured outside the Park at sites where no cultivation occurred. Second, predator abundance might be lower outside the Park. While most mammals found in the Park were also seen by people in the Open Area (A. Msago, personal communication), estimated densities of small diurnal carnivores such as mongooses were lower
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in the Open Area (Caro, 1999a). Relative densities of snakes and raptors are unknown but there were more perching sites for raptors inside the Park which is known to increase predation on Mastomys natalensis (van Gulck et al., 1998). Third, competition between ungulates and rodents could be higher inside the Park. Evidence from Kenya shows that small mammal abundance increased sharply in the year following experimental exclusion of large ungulates (Keesing, 1998, 2000). Certainly large wild mammal densities were signi®cantly lower in the Open Area than in the Park; however, livestock densities were far higher in the Open Area (Caro, 1999a). It is dicult to assess the eects of competition from livestock and wild ungulates without experimentation (e.g. Young et al., 1998). 5. Conclusions This is one of a very few studies that has compared small mammal fauna inside and outside a fully protected area in the tropics (but see Decher and Bahiran, 1999) and has shown that species richness and abundance are higher outside. This could be due to relatively low densities inside this particular park as suggested by comparisons with other protected areas, or to relatively high densities outside con®rming indirect evidence from a wide variety of regions that habitat disturbance promotes small mammal abundance, or to both. Whatever causal factors underly these dierences, these ®ndings address the eectiveness of using species as umbrellas for conservation. Since protected areas in East Africa were set up to conserve large mammal populations, it seems that large bodied species may not act as eective umbrella species for smaller mammals despite having much larger home ranges, and that protected areas are performing a relatively poor service in protecting small mammals in comparison to anthropogenically disturbed habitats. Indeed, multiple-use areas which sanction human settlements and subsistence activities to the detriment of large mammal populations (Caro et al., 1998) could be an important form of protection for small, non-volant mammals. Acknowledgements I thank the Government of Tanzania, particularly the Commission of Science and Technology, Tanzania Wildlife Research Institute and Tanzania National Parks for permissions, the University of California faculty research grant program for funding, and Friends of Conservation and British Airways frequent ¯ier programme for reduced airfares. Research was conducted under a UC Davis Animal Care and Use Protocol. I thank Monique Borgerho Mulder, Kawawa Khalfan,
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