Chimpanzees as fauna comparisons of sympatric large mammals across long-term study sites.код для вставкиСкачать
American Journal of Primatology 70:402–409 (2008) RESEARCH ARTICLE Chimpanzees as Fauna: Comparisons of Sympatric Large Mammals Across Long-Term Study Sites SAMANTHA M. RUSSAK1,2 AND W.C. MCGREW1,3 1 Departments of Anthropology and Zoology, Miami University, Oxford, Ohio 2 School of Human Evolution and Social Change, Arizona State University, Tempe, Arizona 3 Leverhulme Centre for Human Evolutionary Studies, Department of Biological Anthropology, University of Cambridge, Cambridge, United Kingdom Although much research has shown otherwise, chimpanzees are still often classed as rainforestdwellers. Most long-term studies of wild chimpanzees (Pan troglodytes) are not situated in evergreen, closed-canopy equatorial forests, but instead are conducted in more open habitats. This study aims to elucidate the extent of chimpanzee ecological diversity by scrutinizing (recently) sympatric mammalian fauna at established study sites. We compiled presence or absence data on large mammal species at eight sites: Assirik, Bossou, Budongo, Gombe, Kibale, Lopé, Mahale, and Tai. The sites were rank ordered on the most basic ecological variable: annual total rainfall. Only three of the 65 mammalian genera compiled were sympatric with chimpanzees at all sites: Potamochoerus (bushpig), Syncerus (buffalo), and Panthera pardus (leopard). Some subfamilies (e.g. colobines) were present at most sites, but some families (e.g. hyenids) were absent at most sites. Some taxa (e.g. suids, cercopithecines) correlated better than others (e.g. canids) with basic ecological variables. The most extreme chimpanzee study site for which data are available is Assirik, Senegal. Nowhere else are chimpanzees sympatric with Erythrocebus, Alcelaphus, Hippotragus, and Ourebia. As chimpanzees are often behavioral models for extinct hominins, these living faunal assemblages have implications for paleo-ecological c 2008 Wiley-Liss, Inc. reconstructions of ancestral habitats. Am. J. Primatol. 70:402–409, 2008. Key words: Pan troglodytes; faunal assemblage; biogeography; chimpanzee ecology INTRODUCTION Despite decades of field data to the contrary, wild chimpanzees (Pan troglodytes) are still characterized as rain forest-dwellers in contemporary textbooks [e.g. Relethford, 2005; p 279], and secondary reviews [e.g. Begun, 2004; p 20]. However, most long-term studies of wild chimpanzees are not situated in evergreen, closed-canopy equatorial forests, but instead take place in more open habitats. Chimpanzees are found in 21 countries from far west to east Africa, from Senegal to Tanzania, and over 201 of latitude. Sites differ greatly in annual rainfall, lengths of dry season, and vegetation, ranging from dry, open savanna to wet, closed rainforest to mosaic habitats. The biogeographical distribution of faunal communities is related to variation in climate, vegetation, and other ecological variables, with organisms being adapted for specific environments [Fashing & Gathua, 2004; Meiri et al., 2005; Owen-Smith, 1999]. For example, wildebeest and zebra are only found in open grassland habitats, whereas mammals like dikdik and bushbuck are typically found in areas with patchy vegetation and a woody overstory [McNaughton & Georgiadis, 1986]. This relationship between r 2008 Wiley-Liss, Inc. faunal diversity and environment of ecological adaptation can sometimes be complicated by taxonomy; some taxon variants are distinguished on a subspecific level (e.g. forest versus savanna buffalo, Syncerus spp.), whereas others on a specific level (e.g. forest versus savanna elephant, Loxodonta cyclotis, L. africana), making levels of similarity unclear [de Vivo & Carmignoto, 2004]. Given the strong ecological correlations noted above, the mammalian fauna sympatric with chimpanzees should vary greatly across sites, but this has never been elucidated. Therefore, this study examines the extent of chimpanzee ecological diversity by scrutinizing (recently) sympatric mammalian fauna at six established study sites. The resulting Contract grant sponsor: Miami University Honors & Scholars Program. Correspondence to: Samantha M. Russak, School of Human Evolution and Social Change, Arizona State University, P.O. Box 872402, Tempe, AZ 85287-2402. E-mail: Samantha.Russak@asu.edu Received 28 June 2005; revised 31 October 2007; revision accepted 1 November 2007 DOI 10.1002/ajp.20506 Published online 1 February 2008 in Wiley InterScience (www. interscience.wiley.com). Chimpanzee Mammalian Faunal Communities / 403 description of the range of faunal variation at chimpanzee study sites is an important means for determining the environmental variation in hominin paleo-habitats. METHODS Site Criteria The following criteria were used to pick the chimpanzee study sites: First, they ranged in location across Africa, from east to far west (Fig. 1), covering the three recognized subspecies of P. troglodytes. Second, we chose sites with a wide range in mean annual rainfall, seeking the species’ limits of varying habitats, vegetation, and so, sympatric mammalian fauna (Spearman’s rank correlation between mean annual rainfall and dry season length: r 5 0.83, P 5 0.05). Third, we used sites of long-term study (i.e. four or more annual cycles) to maximize chances of comprehensive coverage of species present. The eight sites in the study of Whiten et al.  met all of these requirements and so were the starting point for this study. Published lists of species of mammals found at each site are usually limited to data on presence or absence, and records of abundance, density, and distribution are usually lacking. The data set includes species of mammals seen at each chimpanzee site at any point since 1960 (the year when the oldest field study began), but owing to increasing environmental pressures, especially human encroachment and predation, some of these species are now absent. The lists are inclusive for large mammals found within the chimpanzees’ ranges, but also include smaller mammals known to be preyed upon by chimpanzees. Therefore, all taxa in the data set are those that interact (directly or indirectly) with chimpanzees. Rodents, bats, insectivores, and elephant shrews were excluded from consideration as not often being recorded during censuses by diurnal primatologists. Two sites were dropped from the analysis: Lopé is an anomalous mosaic of rain forest and anthropogenic savanna; chimpanzees cross ‘‘empty,’’ open grasslands from one forest fragment to another [Tutin et al., 1997b]. Bossou is extraordinarily depauperate (c.f. ‘‘empty forest syndrome’’) because of its unprotected status and high-density human population. In addition, parts of the Mahale Mountains National Park outside the chimpanzees’ range have mammalian taxa that are not included here. Although comparisons of taxa on the level of species would reveal characteristics particular to a very specific habitat, this study compares taxa on a generic level to enable broader comparisons across study sites so that the inherent differences in species exhibit due to environmental conditions do not constrain the analysis of this study. Site Characteristics Assirik Mt. Assirik, in the Niokolo-Koba National Park in southeastern Senegal, is the driest study site for long-term studies of chimpanzees [McGrew et al., 1981] (Table I). The area is predominantly grassland, but also has deciduous woodland, bamboo thicket, and gallery forest, providing a hot, dry, open savanna habitat. Evergreen forest comprises only about 3% of vegetation at the study site, but it is disproportionately used by chimpanzees for foraging and nesting. This landscape resembles some stages of African Plio-Pleistocene, and so the fauna present could serve as important paleoecological indicators [McGrew, 1992]. Mt. Assirik provides the most extensive data set for this study, collected by the Fig. 1. Locations of long-term study sites of chimpanzees in Africa [from Whiten et al., 2001]. Am. J. Primatol. 404 / Russak and McGrew TABLE I. Sites of Long-term Study of Wild Chimpanzees [see Whiten et al., 2001] Dominant vegetation types Country coordinatesc 7 monthsa Grassland, woodland, bamboo thicket, gallery foresta Senegal 121530 N, 121460 W SAPP 1976–1979; MAPP 2000l 1531b 6 monthse Closed canopy forest, Marantaceae understory, grasslandb Gabon 01100 S, 111350 E Henschel, personal communication; Tutin et al., p. 1192e Gombef 1600b 6 monthsf Evergreen riverine forest, deciduous dry forest, thicket, grassland, moorlandb Tanzania 41400 S, 291380 E Goodall, p. 49–50f Kibaleg 1671b 5 monthsg Moist evergreen forest, colonizing forestgrassland, swampb Uganda 01320 N, 301230 E Ghiglieri, p. 13–14m; Struhsaker, p. 116n Budongoh 1684a 3 monthsp Semi-deciduous moist rain forestb Uganda 11440 N, 311330 E Reynolds, p. 89–129, 251–253o Mahalej 1774j 5–6 monthsj Semi-evergreen forest, miombo woodlandb Tanzania 61070 S, 291440 E Nishida, p. 18–19j Taii 1800i 3 monthsi Evergreen moist rainforestb Ivory Coast 51520 N, 71200 W Boesch and BoeschAchermann, p. 280–281i Bossouk 2230a 5 monthsq Primary forest patches, secondary forest, cultivated fieldb Guinea 71390 N, 81300 W Humle, personal communication Mean annual rainfall (mm)a Dry season 954d Lopee Sites Assirikd Source of mammal data a Hunt and McGrew ; bAppendix, McGrew et al. ; cSarringhaus, unpubl. data; dMcGrew et al. ; eTutin et al. [1997b]; fGoodall ; Struhsaker ; hReynolds ; iBoesch and Boesch-Achermann ; jNishida ; kMatsuzawa ; lSee site characteristics; mGhiglieri ; nStruhsaker ; oReynolds ; pNewton-Fisher ; qTakemoto . g Stirling African Primate Project February 1976– December 1979 and the Miami Assirik Pan Project February–April 2000. Lope´ The Lopé Reserve is in central Gabon in the Congo Basin [Tutin et al., 1997a]. The area is characterized by evergreen forest with a dense understory dominated by Marantaceae, and by fire-maintained, anthropogenic savanna grassland [White et al., 1995]. Although the amount of rainfall is relatively low for a wet tropical rain forest, constant cloud cover over the area causes high humidity and moisture retention. Research on comparative ecology of sympatric apes has been done there since 1984, but the chimpanzees are not fully habituated [Tutin et al., 1991]. Gombe Gombe National Park is a small national park (5200 ha) in western Tanzania, on the eastern shore Am. J. Primatol. of Lake Tanganyika [Goodall, 1986]. The mean annual rainfall varies considerably. Gombe is a mosaic of habitats [Collins & McGrew, 1988], but the research area has become isolated, as the surrounding areas have been cleared and cultivated. In addition, several species of mammal, such as hippopotamus and buffalo, have been hunted to extinction since research began at Gombe in 1960. Kibale Kibale National Park is in western Uganda, East Africa, and has a mosaic of habitats, including evergreen forest, forest-grassland, and swamp communities [Struhsaker, 1997]. This diversity in vegetation types supports an array of mammalian species. These species were threatened by intensive logging in earlier years and continue to be endangered by human encroachment. There are two main chimpanzee study sites at Kibale, Kanyawara [Wrangham et al., 1991], and Ngogo [Mitani et al., 2000], but they have similar habitats (in terms of Chimpanzee Mammalian Faunal Communities / 405 TABLE II. Artiodactyla, Perissodactyla, and Proboscidea Sympatric with Chimpanzees at Six Long-Term Study Sites Genus Alcelaphus Ourebia Hippotragus Taurotragus Tragelaphus Potamochoerus Syncerus Loxodonta Cephalophus Phacochoerus Hippopotamus Sylvicapra Kobus Hylochoerus Hyemoschus Neotragus Boocerus Choeropsis Total Common name Assirik Hartebeest Oribi Roan antelope Eland Bush-buck Bushpig Buffalo Elephant Duiker Warthog Hippopotamus Bush duiker Waterbuck Giant forest hog Chevrotain Suni/royal antelope Bongo Pygmy hippopotamus Y Y Y Y Y Y Y Y Y Y 10 Gombe Kibale Budongo Mahale Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y 5 9 Tai Y Y Y Y Y Y Y Y Y 7 7 9 Study sites listed left to right in order of increasing mean annual rainfall. both flora and fauna) and rainfall, so for this study they have been combined [Ghiglieri, 1984]. Budongo Also in western Uganda is the Budongo forest [Reynolds, 1965, 2005]. Budongo is characterized by semi-deciduous tropical rain forest. This area has undergone intensive logging over decades but still supports a variety of fauna [Plumptre & Reynolds, 1994]. Although extensive research has been done in Budongo, there has been no published comprehensive list of large mammals; the data used in this study are taken from Reynolds’ [1965, 2005] study. Taı¨ Taı̈ National Park is located in southeastern Ivory Coast, West Africa [Boesch & Boesch-Achermann, 2000]. It is the largest remaining block of moist evergreen forest in West Africa, and is home to many endemic and endangered species, such as the pygmy hippopotamus. Several neighboring communities of chimpanzees have been studied [Herbinger et al., 2001]. This area has remained little disturbed by logging, but poaching has wiped out a number of animals in the park including buffalo [Boesch & Boesch-Achermann, 2000]. Mahale Mahale Mountains National Park is located in western Tanzania [Nishida, 1990]. The mountains run in a straight line from north-west by west to south-east by east, creating two different types of habitats on either side of the mountain range. The west side of the mountains (where most of the chimpanzee research occurs) is wetter, being characterized as tropical semi-evergreen forest with biogeographic links to the Congo basin. A rain shadow from the mountains on the east side causes it to be drier, with miombo woodland and open savanna [Itani, 1979]. This study concentrates on the mammals found in areas occupied by chimpanzees studied long term [Uehara & Ihobe, 1998]. It is the only study of chimpanzees where sympatric mammals have been monitored [Uehara, 2003]. Bossou Bossou is located in southeastern Guinea, West Africa [Matsuzawa, 2002; Sugiyama, 2004]. It is the wettest of the eight sites used in this study and is characterized by primary and secondary forest, cultivated field, and savanna [Sugiyama & Koman, 1992]. The area is unprotected and human population density is high, especially after several influxes of refugees from wars in neighboring countries. The relict chimpanzee community at Bossou is small and isolated, and the abundance of other species of mammals is low, mainly because of hunting and snaring. RESULTS Table II shows sympatry between chimpanzees and three orders of large mammals: Artiodactyla, Am. J. Primatol. 406 / Russak and McGrew TABLE III. Carnivora Sympatric with Chimpanzees at Six Long-Term Study Sites Genus Lycaon Herpestes Atilax Canis Crocuta Panthera leo Viverra Mungos Felis Genetta Panthera pardus Aonyx Mellivora Nandinia Crossarchus Bdeogale Lutra Ichneumia Civettictis Ictonyx Liberiictis Poiana Total Common name Assirik Gombe Wild dog Mongoose Marsh mongoose Jackal Spotted hyena Lion Large civet Banded mongoose Small cat Genet Leopard Clawless otter Honey badger Palm civet Cusimanse Black-footed mongoose River otter White-tailed mongoose African civet Zorilla Liberian mongoose Linsang Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Kibale Budongo Mahale Tai Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y 11 13 16 3 13 12 Study sites listed left to right in order of increasing mean annual rainfall. Perissodactyla, and Proboscidea. These 18 genera range from monotypic taxa, e.g. Phacochoerus aethiopicus, Boocerus euryceros, to speciose radiations, e.g. Cephalophus, 12 spp., Tragelaphus, 4 spp (common names for taxa listed here and below can be found in Tables II–V). Only two genera, Potamochoerus and Syncerus, are found at all six study sites, although three other genera, Tragelaphus, Loxodonta, and Cephalophus, lack only one site each of being omnipresent. In contrast, half of the genera (nine of 18) occur at only one site. Of these nine genera, eight are found at either of the two habitat extremes; Alcelaphus, Ourebia, Hippotragus, and Taurotragus at the dry, open habitat of Assirik and Hyemoschus, Neotragus, Boocerus, and Choeropsis, at the wet, closed site of Tai. Of the sites, Assirik has the most sympatric genera, and Gombe the least. Table III shows sympatry between chimpanzees and 21 genera of carnivores; 15 of these genera are monotypic, e.g. Lycaon pictus, Mellivora capensis (note that for this study one genus, Panthera, has been split into two, P. leo and P. panthera, given the marked morphological, ethological, and ecological differences between the two species). Only one taxon, the leopard, is sympatric with the chimpanzee at all six sites, but several other small-bodied nocturnal carnivores (Felis, Genetta, Viverra) are found at all but one site. Only four of the 21 taxa are found at only one study site, and only two of these occur at the Am. J. Primatol. extreme sites, being Liberiictis and Poiana at Tai. Kibale has more than five times as many carnivore genera than does Budongo, despite their similar annual rainfalls and geographical proximity. Table IV shows there to be 13 genera of nonhuman primates that are sympatric with chimpanzees at the six sites. No genus is omnipresent, but two, Cercopithecus and Papio, are found at five; the exceptions are at the extremes: Assirik seems to be too dry for arboreal guenons and Tai seems to be too wet for savanna baboons. Four of the 13 genera are sympatric with apes at only one of the six sites: Erythrocebus only at Assirik; Lophocebus only at Kibale; Otolemur only at Mahale; Cercocebus only at Tai. Once again, Kibale has more than twice as many genera than does Budongo. Table V shows the sympatry of the four remaining orders (Hyracoidea, Lagomorpha, Pholidota, Tubulidentata) with chimpanzees. None comes even close to being omnipresent, but four sites had at least one genus of pangolin (Manidae) or one of the two genera of hyraxes (Procaviidae). Only Assirik, with its open grasslands, had a lagomorph, Lepus. The paucity of taxa from these orders precludes any meaningful comparison across sites. Of the 65 mammalian taxa found at the six study sites, only three genera Potamochoerus, Syncerus, and Panthera pardus, were present at all study sites. Furthermore, the mammalian fauna assemblages Chimpanzee Mammalian Faunal Communities / 407 TABLE IV. Primates Sympatric with Chimpanzees at Six Long-Term Study Sites Genus Erythrocebus Perodicticus Galago Chlorocebus Papio Procolobus Cercopithecus Colobus Euoticus Galagoides Lophocebus Otolemur Cercocebus Common name Assirik Patas monkey Potto Lesser bushbaby Vervet Baboon Colobus Guenon Black-and-white colobus Needle-clawed galago Dwarf bushbaby Grey-cheeked mangabey Greater bushbaby Sooty mangabey Y Y Y Y Y Total Gombe Kibale Budongo Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Mahale Tai Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y 5 6 9 4 7 6 Study sites listed left to right in order of increasing mean annual rainfall. TABLE V. Hyracoidea, Lagomorpha, Pholidota, and Tubulidentata Sympatric with Chimpanzees at Six Longterm Study Sites Genus Lepus Smutsia Dendrohyrax Phataginus Orycteropus Heterohyrax Uromanis Total Common name Assirik Hare Giant pangolin Tree hyrax Tree pangolin Aardvark Hyrax Long-tailed pangolin Y Gombe Kibale Budongo Mahale Tai Y Y Y Y Y Y Y Y Y Y Y Y Y 1 1 3 1 4 4 Study sites listed left to right in order of increasing mean annual rainfall. that are sympatric with chimpanzees are specific to each study site and vary widely. Kibale has the most of the 65 genera, at N 5 37, but Budongo has only 15, whereas the other four fall in a narrower range of 25–31. DISCUSSION Interpreting these data is difficult because it seems likely that not all data sets on mammals, even at the crudest level of presence/absence are complete, or even of comparable status (i.e. collected in the same manner or for the same purpose). It is unlikely that Kibale really has 2.5 times the number of mammalian taxa as Budongo, given that the two sites are near neighbors in western Uganda, and have similar rainfall and vegetation. Instead, it seems likely that the differences reflect differences in methods of data collection across sites, e.g. researchers who can follow apes from nest to nest are active before sunrise and after nightfall, and so are more likely to meet nocturnal taxa. However, cross-site differences cannot be explained by length of study: the site of the shortest study (Assirik, 5 years) has 27 genera, whereas the site of the longest study (Gombe, 45 years) has 25. If one limits comparison to large-bodied or diurnal species, the contrasts still hold, as shown in Tables II–IV. Hartebeest, oribi, roan antelope, and eland are five savanna forms of ungulate, just as chevrotain, dwarf antelopes, bongo, and pygmy hippopotamus are evergreen closed forest taxa. In between are a variety of bovids and suids that show much greater habitat flexibility, including two of the three omnipresent forms, bushpig and buffalo. In this light, elephants and duikers (Cephalophus, spp.) are notably absent from Gombe, but they ‘‘should’’ be there according to the ecology of the site. Gombe is by far the smallest of the study sites, so it is not surprising that elephants have been extinguished there, but the absence of any Cephalophus is surprising. Am. J. Primatol. 408 / Russak and McGrew Among carnivores, the small-bodied felids, herpestids, mustelids, and viverrids are mostly nocturnal and so easily missed by diurnal researchers. The remaining four large-bodied taxa (Lycaon, Canis, Crocuta, Panthera) are obvious by sight, sound, or spoor, yet their pattern of presence/ absence is confusing. Why do Assirik, Kibale, and Mahale have Canis, but not Gombe or Budongo? (Tai is not within the species distribution of wild Canis.) The same question can be asked of the inconsistent presence/absence of Crocuta. Perhaps these species were hunted to extinction by humans; to fully answer these questions would require a more detailed study of the faunal and environmental history of each site. Again, Gombe looks depauperate, lacking jackal, hyena, and lion. Only the leopard, the carnivore species with the world’s largest distribution, is a constant companion of the chimpanzee among the range of carnivores. Among the primates, the distribution of nocturnal prosimians is highly problematic; none of the six chimpanzee study sites has been subject to intensive study of these taxa. However, differences between the suites of diurnal monkeys (note that all six sites lack gorillas) are presumed to be accurate, given that they are sought-after prey or competitors for chimpanzees. Assirik seems to be too dry and open to support arboreal guenons and the gallery forest too sparse to support colobines. Tai is too wet and closed for Papio and Chlorocebus. The two Tanzanian sites lack mangabeys altogether, though they are found elsewhere in the country, and Gombe also lacks any form of black and white colobus, which is just as puzzling as Budongo’s lack of red colobus. The stochastic vagaries of what taxa were left behind in Pleistocene refugia during dry periods, plus the fact that all four East African sites are on or near the Great Rift, may account for some variation [see Gibernau & Montuire, 1996]. Overall, the distribution patterns of the mammals at the six chimpanzee study sites are consistent with gross biogeographical patterns for mammals [e.g. Badgley & Fox, 2000; McNaughton & Georgiadis, 1986; Owen-Smith, 1999]. For example, herding bovids (and the group-organized hunters that prey upon them) require vast open spaces [de Vivo & Carmignoto, 2004]. Three of the four genera from Table II (Alcelaphus, Hippotragus, and Taurotragus) that occur only at Assirik, the driest and most open of the chimpanzee sites, are the only herding artiodactyls of the sample, excluding the omnipresent Syncerus. The only social predators in the sample, wild dog, hyena, and lion were also most commonly found at the more open sites of Assirik, Gombe, and Mahale. de Vivo and Carmignoto  showed that large body size is highly correlated with open landscapes. Savanna taxa are generally larger than their rain forest counterparts. Duikers (Cephalophinae) Am. J. Primatol. occur at most sites, but species vary in size; the smallest species, the blue duiker (Cephalophus monticola) occurs at more closed sites like Tai, Budongo, and Kibale while one of the larger species, the red-flanked duiker (Cephalophus rufilatus) is only found at Assirik among the six sites. When taken to the generic level, as in this study, the ecological correlation with body size can be lost. Despite being classed as a rainforest-typical species in so many secondary sources, chimpanzees inhabit a wide range of ecotypes, most of which are mosaics of vegetation types. These differences in chimpanzee habitat extend to their sympatric faunal communities. The low overlap of taxa between sites reflects the large diversity of mammalian communities that co-occur with these apes. More studies need to be done of P. troglodytes at sites with annual rainfalls of below 1,500 mm or above 2,000 mm (e.g. Fongoli, Semliki, Ugalla, or Goualougo, Kalinzu, respectively). No single site is typical of the species P. troglodytes; even the site richest in mammalian diversity, Kibale, has only 57% (37 of 65) of the genera that co-occur with chimpanzees. Thus, chimpanzees should be considered ecological generalists. 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