Introduction
The bush dog Speothos venaticus is one of the lesser-known Neotropical canids. Although it has been the subject of several captive behavioural studies (Kleiman, Reference Kleiman1972; Brady, Reference Brady1981; Biben, Reference Biben1983; Macdonald, Reference Macdonald1996) only two ecological studies have been conducted in the wild (Zuercher et al., Reference Zuercher, Gipson and Carrillo2005; E. Lima & J.C. Dalponte, pers. comm.). The majority of information comes from scattered incidental observations of predatory behaviour (Peres, Reference Peres1991; Aquino & Puertas, Reference Aquino and Puertas1997; Wallace et al., Reference Wallace, Painter and Saldania2002), group size (Dalponte, Reference Dalponte1995; Aquino & Puertas, Reference Aquino and Puertas1997; Silveira et al., Reference Silveira, Jácomo, Rodrigues and Diniz-Filho1998), and presence (Strahl et al., Reference Strahl, Silva and Goldstein1992; Silva & Soares, Reference Silva and Soares1999; Barnett et al., Reference Barnett, Shapley and Engstrom2001). The bush dog is categorized as Near Threatened globally (IUCN, 2008) but Vulnerable in Brazil (Oliveira & Dalponte, in press) and regionally Endangered in Maranhão state, northern Brazil (Oliveira, 2007), in particular because of high rates of habitat loss and fragmentation in eastern Amazonia (INPE, 2008).
Although historically reported from eastern Panama south through to south-eastern Brazil, eastern Paraguay and north-eastern Argentina, the actual distribution of the species is unclear. Current distribution maps lack exact locations (Ginsberg & Macdonald, Reference Ginsberg and Macdonald1990; Eisenberg & Redford, Reference Eisenberg and Redford1999) and may overestimate or, conversely, show gaps in the species' distribution (Emmons & Feer, Reference Emmons and Feer1997), as appears to be the case in eastern Amazonia.
Given the scarcity of information on the distribution and natural history of the bush dog I report here a test of the hypotheses that the species is almost exclusively associated with conserved areas, as indicated in earlier literature, and that, as widely assumed, it is found throughout all of northern Brazil. I also evaluated the role that the region's conservation units and the bush dog's biology could play in the species' conservation.
Methods
The areas of northern Brazil considered in this analysis include the states of Amapá, Pará, Maranhão and Tocantins, especially that part east of the Tocantins River (Fig. 1). The majority of this region is covered by both disturbed and undisturbed Amazon forest, with mangroves and other coastal vegetation, savannah in the south and east, and transitional areas between (IBGE, 1993).
Distribution of the bush dog in northern Brazil, illustrating the locations of field observations and records in the literature and in museums (the numbers correspond to the numbered localities in Table 2).
I used three sources of information. Firstly, I located museum specimens in the Museu Paraense Emílio Goeldi (Belém, Brazil) and Smithsonian National Museum of Natural History (Washington, DC, USA). Secondly, during 1991–2007 field observations were made sporadically throughout eastern Amazonia and adjacent areas in Maranhão state by myself, other biologists, and/or knowledgeable local people. Biologists who contributed information had previous experience with carnivores. Information from knowledgeable local people was included only from those who made a precise morphological description followed by correct identification of plates or photographs and could provide information on bush dog biology (e.g. ‘the bush dog that hunts in packs pursuing paca, agouti and deer'). Thirdly, I reviewed the literature for additional locations. Where possible, estimated geographical coordinates were assigned to each reported location, and otherwise the municipal coordinates were used. However, the habitat described was always that of the observation location. For museum specimens habitat type was determined using Brazil's most recent vegetation map (IBGE, 1993) and was assumed to come from undisturbed areas.
The impact of six human activities and one natural effect on bush dogs was assessed (Table 1; Oliveira, 1998, 2007). Each impact was ranked as: high negative, low/moderate negative, no effect/not applicable, unknown, uncertain, and positive. To evaluate each impact factor, information on species biology and conservation (Oliveira, in press) were associated with data gathered in the states of Pará and Maranhão. These areas ranged from highly impacted to pristine, mostly within Amazonia but also in savannah.
Factors affecting bush dogs in northern Brazil (modified from Oliveira, 2007).
Results
Distribution
The distribution of bush dogs in northern Brazil is widespread but patchy. The majority of the 35 locations obtained were in eastern Amazonia, with a few in the Cerrado biome characteristic of central Brazil (Table 2). No records were found for the Parnaíba Delta region or the adjoining sand dune formations of Lençóis Maranhenses (north-eastern Maranhão). The species also appears to be absent from most of the floodplains of Baixada Maranhense. The Parnaíba River and the savannahs therefore appear to be the eastern limit of bush dog distribution in northern Brazil (Fig. 1), and thus the hypothesis that the bush dog is found throughout all of northern Brazil is refuted.
Location and habitat type for bush dogs in northern Brazil (Fig. 1).
1 Habitat was considered pristine unless noted otherwise
2 MPEG, Museu Paraense Emílio Goeldi, Belém, Brazil; USNM, Smithsonian National Museum of Natural History, Washington, DC, USA
Habitat association
The majority of records were from undisturbed lowland terra firme forest but also included pre-montane forest, savannah and disturbed areas (Table 2). Excluding museum localities, c. 43% of records were from impacted areas. In eastern Amazonia these included heavily logged and fragmented forest, Eucalyptus plantation, and cattle-pasture mosaic in Maranhão's Bico do Papagaio region (with one live-captured specimen) and heavily logged forest patches and pasture by the Capim River in Paragominas and Tomé Açu. In both areas pristine or well-preserved forests no longer exist in or around the vicinity, and thus the hypothesis that the bush dog is almost exclusively associated with conserved areas is refuted.
There were also records from babassu palm Orbignia phalerata forests (anthropogenic formations dominated by these palms). Records also exist in a late secondary forest/babassu palm forest area in a densely populated and disturbed region around Bacabal in central Maranhão, a disturbed secondary forest/babassu palm forest mosaic around Pirapemas and Conceição do Lago Açu, and a highly disturbed babassu palm forest in the Pindaré Indian Reserve. The observation in Papagaio was made in a disturbed deciduous forest, whereas in Mirador State Park, an area of moderate to highly disturbed savannah, a pack of bush dogs was seen using an armadillo burrow as a den for 2 years. These are the first reports of bush dogs using highly disturbed habitats.
In Maranhão bush dogs were absent from mangrove forests and coastal vegetation, as well as from most of the Baixada Maranhense floodplains. In the 1970s an experienced hunter reported bush dogs in the Nova Olinda area, which is located in the border area of the Amazonian rainforest and Baixada floodplains (a mosaic of Amazonian forest and seasonally flooded grasslands). Recent surveys found evidence of bush dogs in only one area in the floodplains region of Baixada Maranhense (R.R. Veloso Jr, pers. comm.).
Conservation issues
Bush dogs are rare throughout the region surveyed. Deforestation, and hence habitat loss (Oliveira, 1998, 2007) and anthropogenic impacts (infectious diseases from domestic dogs and hunting for prey) appear to be the main threats to the bush dog in the states of Pará and Maranhão (Table 1). Poaching and predator control to protect livestock does not seem to be a current threat. Neither commercial use nor use as pets was detected. There was a single instance of an individual killed, for no specific reason, after being detected by group vocalizations. Competition with other carnivores has a potential negative impact.
In northern Brazil bush dogs have been recorded in or adjacent to some protected areas (Arruda & Behr, Reference Arruda and Behr2002; Oliveira & Dalponte, in press). Of these the most important for bush dog conservation in the rainforest is the area around Serra dos Carajás (Fig. 1, location 9), totalling c. 27,280 km2, and the interconnected mega-reserves that form the Calha Norte corridor, totalling > 167,000 km2 (CI-Brasil, 2006), because of their size, good habitat quality, and low human pressure. In the savannah the area around Nascentes do Rio Parnaíba National Park (Fig. 1, locations 33 & 34), totalling c. 15,000 km2, appears to be the most important in the Cerrado.
On the northern savannahs the main areas for bush dog conservation are Mirador State Park (5,000 km2) and Nascentes do Rio Parnaíba National Park/Tibagi Ecological Station/Jalapão State Park, which forms a total protected area of c. 15,000 km2.
Discussion
Distribution and habitat association
The eastern limit of the bush dog's distribution in northern Brazil (Fig. 1) differs from previously published distribution maps (Ginsberg & Macdonald, Reference Ginsberg and Macdonald1990; Eisenberg & Redford, Reference Eisenberg and Redford1999), which often include the entire north-east of Brazil. No records or specimens have, however, ever been reported in the xeric north-east (Mares et al., Reference Mares, Willig and Lacher1985; Willig & Mares, Reference Willig and Mares1989). The absence of bush dogs from almost all of the floodplains of Baixada Maranhense contrasts with its occurrence in the floodplains of the Brazilian Pantanal (Oliveira, in press; Oliveira & Dalponte, in press). However, this absence could be a consequence of a long history of human occupation and subsequent habitat degradation and prey depletion.
In Venezuela bush dogs occur in tropical and pre-montane humid and very humid forests (Bisbal, Reference Bisbal, Redford and Eisenberg1989) and in Guyana the species' habitat range includes scrub forest, evergreen montane forest, scrub savannah and lowland rainforest (Barnett et al., Reference Barnett, Shapley and Engstrom2001). Emmons & Feer (Reference Emmons and Feer1997) stated that most bush dog records were for dry forests and rainforests near savannah. Langguth (Reference Langguth and Fox1975) considered the species primarily a forest dweller that visits open areas on the edge of forests. The species' habitat (consisting of open and closed vegetation) is similar in the Interior Atlantic Forest and Cerrado of eastern Paraguay (Zuercher & Villalba, Reference Zuercher and Villalba2002; Zuercher et al., Reference Zuercher, Gipson and Carrillo2005). Although undoubtedly associated with forests (Langguth, Reference Langguth and Fox1975; Bisbal, Reference Bisbal, Redford and Eisenberg1989; Dalponte, Reference Dalponte1995) bush dogs have been recorded in more open habitats in Brazil and Paraguay (Silveira et al., Reference Silveira, Jácomo, Rodrigues and Diniz-Filho1998; Zuercher & Villalba, Reference Zuercher and Villalba2002). Within the Cerrado biome in Brazil they have been found mostly in gallery forests (Dalponte, Reference Dalponte1995; Eisenberg & Redford, Reference Eisenberg and Redford1999) but also far from forest cover, in open woodland savannah (cerrado sensu stricto; Oliveira, 1996; Silveira et al., Reference Silveira, Jácomo, Rodrigues and Diniz-Filho1998). The species' association with watercourses suggested by some authors (Langguth, Reference Langguth and Fox1975; Strahl et al., Reference Strahl, Silva and Goldstein1992) appears to be correct for all reported records in northern Brazil. This is not surprising as the semi-webbed feet of bush dogs appear to be an adaptation for swimming and indicate that watercourses are not a barrier to movement (Strahl et al., Reference Strahl, Silva and Goldstein1992). However, there are also records of bush dogs far from watercourses (Silveira et al., Reference Silveira, Jácomo, Rodrigues and Diniz-Filho1998).
Although a recent survey obtained unconfirmed information about the species in the semi-arid thorny scrub of the caatinga (central Bahia state; C. Campos, pers. comm.) there are no other records of bush dogs in this biome (Mares et al., Reference Mares, Willig and Lacher1985; Willig & Mares, Reference Willig and Mares1989). The closest location to this semi-arid environment with confirmed records of bush dogs is Chapada Diamantina National Park, a mosaic of savannah, semi-arid scrub and deciduous forest in central Bahia (R. Leite, pers. comm.).
Conservation issues
The bush dog appears to be rare in northern Brazil, as it is across its entire range (Strahl et al., Reference Strahl, Silva and Goldstein1992; Zuercher et al., Reference Zuercher, Swarner, Silveira, Carrillo, Sillero-Zubiri, Hoffmann and Macdonald2004). Although no threats, with the possible exception of habitat encroachment, have been previously described for this canid (Ginsberg & Macdonald, Reference Ginsberg and Macdonald1990), exposure to infectious diseases from domestic dogs, as a result of human encroachment, could affect bush dogs because they appear to be highly susceptible (Oliveira, in press). Canine distemper virus, canine parvovirus and rabies can cause population declines and even local extinctions of wild canids and other carnivores (Funk et al., Reference Funk, Fiorello, Cleaveland, Gompper, Gittleman, Funk, Macdonald and Wayne2001). Such epidemics may have been responsible for the temporary disappearance of short-eared dog Atelocynus microtis during 1970–1987 in the Manu area of Peru (Leite-Pitman & Williams, Reference Leite-Pitman, Williams, Sillero-Zubiri, Hoffmann and Macdonald2004). Similarly, in the late 1980s in Mirador State Park, Brazil, an epidemic may have caused a population crash of crab-eating zorros Cerdocyon thous (Oliveira, 1996). Habitat alteration was originally thought to have a high negative impact on the bush dog (Oliveira, 1998) but the records presented here suggest the species is more resilient to human disturbances than previously thought.
Conservation implications of bush dog biology
Although knowledge of bush dog diet is largely anecdotal, they are considered highly carnivorous, with large rodents being their main prey. In bush dog scats from the dry season in eastern Paraguay 63% contained large rodents (Azara's agouti Dasyprocta azarae and paca Agouti paca) and 64% small mammals (Zuercher et al., Reference Zuercher, Gipson and Carrillo2005). In the savannahs of Mato Grosso, Brazil, a radio-tracked pack is preying heavily on armadillos Dasypus novemcinctus (E. Lima & J.C. Dalponte, pers. comm.). These findings support reports from local people about the bush dog's diet (Peres, Reference Peres1991; Oliveira, in press). Even larger prey, such as deer Mazama spp., capybara Hydrochaeris hydrochaeris and peccaries Tayassu spp. may be predated (Wallace et al., Reference Wallace, Painter and Saldania2002). There are observations of two dogs chasing black-rumped agouti Dasyprocta prymnolopha and paca, and a pack of six chasing and killing an adult paca (J. Silva Jr, pers. comm.; P. Dias, pers. comm.).
Large rodents and armadillos are important in the diets of jaguar Panthera onca, puma Puma concolor and ocelot Leopardus pardalis (Oliveira, 2002a; Moreno et al., Reference Moreno, Kays and Samudio2006; Oliveira et al., in press) and thus competitive intra-guild interactions could affect bush dogs. Prey availability may possibly be more important for long-term bush dog conservation than habitat integrity per se, as noted for other carnivores (Fuller & Sievert, Reference Fuller, Sievert, Gittleman, Funk, Macdonald and Wayne2001; Oliveira et al., in press). In Paraguay the mean weight of the vertebrate prey of bush dogs is 2.2 kg (Zuercher et al., Reference Zuercher, Gipson and Carrillo2005). This is c. 40% of the species' body mass, a unique feature for a c. 6 kg carnivore. The hyper-carnivorous diet of bush dogs therefore appears to be more similar to the diets of larger sympatric felids than to the diets of sympatric canids (short-eared dog, crab-eating zorro, maned wolf Chrysocyon brachyurus, and hoary fox Pseudalopex vetulus), which all have omnivorous diets. The preliminary minimum home range estimate for a radio-tracked bush dog pack is > 100 km2 (E. Lima & J. Dalponte, pers. comm.), which is large compared to that of hyper-carnivorous, equivalent-sized, Neotropical felids (Oliveira et al., in press). If such large home ranges are usual, then huge areas will be needed for long-term conservation of the bush dog.
Protected areas
Within the states of Amapá, Pará, Maranhão and northern Tocantins there are 18 protected national parks and strictly protected areas encompassing c. 145,056 km2 (> 477,000 km2 if protected areas that allow resource use, and indigenous lands, are included; IBAMA, 1995; CI-Brasil, 2006). However, bush dogs have been reported in only nine of these areas. Additionally, because the bush dog appears to be rare everywhere, it is unlikely that any of these areas, if isolated, could maintain viable populations in the long-term. However, the areas of Calha Norte, south-western Pará (Carajás) and the northern savannah conservation block, considered important for jaguar conservation because of their size and habitat integrity (Oliveira, 2002b), are important for bush dog conservation.
Protected areas large enough to maintain jaguars and pumas will probably not be able to support viable populations of a smaller competitor such as the bush dog (Woodroffe, Reference Woodroffe, Gittleman, Funk, Macdonald and Wayne2001; Oliveira et al., in press). The latter would have to range more widely to acquire the necessary resources and, thus, live at lower densities. Therefore no conservation units could maintain, if isolated, long-term viable populations of this canid.
Current conservation measures for bush dogs in Brazil exist solely on paper. They are protected by the native wildlife law and the threatened species law but no specific conservation action has ever been taken. The captive population in Brazil is small, with only 22 specimens in five institutions, and is not reproducing adequately (Ramos et al., 2003). Additional research on the species' ecological and conservation needs, especially those related to density and area requirements, associated with stronger environmental actions to guarantee the effective protection of reserves are needed to develop a conservation strategy for the species throughout Brazil. As there is insufficient information available on this naturally rare canid, integrated multidisciplinary studies on all aspects of the species’ natural history throughout its wide geographic range are required to develop a conservation action plan.
Acknowledgements
I greatly appreciate the invaluable comments on earlier versions of the manuscript by Karen DeMatteo, Gerald L. Zuercher, Flávio H.G. Rodrigues, Renata Leite-Pitman and two anonymous reviewers. I also thank the field information provided by Geraldo Sousa, José de Sousa e Silva Jr, Roberto Rodrigues Veloso Jr, Alexandre Caminha de Brito, Bernardo Britto and Paulo Adriano Dias, and Rogério Cunha de Paula for the map. Logistical support in several areas was provided by CENAP-ICMBio and Instituto Pró-Carnívoros.
Biographical sketch
Tadeu Gomes de Oliveira's main research interests are the ecology, conservation and natural history of Neotropical carnivores, especially felids and threatened species. Currently he is leading a country-wide multidisciplinary research project on the ecology and conservation of the six smallest Brazilian felids (ocelot, margay, little spotted cat, jaguarundi, pampas cat and Geoffroy's cat), ecological studies on other carnivore species (crab-eating zorro, crab-eating raccoon, otter), and investigating community composition of mammals in northern Brazil both in the Amazon and savannahs. He is also involved in reintroduction, status assessment and conservation action planning for threatened species.
