Introduction
The marsh deer Blastocerus dichotomus is the largest South American deer, weighing up to 125 kg and reaching 1.2 m at the shoulder (Pinder & Grosse, Reference Pinder and Grosse1991; Salazar-Bravo et al., Reference Salazar-Bravo, Tarifa, Aguirre, Yensen and Yates2003). Some particular anatomical characteristics of the marsh deer, such as the presence of an interdigital membrane, elongated hooves and relatively long limbs, are adaptations to marshy and flooded environments (Tomas et al., Reference Tomas, Beccaceci and Pinder1997).
This deer appears to be a generalist in its use of open habitats and a specialist in terms of water depth, preferring to forage in inundated areas with a depth of c. 0.7 m (Mauro et al., Reference Mauro, Mourão, Silva, Coutinho, Tomas and Magnusson1995), although it has been suggested that the selection and use of habitat by marsh deer is determined mainly by its diet (Tomas et al., Reference Tomas, Beccaceci and Pinder1997; Tomas & Salis, Reference Tomas and Salis2000). The species is restricted to humid areas, originally occuring in several types of wetland in Argentina, Bolivia, Brazil, Paraguay, Peru and Uruguay, but its distribution has been severely reduced (Pinder & Grosse, Reference Pinder and Grosse1991; Tomas et al., Reference Tomas, Beccaceci and Pinder1997). Because of the reduction in its population and habitat loss the marsh deer is listed on CITES Appendix 1 and is categorized as Vulnerable on the IUCN Red List (Pinder & Grosse, Reference Pinder and Grosse1991; Wemmer, Reference Wemmer1998; Duarte et al., Reference Duarte, Varela, Piovezan, Beccaceci and Garcia2008; Ríos-Uzeda & Ayala, Reference Ríos-Uzeda and Ayala2009). Its biology remains largely unknown (Tomas et al., Reference Tomas, Beccaceci and Pinder1997) and there is a lack of information about the distribution and conservation status of the species at a continental scale (Wemmer, Reference Wemmer1998).
The Bolivian savannahs are one of the three largest flooded savannah systems in South America (Hamilton et al., Reference Hamilton, Sippel and Melack2002, Reference Hamilton, Sippel and Melack2004). The other two large wetlands are the comparatively better known Brazilian Pantanal and the Llanos of Orinoco in Venezuela. Marsh deer do not occur in northern South America (Eisenberg, Reference Eisenberg1989) but the white-tailed deer Odoicoleus virginianus is present in the Llanos. The Pantanal probably holds the largest marsh deer population (Mourão et al., Reference Mourão, Coutinho, Mauro, Campos, Tomás and Magnusson2000). Unlike the better known Pantanal and Orinoco savannah, the Bolivian savannahs have received little scientific attention because of difficulties of access and geographical isolation (Haase & Beck, Reference Haase and Beck1989; Hanagarth, Reference Hanagarth1993; Langstroth, Reference Langstroth1999).
Although large areas of the Bolivian savannahs do not have any detectable human activity, cattle ranching is the principal economic activity in the region (Hanagath, Reference Hanagarth1993; Langstroth, Reference Langstroth1999). In contrast to other Neotropical floodplains, which are known to harbour marsh deer populations in areas with considerable habitat alteration, as in the floodplains of the Paraná River (Pinder, Reference Pinder1996; Piovezan, Reference Piovezan2004) and the Brazilian Pantanal (Silva et al., Reference Silva, Mauro, Mourão and Coutinho1999), large portions of the Bolivian savannahs are almost pristine. However, no large-scale assessment of the marsh deer population of Bolivia has been carried out (Tomas et al., Reference Tomas, Beccaceci and Pinder1997; Wemmer, Reference Wemmer1998; Rumiz, Reference Rumiz2002). Subsistence hunting by indigenous people in the absence of any management programme, poaching and diseases of cattle are the main threats to the marsh deer in this area (Rumiz, Reference Rumiz2002; Ríos-Uzeda & Ayala, Reference Ríos-Uzeda and Ayala2009). The aim of this study was to estimate the population size of the marsh deer in three areas of the northern Bolivian savannahs and to evaluate the importance of these areas for the conservation of the species.
Study area
Bolivia's northern savannahs (Fig. 1) are known as the Llanos de Moxos, a series of floodplains in the Amazon lowland basin of Bolivia comprising mainly open, wet savannah (Langstroth, Reference Langstroth1999), drained by the headwaters of the Madeira River (Hamilton et al., Reference Hamilton, Sippel and Melack2002). The area of these savannahs is c. 150,000 km2 and the core area is bordered by the Beni, Mamoré and Iténez rivers. Mean annual rainfall is 1,300–2,000 mm, falling mostly in December–March (Hamilton et al., Reference Hamilton, Sippel and Melack2004). Mean annual temperature is 25.9°C in northern La Paz, 26.8°C in northern Beni (Haase & Beck, Reference Haase and Beck1989) and 27°C in central Beni (Hanagarth, Reference Hanagarth1993). The mean altitude is c. 150–160 m, ranging from 135 m in the north-east to 210 m in southern Chapare (Langstroth, Reference Langstroth1999). The three survey areas were the northern La Paz savannahs in the western Beni region, the Mamoré savannahs in the central Beni region, and the Iténez savannahs in the Baures subregion in the eastern Beni region (Fig. 1).
Fig. 1 The savannahs of northern Bolivia, indicating the locations of the three sites (northern La Paz, Mamoré and Iténez) surveyed for the marsh deer Blastocerus dichotomus. The numbers indicate the 11 survey blocks (see Table 1 for further details). The shaded rectangle on the inset indicates the location of the main map in northern Bolivia.
Methods
We conducted aerial surveys during the dry season of 2007 (May–August): in the northern La Paz savannahs during 7–12 May, the Mamoré savannahs during 23–24 June, and the Iténez savannahs during 1–4 August. We counted marsh deer from a Cessna 206 aeroplane flying at 200 km h−1 and 60 m above the ground. The team for each survey consisted of the pilot, a navigator and four observers, two on each side of the aeroplane. We counted the deer in 200-m wide transects delimited by a pair of rods fixed on the wing struts (Bayliss & Yeomans, Reference Bayliss and Yeomans1989; Mourão et al., Reference Mourão, Coutinho, Mauro, Campos, Tomás and Magnusson2000).
A total of 101 transects of unequal sizes were systematically distributed 5 or 10 km apart in 11 blocks with areas of 1,550–3,511 km2: five blocks in the La Paz region, two in the Mamoré region and four in the Iténez region (Table 1). All except one block were surveyed in the morning. Sampling intensity was defined as the ratio of the area sampled (i.e. the sum of the areas of the strip transects) and the total area surveyed (Table 1). Counts were tallied at the end of each unit of 1 minute of flight (3.3 km of transect).
Table 1 Estimates of density and abundance of marsh deer Blastocerus dichotomus in 11 sampling blocks in three regions: northern La Paz, Mamoré and Iténez (Fig. 1).
Because aerial counts are known to be negatively biased (Caughley, Reference Caughley1977) we used the double-count method to improve the accuracy of counts on both sides of the aeroplane (Caughley & Grice, Reference Caughley and Grice1982; Bayliss & Yeomans, Reference Bayliss and Yeomans1989; Graham & Bell, Reference Graham and Bell1989; Sinclair et al., Reference Sinclair, Fryxell and Caughley2006). The two observers on the same side of the aeroplane independently counted the animals in the same transect. Thus, by assessing the number of animals sighted by observer 1 and missed by observer 2 (S 1), the number of animals sighted by observer 2 and missed by observer 1 (S 2), and the number of animals sighted by both observers (B), it is possible to estimate the probability (P) of observers sighting an animal in a transect as follows:
and the multiplicative correction factor (CF) applied to the number of animals sighted by the observers is:
As in most studies using this method (e.g. Caughley & Grice, Reference Caughley and Grice1982; Bayliss & Yeomans, Reference Bayliss and Yeomans1989; Mourão et al., Reference Mourão, Coutinho, Mauro, Campos, Tomás and Magnusson2000) we used the counting unit to define whether an animal was seen by one or both observers. We then compared the corrected counts between the two teams of observers (i.e. the two sides of the aeroplane) by transects and the three surveyed regions using an ANOVA with repeated measures (using SYSTAT v. 11; Systat, Chicago, USA). If the corrected counts by regions did not differ between sides of the aeroplane and the corrected counts by side did not interact with regions we then pooled the corrected counts of both sides of the aeroplane to estimate marsh deer abundance, density and standard errors for blocks, regions and total area. We estimated these parameters using the equations provided by Sinclair et al. (Reference Sinclair, Fryxell and Caughley2006) for sample units of different sizes and without replication, and used a one-factor ANOVA to examine differences in densities between the three surveyed areas.
In addition, we estimated the abundance and associated standard errors for the entire survey area, and how many years of monitoring would be required to obtain sufficient power to detect decreases in numbers over the entire area (Gerrodette, Reference Gerrodette1987, Reference Gerrodette1993). For these analyses we assumed that the marsh deer follows an exponential growth model and that the coefficient of variation is proportional to the inverse of the square root of the estimate, which is expected when the samples are strip transects (Marsh, Reference Marsh, O'Shea, Ackermann and Percival1995).
Results
We counted a total of 159 marsh deer, 86 in the La Paz region, 31 in Mamoré and 42 in Iténez. We were only able to determine the sex and age of deer in < 10% of observations, mostly solitary animals. Only 23 observations (19%) consisted of groups of two or more animals. The observers on the right side of the aeroplane missed fewer animals than those on the left side, although both sides consistently missed more animals in the Iténez region than in La Paz, and more in La Paz than in Mamoré. The probabilities of observers sighting marsh deer were sufficiently large (i.e. > 0.45) to provide valid estimates (Potvin et al., Reference Potvin, Breton and Rivest2004; Potvin & Breton, Reference Potvin and Breton2005) and therefore we applied the double-count method to improve the accuracy of the counts. The resulting correction factors were 1.03–1.94. The corrected counts by transects did not differ between sides of the aeroplane (F 1,98=0.204, P=0.653) nor did they interact with the blocks (F 2,98=1.275, P=0.284). We therefore pooled the corrected counts from both sides of the aeroplane to estimate the density of the marsh deer.
The corrected, estimated density of marsh deer was 0.24±SE 0.03 km−2 in northern La Paz, 0.12 km−2±SE 0.03 in the Mamoré region and 0.15 km−2±SE 0.03 in the Iténez region. These estimates did not differ significantly between regions (F 2,8=1.27, P=0.33). Block 4 in La Paz had the highest density of marsh deer and Block 6 in the Mamoré region the lowest (Table 1).
Corrected, estimated total abundance was c. 5,000 marsh deer for the three areas combined (Table 1). The power analyses suggested that maintaining the overall sampling intensity at 5% we would need eight or five surveys (i.e. years) to detect a decrease of 5 or 10%, respectively, in corrected marsh deer abundance but that a decrease of 30% could be detected by just two surveys.
Discussion
Aerial surveys
Only one aerial survey of marsh deer had been carried out previously in Bolivia, in a 820-km2 area in the northern La Paz Department in May 2004 (H. Gomez & B. Ríos-Uzeda, pers. obs). Other data on marsh deer in Bolivia are restricted to presence/absence data (Tarifa, Reference Tarifa, Ergueta and de Morales1996; Townsend, Reference Townsend1996; Anderson, Reference Anderson1997), without ecological information (Tarifa, Reference Tarifa, Ergueta and de Morales1996; Rumiz, Reference Rumiz2002). Bolivia's northern savannahs are the north-western limit of the marsh deer's range (Pinder & Grosse, Reference Pinder and Grosse1991; Tomas et al., Reference Tomas, Beccaceci and Pinder1997). Our estimated densities were lower than those reported for the wet savannahs in the centre of the species' historical range but higher than those from its southern geographical limit. In the Brazilian Pantanal estimates range from 0.09 km−2 (Mauro, Reference Mauro1993) to 0.98 km−2 (Mourão et al., Reference Mourão, Coutinho, Mauro, Campos, Tomás and Magnusson2000). Tomas et al. (Reference Tomas, Salis, Silva and Mourão2001) found that local density changed little across seasons, from 0.382 km−2 during the dry season to 0.395 km−2 during the wet season, but that floods strongly affected marsh deer distribution. Three independent surveys carried out in the same floodplain area of the Paraná River reported similar densities (0.51 km−2, Mourão & Campos, Reference Mourão and Campos1995; 0.48–0.53 km−2, Pinder, Reference Pinder1996; 0.49 km−2, Andriolo et al., Reference Andriolo, Piovezan, Paranhos da Costa and Duarte2005), despite using different methods to correct for visibility bias, including line transects (Pinder, Reference Pinder1996; Andriolo et al., Reference Andriolo, Piovezan, Paranhos da Costa and Duarte2005) and the double-count method (Mourão & Campos, Reference Mourão and Campos1995; Pinder, Reference Pinder1996). A relatively low density of 0.09 km−2 was found in the Natural Reserve of Iberá, Argentina, near the southern limit of the species' range (Beccaceci, Reference Beccaceci1994).
The highest density of marsh deer that we recorded was in the northern La Paz Department, the extreme north-west limit of the species in South America. This relatively high density may be explained by the low human population density in this area (Haase & Beck, Reference Haase and Beck1989; Hanagarth, Reference Hanagarth1993) and because the savannah in this area is relatively well conserved and has a higher percentage of open humid savannah than the Mamoré and Iténez regions. Overall, the survey blocks with the lowest densities were drier or have large extensions of woody savannah. The marsh deer has a similar distribution pattern in the Brazilian Pantanal (Mauro, Reference Mauro1993).
The estimated abundance of marsh deer in the three surveyed areas, totalling 27,700 km2, was c. 5,000. Although the accuracy of the counts was corrected this is still a conservative estimate. Because we used units of 1 minute of flight to determine whether both observers counted the same individuals it is possible that different deer might have been assigned as the same and we may thus have underestimated the correction factor (Mourão et al., Reference Mourão, Coutinho, Mauro, Campos, Tomás and Magnusson2000; Sinclair et al., Reference Sinclair, Fryxell and Caughley2006). We have not attempted to extrapolate our estimates to the whole area covered by Bolivia's northern savannahs because the areas we surveyed may be those most suitable for the marsh deer.
Management implications
The northern savannahs of Bolivia are remote, difficult to access and generally still pristine, although we observed moderate cattle-raising activities. The population of marsh deer in this region is of considerable importance, in particular because the main known refuge of the marsh deer, the Brazilian Pantanal, is threatened by large-scale deforestation and human alterations of the flood pulse. It has been estimated that >40% of the forest and savannah habitats of the Pantanal have been altered for cattle ranching through the introduction of exotic grasses (Harris et al., Reference Harris, Tomas, Mourão, Silva, Guimarães, Sonoda and Fachim2005), and > 100 small hydroelectric dams are being constructed or are planned. Besides their importance for marsh deer conservation the enclaves of savannah in the Bolivian Amazon need to be conserved to protect landscape diversity. We recommend the creation of protected areas in these savannahs, wildlife and domestic health programmes to assess the potential transmission of diseases, and a participative management programme, involving indigenous and other local people, to ensure that marsh deer harvests are sustainable.
The results of this study provide baseline estimates of density and abundance of the marsh deer in the areas surveyed, and demonstrate that an annual monitoring programme for the species is feasible. The next step will be to work with national and local authorities to establish a management programme for the marsh deer in the Bolivian savannahs.
Acknowledgements
This work was made possible by funding from the Russell E. Train Education for Nature Program (WWF), Amazon–Andes Conservation Program (Wildlife Conservation Society, WCS) and the Greater Madidi–Tambopata Landscape Conservation Program, Bolivia (WCS) through a grant from the Gordon and Betty Moore Foundation, the Werner Hanagart Fellowship (Puma Foundation of Bolivia), and WWF–Bolivia through the Foundation of the Noel Kempff Mercado Museum. Claudia Venegas, Diego Romero, Guido Ayala, Freddy Zenteno, Jhonny Ayala, Marcos Teran and Rosario Arispe were the field team in Bolivia and WCS–Bolivia helped with spatial analyses. We are indebted to Walfrido Tomas at Embrapa Pantanal and to Humberto Gómez, Alfonso Llobet, Damián Rumiz, Rob Wallace and an anonymous referee for their comments and suggestions.
Biographical sketches
BorisRios-Uzeda is interested in the ecology and conservation of large neotropical vertebrates such as the Andean condor, Andean bear and marsh deer. For more than 6 years he studied habitat use by these species, and estimated their populations, for the Wildlife Conservation Society in the Madidi region of Bolivia. He is also interested in wildlife management, especially for local communities in lowland Amazonia. He is now working on conservation issues at a national scale. GuilhermeMourão carries out research for the Wildlife Laboratory at Embrapa Corumba in the Brazilian Pantanal. He is currently studying the ecology of large- and medium-sized vertebrates such as the jaguar, ocelot, coati, tapir, caiman, giant otter, pampas deer and marsh deer in this unique ecosystem.
