New record of giant anteater Myrmecophaga tridactyla ( Pilosa , Myrmecophagidae ) in Northeast Brazil

The giant anteater (Myrmecophaga tridactyla) is the largest living anteater, which due to several anthropic impacts, is threatened with extinction. So far, there was only one locality with a confirmed record of M. tridactyla in Northeast of Brazil. We present a new direct record of the species in Brazilian Northeast, registered in July 2017 by camera trap, in an arboreal caatinga area, municipality of Sento Sé, Bahia. This record is the second one of the species in the Caatinga Biome and confirms the occurrence of M. tridactyla in the state of Bahia. It constitutes the first direct record of M. tridactyla in more than 13 years of monitoring in the study area, suggesting that the species is locally rare.


Introduction
The family Myrmecophagidae is composed of medium and large mammals with modern representatives divided into two genera, Myrmecophaga and Tamandua.Both Tamandua tetradactyla (Linnaeus 1758) and Myrmecophaga tridactyla (Linnaeus 1758) occur in Brazil (Gardner, 2007;Medri et al. 2011;Gaudin et al. 2018).Popularly known as the Giant anteater, M. tridactyla is the largest living anteater, weighing over 40 kg (Medri et al. 2011;Miranda et al. 2015).It is usually generalist in habitat use, occupying the Brazilian savanna (Cerrado biome), wetlands (Pantanal biome), forest patches, dry forest, and grasslands (Miranda et al. 2014;Gaudin et al. 2018).A population loss of at least 30% over the past 10 years has been estimated based on local extinctions, habitat loss, and deaths caused by fires and road kills.Based on this decline and past threats that are still ongoing today, it is likely that the population has suffered an overall reduction in population size of >30% over the last three generations (suspected to be around 21 years).Because of the real threats to this species and the noticeable declines, a precautionary assessment of Vulnerable A2cd is given (Miranda et al. 2014;MMA, 2014;Miranda et al. 2015).
The species is distributed from Central America to northern Argentina (Gardner, 2007).In Brazil, it occurs in all biomes, but in the Pampa is probably extinct and in the Caatinga there is a single confirmed record (Miranda et al. 2015).The Caatinga is a seasonally dry tropical forest that extends over a large part of South America.It is an exclusively Brazilian biome and covers approximately 11% of the country's territory, straddles all states of the Northeast region (Gariglio et al. 2010).The first record of giant anteater in the Caatinga was obtained in Serra da Capivara National Park (SCNP) where a skull was found in a hunting camp in 1991 (Olmos, 1995).The mention of the occurrence of M. tridactyla in northeastern Brazil occurred in the mid-XVII century.The german naturalist George Marcgravi was the first to describe and illustrate a giant anteater in his work entitled Historiae Naturalis Brasiliae (Marcgravi, 1648).
Monteiro da Cruz et al. (2002) cite the occurrence of M. tridactyla in six sites in the Pernambuco State, including the Serra Negra Biological Reserve, Timbaúba, Custódia, Sítio dos Moreiras, Igarassu and Água Preta, but they do not describe how records were obtained.Later, the presence of the species in the SCNP was confirmed by records in camera traps (Perez, 2008).The species was recorded in Chapada Diamantina National Park (Pereira and Geise, 2009) and in a locality in Paraíba (Feijó and Langguth, 2013) by interviews.The only documented record in state of Ceará comes from a skin from Parambu municipality, southwest of the state (Feijó and Langguth, 2013).Thus, except of the direct record of Peres ( 2008), records of M. tridactyla are anecdotal in the Brazilian Caatinga biome.Here we report a new record of M. tridactyla in the state of Bahia, including undoubtful images of it.
The field study was developed in the region of Boqueirão da Onça (Figure 1), north of the state of Bahia.The study area has approximately 900,000 hectares, extending over the municipalities of Sento Sé, Umburanas, Campo Formoso, Juazeiro and Sobradinho, northern region of state of Bahia (Fukuda et al. 2010).This region is classified by the Brazilian Ministry of the Environment as extremely important for the conservation of biodiversity (MMA, 2016).In addition, during the study, the area was included in a new Protect Area, the Boqueirão da Onça National Park, proposed by the Brazilian Ministry of Environment.
The climate in the region is semi-arid with an average annual precipitation of 693 mm.The landscape is heterogeneous and includes several habitats such as "arboreal caatinga", "valleys and plateaus" (Dias et al. 2019).We carried out a research with 60 camera-traps (Bushnell and Acorn Ltl-5210ª) between January and July of 2017 to estimate the occupancy patterns of medium and large-sized mammals in the area (see Dias et al. 2019).Cameras were always installed on trails and roads, with a minimum distance of 1.5 km between stations.In addition, cameras were to 40 cm above the ground in a tree, and in areas most likely to be used by mammals.
With a total effort of 8,570 traps-nights, covering an area of 535 km 2 (Minimum Convex Polygon of the cameras), we obtained 2,839 records of 21 species of wild mammals.On July 3, 2017 at 11:25 am M. tridactyla was filmed (Supplementary file) at a ranch located at coordinates 9°55'47.29"S;41°3'29.83"W,6 km from the village São Pedro in the municipality of Sento Sé.The phytophysiognomy of the area where we obtained the record is composed by arboreal caatinga, at 880 m of altitude.Although water is a scarce resource in the region, there are two perennial water bodies about 2 km from the site where M. tridactyla was recorded (Figure 1).
To our knowledge, this is the first direct record of M. tridactyla confirmed for the state of Bahia and the second for Northeast Brazil.Even though this record does not expand considerably the range of M. tridactyla, especially regarding its entire distribution, it does extend its range in Northeast Brazil in about 300 km southeast of the area where there are recent records of the species (SCNP).
Our record confirms the presence of M. tridactyla in Boqueirão da Onça.Until now, there were only fossil records obtained in the Toca da Boa Vista cave (Cartelle and Hartwig, 1996; Marine Science Institute, UCSB) and reports of hunters about the occurrence of the species.However, this unique recent record of M. tridactyla in the study area despite the great camera-trap effort, is a convincing evidence of its rarity in the biome.Camera traps studies at Boqueirão da Onça have been carried out since 2006, initially by the National Research Center for Carnivore Conservation (CENAP-ICMBio) followed by the Institute for the Conservation of Neotropical Carnivores (Pró-Carnívoros Institute) and only now the species was recorded.Although M. tridactyla has some tolerance to human disturbed areas it generally avoids areas with high levels of contact with humans, cattle and other domestic animals (Shaw et al. 1987).The presence of domestic dogs, for example, is a potential threat.The incidence of dog attacks may reduce the probability of M. tridactyla occurrence and even cause its population decline (Lacerda et al. 2009).In the region of Boqueirão da Onça a large number of dogs is found in the villages near the natural areas and it is common that they make incursions into the forest areas (Dias et al. 2019).This situation is unsettling, since these animals have hunting skills and are usually bred free.In addition, the growing establishment of wind farms in the study area has increased the number of new roads and trails in formerly remote sites (Dias et al. 2019).This has made it easier for hunters, dogs and other domestic animals to access natural habitats, notably threatening the species with great territorial requirements and sensitive to human presence.
Although anthropogenic impacts may threaten the persistence of M. tridactyla, the rarity of this species in the Caatinga may be related to historical and physiological factors.Its diet based strictly on prey with low calorie content, makes M. tridactyla distinct in its physiology with a lower body temperature and lower metabolism when compared with other mammals of similar body mass (McNab, 1984).Furthermore, its long coarse fur coat and large hairy tail provide them effective insulation.Thus, its minimal thermal conductance is 94% of what is expected for the body mass (McNab, 1984).This low value of minimal thermal conductance, together with large body mass, allows M. tridactyla to have a very wide region of thermoneutrality, between 15 °C and 36 °C, for an ant-eating specialist (McNab, 1984;Gaudin et al. 2018).
However, the annual average temperatures in the Caatinga range between 25 °C and 30 °C (Silva et al. 2017).In the dry months the absolute maximum temperatures exceed 40 °C (Prado, 2003), exceeding the upper limit of the thermoneutrality of M. tridactyla.Additionally, portions of the inland dry regions of the biome receive less than 600 mm of rainfall annually (Silva et al. 2017).The number of dry months increases from the edges to the core of the region, with some areas experiencing periods of 7-10 months without water availability for plants, further reducing canopy cover (Prado, 2003).
Taking into account the physiological peculiarities of M. tridactyla and its responses at ambient temperature (Medri and Mourão, 2005), it is presumed that the survival of this species in the Caatinga is a great challenge considering the extreme environmental conditions in this biome.Thus, it is intriguing that some populations of M. tridactyla persist in an environment so adverse as the Caatinga.There is no evidence of physiological adaptations in mammals in the Caatinga related directly to the scarcity of water, although many species may adapt to this condition behaviorally (Carmingnotto and Astúa, 2017).In this sense, the need for water or how much M. tridactyla is physiologically adapted to the water deficit of the Caatinga deserves to be investigated, as well as its behavioral strategies in this biome.
With the creation of Boqueirão da Onça National Park, we expect better monitoring by environmental agencies, since M. tridactyla and other endangered species continue to be exposed to a series of impacts and anthropogenic pressures in the region.Our record expands the knowledge of the Caatinga mammalian fauna and the distribution of M. tridactyla, especially considering that the Boqueirão da Onça region is at the limit of the distribution of the species (Miranda et al. 2015).We also highlight the local rarity of this mammal, based on the low frequency of detection, since a single record occurred in more than 13 years of camera-trap monitoring in the region, including the present study.In this way, other species of common mammals of the Cerrado, which may also have restricted distributions in the Caatinga, should have their occurrence in this biome investigated.

Figure 1 .
Figure 1.Study area and records of Myrmecophaga tridactyla in Northeast Brazil.