MATERIALS AND METHODS

Study area. The study was performed in a cattle ranch of the Humid Chaco Ecoregion in Paraguay (Fig. 1). The property is located in the floodplain of the Paraguay River and is mainly dedicated to extensive free-range cattle ranching since at least 1904, however, no evidence of drastic forest clearings was found in the last 114 years (visual comparative of a drawn map from 1904 signed by E. Dominguez and vegetation map elaborated by Z. El Raiss), maintaining its original vegetation cover, except for selective extraction of wood used for cattle ranching infrastructure (i.e., cabin construction, fencing and bridges mostly from Schinopsis balansae Engler, Copernicia alba Morong and Prosopis spp.) (^{Laino et al., 2017}). Predominant ecosystems of the area include wetlands and natural vegetation formations conditioned by topography and frequent flooding (^{Ginzburg & Adamoli, 2006}) creating a mosaic of subtropical forests, grasslands and marshes (^{Mereles et al., 2013}). Rainfall averages 1,200 mm per year, and the temperature means 15°C in the coldest periods (June-August) and 28°C in the hottest months (December-February) (^{Mereles et al., 2013}; ^{DMH, 2018}). The total ranch area is 4,000 ha, however the sampling site covered 500 ha non-randomly selected according to accessibility and flooding conditions during the time of the sampling.

Fig. 1. Location of the study area in the Humid Chaco Ecoregion in Paraguay (left) and camera-trap ubications from November 2016 to March 2018. The numbers of the amplified area (right) indicate the date and season in which the trap cameras were placed in the different forests types (see Tab. I). 

The study was conducted in three vegetation types: i) Riparian forests associated to wetlands (W-RF), ii) Mesoxerophytic semi-deciduous forests dominated by Schinopsis balansae (MXF), and iii) Floodable sub-humid forest islets (FSF) (Fig. 1). Wetlands are low floodable areas which vary with the rainy season, where vegetation is represented by emergent stands of Typha, Cyperus and Thalia; in open waters, also including floating stands of Pistia, Eichornia, Victoria among others (^{Peña-Chocarro et al., 2006}). W-RF in our study site are usually associated to a ~50-100 m riparian forest strip linked to periods of flooding (^{Maturo et al., 2005}; ^{Peña-Chocarro et al., 2006}); common tree species for our study site are Peltophorum dubium (Spreng.) Taub., Ocotea diospyrifolia (Meisn.) Mez, Nectandra angustifolia (Schrad.) Nees, Inga vera Willd, and Genipa americana L., with lower presence of Vitex megapotamica (Spreng.) Moldenke and Terminalia trifolia Spreng. MXF or quebrachales are dominated by Schinopsis balansae and Libidibia paraguariensis (D. Parodi) Burkart and occasionally Aspidosperma quebracho-blanco Schltdl. (^{Mereles, 2005}; ^{Peña-Chocarro et al., 2006}). FSF are present in the Paraguay River floodplain and are associated with palm groves of Copernicia alba (^{Perez de Molas, 2016}). Some tree species of the FSF are common with the riparian forest, however, these forests occur in well-defined islets, usually surrounded by savannas rather than following the course of streams or wetlands; some species common to this type of forest and our study site include: Peltophorum dubium, Enterolobium contortisiliquum (Vell.) Morong, Ficus enormis (Miq.) Miq., Ocotea diospyrifolia, Sapium haematospermum Müll.Arg., Gleditsia amorphoides (Griseb.) Taub., Guazuma ulmifolia Lam., Chloroleucon tenuiflorum (Benth.) Barneby & J.W.Grimes, Handroanthus heptaphyllus (Vell.) Mattos, Syagrus romanzoffiana (Cham.) Glassman and Copernicia alba.

Methods. We used five Bushnell Trophy Cam HD Essential camera-traps from November 2016 to March 2018. Cameras were installed 45 cm above the ground and were programmed to operate 24h00 per day, reaching a total sampling effort of 1,268 camera-days. Camera-traps were rotated in the three forest types previously described: i) Riparian forests associated to wetlands (W-RF), ii) Mesoxerophytic semi-deciduous forests dominated by Schinopsis balansae (MXF), and iii) Floodable sub-humid forest islets (FSF) (Tab. I, Fig. 1). Cameras were rotated to standardize sampling efforts across habitat types.

Photographs and videos taken by camera-traps were considered records (see two records of this research in Figs 2, 3). Only the first record was considered when more than one photograph or video of the same species was taken at the same camera-trap within a 1 hr interval. Between 1 and 21 photos and 0 and 3 videos were obtained for each record for this study. Sampling effort and capture success were calculated according to ^{Srbek-Araujo & Garcia Chiarello (2005}) (Tab. II). Social behavior was described through the patterns of activity and number of individuals in each record.

Figs 2, 3. Photos taken by trap cameras in the Humid Chaco Ecoregion in Paraguay: 2) Giant anteater (Myrmecophaga tridactyla Linnaeus, 1758) on March 20th, 2017; 3) Lesser anteater (Tamandua tetradactyla Linnaeus, 1758) on November 28th, 2017. 

RESULTS

Habitat preference. Mean capture success for T. tetradactyla was 0.7% and 1.3% for M. tridactyla (Fig. 4). In both species, capture success was greater in Floodable sub-humid forest islets (FSF). T. tetradactylaappeared more frequently in FSF (1.2%), followed by Mesoxerophytic semi-deciduous forests dominated by Schinopsis balansae (MXF) and Riparian forests associated to wetlands (W-RF), with 0.7% and 0.2%, respectively. While, M. tridactyla capture success was greater in FSF (2.3%), followed by W-RF (1.2%) and MXF (0.5%).

Fig. 4. Capture success (%) of lesser anteater (Tamandua tetradactyla Linnaeus, 1758) and giant anteater (Myrmecophaga tridactyla Linnaeus, 1758) in the Humid Chaco Ecoregion in Paraguay using trap-cameras from November 2016 to March 2018 by forest types: W-RF, Riparian forests associated to wetlands; MXF, Mesoxerophytic semi-deciduous forests dominated by Schinopsis balansae; FSF, Floodable sub-humid forest islets. 

Social behavior. Most detections consisted of individual anteaters for both species (Figs 2, 3), for M. tridactyla, 88% (n=15) records were of solitary giant anteaters and 12% (n=2) were mother-young pairs; juvenile giant anteaters transported on their mother’s back were observed only during summer (December 2016 and November 2017). For T. tetradactyla, 89% (n=8) of the records were of solitary individuals, while only one detection included a female with offspring, observed in November 2017.

Activity patterns. Both species showed a pattern of crepuscular and nocturnal activity with a peak of records around midnight (Fig. 5). M. tridactyla was recorded between 17h00 and 09h00, with the highest frequency of detection between 21h00 and 01h00 (58.8%). Meanwhile, T. tetradactyla was recorded between 18h00 and 02h00, with the highest period of activity between 22h00 and 01h00 (55.4%). M. tridactyla was always detected between 11°C and 26°C, while T. tetradactyla was always detected between 15°C and 23°C.

Fig. 5. Records (%) by hour of the day of giant anteater (Myrmecophaga tridactyla Linnaeus, 1758) and lesser anteater (Tamandua tetradactyla Linnaeus, 1758) in the Humid Chaco Ecoregion in Paraguay using trap-cameras from November 2016 to March 2018. 

Both species capture success was greater during spring time: 2% for M. tridactyla and 1.2% for T. tetradactyla (Tab. II), however, it should be noted that sampling was not evenly distributed for all seasons in all vegetation types due to floods caused by heavy rain. Sampling was conducted in all seasons of the year for FSF, in spring and summer for W-RF, and in autumn, winter and summer for MXF (Tab. I).

DISCUSSION

Our results showed a preference of anteaters for the Floodable sub-humid forest islets (FSF), however, both species also appeared in other forest types. At a continental scale, giant anteaters are more frequently recorded in dry forests than in moist forests (^{Quiroga et al., 2016}). Lesser anteaters are climbers and inhabit mainly forested environments and giant anteaters live in forested areas and in open areas, where they are more abundant due to their limited ability to climb (^{Rodrigues et al., 2008}). However, a study carried out in the central region of the Pantanal (Brazil) reported the highest densities of M. tridactyla and T. tetradactyla in forest landscapes compared to open grasslands and scrubs, where they also were detected (^{Desbiez & Medri, 2010}).

Our sampling site covered 500 ha in three forest types, grasslands and shrublands were not considered for this study. Studied forests islets are immersed in flood-prone savannas, however, camera-traps were only placed inside arboreal vegetation. Anteaters generally use a mosaic of habitats (e.g., forest islets for shelter and rest and savannas for foraging and daytime rest) (^{Desbiez & Medri, 2010}; ^{Quiroga et al., 2016}), therefore, we recommend further research that also includes other plant formations. Size and shape of forest islets were not considered in this study because of their variability, while FSFs and the MXFs are larger and develop naturally in circular, oval or irregular shapes in slightly elevated areas of the floodplain; W-RFs are sinuous formations extending along wetlands and rivers.

Both species were usually detected alone, but occasionally females were observed carrying pups on their back, as reported by ^{Desbiez & Medri (2010}), ^{Figel et al. (2015}) and ^{Passos et al. (2016}). Anteaters are usually nocturnal, although they occasionally engage in diurnal activity (^{Rodrigues et al., 2008}). According to our results, both species showed a pattern of crepuscular and nocturnal activity with a peak of records around midnight. Giant and lesser anteaters display both nocturnal and diurnal activity as part of a thermoregulatory behavior to avoid exposure during the hottest or coldest hours of the day (^{Desbiez & Medri, 2010}). Giant anteaters spend more hours active and are more nocturnal during summer, and wild-reared individuals are more nocturnal than captive-reared ones (^{Di Blanco et al., 2016}). In some regions and during some periods, they display much more diurnal than nocturnal activity (^{Rodrigues et al., 2008}). Activity patterns can be especially distinct in the southernmost limit of their geographic distribution which is characterized by marked thermal seasonality (^{Di Blanco et al., 2016}) as in the Humid Chaco.

Important limitations of this study are the small sampling size and limited number of camera-traps and the lack of systematic sampling during the four seasons of the year in the three analyzed forest types and in other plant formations of the study area, however, there are few published studies regarding anteaters in Paraguay and errors and contradictions persist in literature (^{Smith, 2007}, ²⁰¹²; ^{Smith & Rios, 2018}). This research provides preliminary data on the species in the Humid Chaco, which is a key step for the design of conservation strategies for M. tridactyla and T. tetradactyla and as basis for further studies.

In addition to cattle and anteaters, camera-traps also recorded 43 species of wild animals of which three are threatened or near threatened: bare-faced curassow (Crax fasciolata), greater rhea (Rhea americana) and neotropical otter (Lontra longicaudis). Results suggest that cattle ranching activities developed in low-altered ecosystems, where low densities of cattle are maintained on native pastures (savannas) and the different types of forests are conserved, allow, so far, coexistence with anteaters and other wild animals.

Anteater populations are threatened by highway road kills and fire, which is the most common cause of M. tridactyla death in Brazil (^{Silveira et al., 1999}; ^{Fonseca & Rylands, 2004}). Fire is an ecological component in the design of the vegetation of the Humid Chaco due to the high productivity of the herbaceous stratum and an insufficient level of herbivory to assimilate all the production of herbaceous biomass (^{Ginzburg & Adamoli, 2006}). In savannas, the presence of cattle along with the conservation of the forest islets could be a key combination for anteater conservation, highlighting the importance of conserving wetlands and their associated riparian forests in the region as natural refuges for wild animal species.