Findings

The family Rheidae is endemic to the Neotropics and comprises two species of large flightless birds: Rhea americana and Rhea (Pterocnemia) pennata (Blake [1977]). R. pennata includes three subspecies: R. p. pennata, present in southern Chile and west-central and southern Argentina, in the Andean Precordillera steppes and Patagonian plateaus up to 2,000 m above sea level (a.s.l.); R. p. tarapacensis, which is distributed throughout northern Chile; and R. p. garleppi, occurring in southern Peru, southwestern Bolivia, and northwestern Argentina. The latter two subspecies inhabit open plains with grasslands, shrublands, and in the intermountain valleys of the Puna plateau above 3,500 m a.s.l. (Plenge [1982]; Cajal [1988]; Folch [1992]).

Wild populations of R. p. garleppi are found in low densities, with severe fluctuations throughout the species' distribution range, and with a tendency to decrease or become locally extinct in many cases (Cajal [1988]; Chebez [2008]). In the Puna, the main factors that negatively affect wild populations of this ratite are hunting for meat consumption and egg harvesting as subsistence resources (Barbarán [2004]; Hernandez [2011]). Another threat is the use by local people of by-products, such as feathers, skin, fat, and bones (Barbarán [2004]). In this scenario, and in order to ensure their long-term conservation, the subspecies R. p. garleppi is considered at risk of extinction (CITES [2014]) and R. pennata has been categorized as near-threatened (IUCN [2014]). However, the lack of knowledge regarding the current status of wild populations of R. p. garleppi hinders the conservation of this subspecies. The aim of this study was to provide updated information on the density and abundance of R. p. garleppi in the southern Puna ecoregion of Argentina.

This study was conducted in Don Carmelo Private Reserve (400 km2), located on the Andean Precordillera of San Juan province in Argentina (30°56′52″ S, 69°05′02″ W; 3,100 m a.s.l.). The Reserve is located in the Argentine Puna ecoregion, in the southeastern border of the Altiplano in the central Andes (Bonaparte [1978]). The climate is arid and cold, with intense solar radiation, strong winds, and daily temperature fluctuations that may exceed 30°C (Reboratti [2006]). Precipitations are scarce and occur between November and February, decreasing to the west and south of the Puna (Cabrera and Willink [1973]). The reserve is located in the subregion known as dry Puna due to the lack of permanent rivers and lakes (Cabrera [1976]). The dominant habitat is the shrub-steppe, with a mean altitude of 13.9 cm (±0.72), and the vegetation is xerophilous, with 88% of bare soil (Cappa et al. [2014]). Wild populations of R. p. garleppi inhabiting similar environments use indistinctly both the grassland plains of Stipa spp. and low shrublands of Adesmia spp, as well as the rocky and non-rocky mountain slopes with shrubs of Lycium spp. and Adesmia spp. and low cover of Stipa spp. (Cajal [1998]). Don Carmelo Private Reserve is a suitable site for the subspecies garleppi because it is not fragmented or disturbed by mining or agricultural activities, and massive tourism is banned.

It is difficult to perform direct observation or monitoring of R. p. garleppi in the study area because these birds run long distances at great speed, their plumage color allows them to mimic the environment, and the topography of the area is irregular. Therefore, we decided to use the fecal count technique as an indirect method for estimating population density (Ojasti and Dallmeier [2000]). This method has been used effectively in other studies on wild populations of rheas (Bazzano et al. [2002]; Herrera et al. [2004]; Kusch and Henríquez [2011]). Six samplings were conducted between 2011 and 2012 (September and November 2011; March, April, July, and November 2012). In each sampling, 20 randomized transects were spaced at least 400 m apart. This randomized design ensured sample independence, allowing us to consider each transect as true replicates by avoiding repetition of a single transect in successive monthly samplings. Transects of 500 m long were walked by a single observer in search of feces. The exact perpendicular distance from the path to each encountered feces was measured with metric tape by an assistant. Thus, the observer never left the transect, avoiding the record of additional feces. All encountered feces were collected to avoid double counting. Density of R. p. garleppi was calculated monthly using Distance 6.0 software (Thomas et al. [2009]), which requires entering data on individuals' defecation rate and feces permanence in the study area (Buckland et al. [2001]). As we did not have defecation rate data for R. p. garleppi, we used data from a similar species R. americana, following Buckland et al. ([2001]). These species are phylogenetically closely related (Delsuc et al. [2007]), have similar body weight and size (Fowler [1991]; Navarro et al. [1998]; Navarro et al. [2005]), and exhibit a primarily herbivorous diet (Bonino et al. [1986]; Martella et al. [1996]). The defecation rate used was 13.5 feces/individual/day (± 3.1; n = 8) and the permanence time of the feces was 88.15 days (±6.4; n = 14) (NV Marinero, personal observation). To calculate monthly density, we used the negative exponential model with cosine extension (Figure 1). The monthly abundance of R. p. garleppi was determined by multiplying density value of each month by the reserve area (400 km2), following Ojasti and Dallmeier ([2000]). Population size range of R. p. garleppi was calculated considering the average of months with highest density as the upper limit and the average of months with lowest density as the lower limit. Abundance (dependent variable) as a function of months (fixed effect) was calculated using a heteroscedastic mixed model, considering the sampling years (2011 and 2012) as random effect. In addition, given the heteroscedasticity of our data, we indicated that error variance of abundance was different for each month (grouping criterion) in the mixed model, using the function VarIdent (Di Rienzo [2011]). An a posteriori comparison of means of monthly abundance was performed using the Fisher's least significant difference (LSD) test, when differences were significant at P ≤ 0.05 (Balzarini et al. [2008]). Data were Log10-transformed for normalization of residuals. Non-transformed data were expressed as mean ± standard error of the mean. Statistical analyses were performed using Infostat (Di Rienzo et al. [2014]).

Figure 1
figure 1

Histogram of the perpendicular distance of feces of R. p. garleppi recorded at Don Carmelo Private Reserve, San Juan, Argentina. The line represents the fit of the negative exponential function with cosine extension.

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Population size of the subspecies R. p. garleppi presented significant variations among months (F5.84 = 3.61; P = 0.002). The upper limit of the population was 0.75 ind/km2 (±0.15) and was recorded in March, April, and July (2012) (P ≤ 0.05) (Figure 2). This density is the highest published until now, but close to other records obtained in Argentina: 0.67 ind/km2 (29°25′60′ S, 66°50′60″ W, La Rioja) and 0.52 ind/km2 in Laguna de Pozuelo Biosphere Reserve (22°28′S, 66°02′W, Jujuy) (Cajal [1988]; Cajal [1998]; and references therein). The differences in density estimates might be due to the different methods used, considering that Cajal ([1988]) states that the use of a motor vehicle to conduct the surveys of R. p. garleppi might have led to density underestimation. By contrast, we used the line-transect method and fit a detection function of probability of signs, which decreases with distance to the observer. This method reduces the potential bias of the density estimator (Buckland et al. [2001]) and provides a more realistic value of a population's density and abundance in a given area (Thomas et al. [2013]). The lower limit of R. p. garleppi population density was 0.47 ind/km2 (±0.10) in November (2011 and 2012) (P ≤ 0.05) (Figure 2). Although this record is the lowest for our study population, it is still higher than records reported for other wild populations inhabiting Argentina and Perú: 0.41 ind/km2 in Olaroz (23°43′ S, 66°48′ W, Jujuy) (Cajal [1998] and references therein), 0.12 ind/km2 in Laguna Blanca Biosphere Reserve (26°28′ S, 66°48′ W, Catamarca), 0.03 ind/km2 in San Guillermo Biosphere Reserve (29°25′ S, 69°15′ W, San Juan) and 0.01 ind/km2 in Tacna (16°44′ S, 70°16′ W) (Cajal [1988]; Lleellish et al. [2007]). Taking into account the important wild population of the subspecies garleppi present in the study area, it is necessary to promote its in situ conservation because it might become a source of individuals for possible recolonization and/or reinforcement of other populations undergoing higher conservation threat.

Figure 2
figure 2

Variation of monthly abundance of R . p . garleppi in 2011 and 2012 in Don Carmelo Private Reserve, San Juan, Argentina. Solid line, upper limit of population size; dashed line, lower limit of population size. Different letters indicate significant differences (Fisher's LSD, P ≤ 0.05).

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The higher abundance values of R. p. garleppi, with 300 individuals (±60), were recorded during March, April, and July 2012 (P ≤ 0.05) (Figure 2). The record of this upper limit in population size coincided with the occurrence of social groups of R. p. garleppi composed of juveniles, females with juveniles, and males in the reserve (NVM, pers. obs.); this group composition is characteristic of the non-reproductive season of rheas (Hanford and Mares [1985]; Sarasqueta [1990]; Carro and Fernandez [2008]). Thus, the observed increase in population size might be due to a reduction of aggressive behaviors among individuals during the non-breeding season, favoring the formation of groups of numerous individuals that tend to move together (Sarasqueta [1990]). However, it is also very important to consider that the upper limit in the population size of R. p. garleppi could be due to the movements made by the individuals to the reserve in search of refuge from poaching and livestock production, two activities that are more intensively conducted in the surrounding fields during the non-breeding season of the subspecies garleppi (Ordoñez [2006]). This perception of a protected area as refuge from the surroundings has also been described for other native herbivores, such as Lama guanicoe in the Monte arid ecoregion in Argentina (Acebes et al. [2010]). Moreover, abundance fell to 188 individuals (±40) in November (2011 and 2012) (Figure 2). This lower limit of population size corresponds to the breeding season of R. p. garleppi. While there was a record of an orphan egg in September 2012, no nest was found, despite the intensive search made inside the reserve. This drop in the number of individuals may be related to the species' nesting preferences, since individuals tend to select sites with high shrub cover, instead of pastures, which favors concealment and protection against predators and severe climate conditions (Bellis et al. [2006]; Barri et al. [2009a]). These sites are scarce in the study area, where shrub cover is only 16%, and pastures are 24%, whereas the remaining cover corresponds to bare soil (NV Marinero, unpublished data). Therefore, it is likely that during the reproductive season, R. p. garleppi individuals move toward surrounding areas about 14 km away from the reserve and below 2.500 m a.s.l. (NVM personal observation), where the habitat is dominated by an open shrubland of L. divaricata (Márquez [1999]). Indeed, reproductive groups of males with females, males with chicks, and juveniles have been observed in this environment adjacent to the reserve (NV Marinero, unpublished data).

We were not able to compare our results with wild populations from Bolivia because there are no studies published on the density of R. p. garleppi in that country, despite the heavy use of this subspecies by local communities, to the extent that wild populations may be decimated (Balderrama [2009]).

Our density records of R. p. garleppi (Figure 2) are higher than density values of R. p. tarapacensis present in different protected areas of Chile, which vary between 0.002 ind/km2 (Isluga Volcano National Park, 19°9′5″ S, 68°49′27″ W) and 0.022 ind/km2 (National Monument Salar Surire, 18°49′41″ S, 69°3′39″ W) (Acuña et al. [2008]). However, our estimations are lower than the values recorded for R. p. pennata in the Patagonia of Chile and Argentina, with records of 8 ind/km2 (50°46′S, 74°6′W, Ultima Esperanza, Chile), 2.93 ind/km2 (Santa Cruz, Argentina), 2.51 ind/km2 (Chubut, Argentina), 2.06 ind/km2 and 1.55 ind/km2 (Rio Negro, Argentina), and 1.94 ind/km2 (Neuquén, Argentina), although higher than in some areas of its northern distribution in Neuquén province, Argentina (Servicio Agrícola y Ganadero SAG [2002]; Navarro et al. [1999]; Secretaría de Ambiente y Desarrollo de la Nación SAyDS [2000]; Novaro et al. [2000]; Barri et al. [2009b]). In Argentina, in general, R. p. garleppi would occur at lower densities than R. p. pennata, which could be related to the primary productivity of the ecosystems. Specifically, the subspecies R. p. garleppi is distributed throughout the Puna ecoregion, where the low biomass production in the environment determines a lower carrying capacity. By contrast, the Argentine Patagonia, where R. p. pennata occurs, comprises a wider range of environments; the Monte and the Patagonia phytogeographic provinces, the Monte-Patagonia ecotone as well as ‘mallines’ (patchily distributed wetland areas), which provide habitat this ratite with important food resources (Oesterheld et al. [1998]; Bellis et al. [2006]; Guevara et al. [2006]; Bianchi and Bravo [2008]).

This work provides the highest density record for R. p. garleppi so far and highlights changes in population size related to the characteristics of the life history of rheas and human factors that negatively affect the survival of wild populations.

Authors' information

NVM is a fellow and JLN and MBM are researchers of the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and teachers of the Universidad Nacional de Córdoba.