Guanacos (Lama guanicoe) are large ungulates that have been valued by human populations in South America since the Late Pleistocene. Even though they were very abundant until the end of the 19th century (before the high deforestation rate of the last decades), guanacos have nearly disappeared in the Gran Chaco ecoregion, with relicts and isolated populations surviving in some areas, such as the shrubland area near the saline depressions of Córdoba province, Argentina. In this report, we present the first data from a locally endangered guanaco wild population, through the study of skeletal remains recovered in La Providencia ranch. Our results showed that most of the elements belonged to adults aged between 36 and 96 months; sex evaluation showed similar numbers of males and females. Statistical analysis of the body size of modern samples from Córdoba demonstrated that guanacos from the Chaco had large dimensions and presented lower size variability than the modern and archaeological specimens in our database. Moreover, they exhibited dimensions similar to those of modern guanacos from Patagonia and San Juan, and to archaeological specimens from Ongamira and Cerro Colorado, although further genetic studies are needed to corroborate a possible phylogenetic relationship. Finally, we used archaeozoological techniques to provide a first characterization of a relict guanaco population from the Chaco ecoregion, demonstrating its value to the study of modern skeletal remains and species conservation biology.
Citation: Costa T, Barri F (2018) Lama guanicoe remains from the Chaco ecoregion (Córdoba, Argentina): An osteological approach to the characterization of a relict wild population. PLoS ONE 13(4): e0194727. https://doi.org/10.1371/journal.pone.0194727
Editor: Dennis F. Lawler, Illinois State Museum, UNITED STATES
Received: April 29, 2017; Accepted: March 8, 2018; Published: April 11, 2018
Copyright: © 2018 Costa, Barri. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper and its Supporting Information files.
Funding: Financial support was provided by Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET).
Competing interests: The authors have declared that no competing interests exist.
According to Raedeke’s  estimations, about 50 million guanacos (Lama guanicoe) would have lived in South America during pre-Hispanic times. Archaeological data from Argentina showed that these ungulates have been valued economically and ideologically by human populations in the Late Pleistocene and throughout the Holocene [2–11]. In the central mountains of Córdoba, an area of the Gran Chaco ecoregion, guanacos also would have played an important role in the lives of indigenous people [12–16].
Since the Spanish colonization, the Gran Chaco has suffered a transformation from natural areas to agricultural landscapes. However, in the last decades, due to technological and socio-economic advances, the habitat destruction increased exponentially, with millions of lost hectares of forests and savannahs. Currently, crops are produced (mainly soybean) along with cattle raising, causing great loss of biodiversity [17–20]. At the beginning of the 20th century, guanaco populations surviving in Córdoba mountain ranges were valued for their meat and skin; they also were hunted viciously for sport shooting ( p.340-342). Today, the few remaining guanacos are isolated in the shrublands near the saline depressions .
The era of anthropocene defaunation  has seen massive biodiversity extinction during the last century. Current wildlife populations are in marked decline . New data from locally endangered wildlife populations are important for the conservation of species. The study of guanacos, large ungulates that can play an important role in the control of vegetation composition and structure [25–27], should include analysis of modern bone collections in order to obtain data for species protection. We used archaeozoological methods to offer new insights into changes that occurred in guanaco body sizes throughout the Holocene and in the modern population death profile. The techniques used for this study could advance the understanding of (a) the role that humans played in ecosystem changes, especially hunting and overexploitation during the early twentieth century ( p.339-345), and (b) the reasons for current declines of guanaco populations in Córdoba province.
Regional archaeological models have suggested that the numbers of guanacos in Córdoba could have been reduced since pre-Hispanic times due to human overexploitation . Nonetheless, current guanacos are endangered in the Chaco area due to habitat loss associated with the introduction of European cattle, historical (colonial and capitalist) overexploitation, and urban expansion processes, among other anthropogenic factors associated with defaunation.
Paleozoological assemblages provide important data concerning anthropogenic and ecological processes that can be used in conservation biology [28–32]. In this report, we characterize age and sex of guanacos in modern bone remains from a relict population recovered from 7 sites in an area located in the Corredor Biogeográfico del Chaco Árido. For this purpose, we used common archaeozoological practices. We also used osteometric techniques to compare the body size of the modern sample with specimens from surrounding areas and local archaeological sites, to obtain a better definition of the variability in species size. Based on this comparison, we discuss size changes that may be associated with the isolation of the current population, as well as relationships with archaeological specimens.
Finally, this report aims to demonstrate that the analysis of a modern collection using archaeozoological techniques can offer new insights that should help develop a better conservation agenda for the locally endangered guanacos.
Guanacos and humans, zooarchaeological data
Regional zooarchaeological data indicate that indigenous people used guanacos as a resource since the Early Holocene [12–16]. Nonetheless, Rivero et al.  argue that the use of wild camelid populations by humans, as their main resource, could have not been sustained beyond the Late Holocene (3000 B.P.). These interpretations are based on the zooarchaeological analysis of 14 sites dating to Early-Late Holocene and the apparent decreasing presence of Lama sp. remains over time .
Rivero & Medina  analyzed the archaeofaunal assemblages of 8 sites and introduced the records from 2 other assemblages (Quebrada del Real 1-Component 1, Quebrada del Real -Component 2) . The authors suggest two hypotheses to explain reduced camelid density and increased numbers of smaller-sized animals in the zooarchaeological record. The first hypothesis suggests that participation of women and children in the economy contributed to hunting or collection of the smaller animals. The second hypothesis proposes that the growth in the human population, with resulting overexploitation of camelids, was the main factor that led humans to seek other resources .
Mitochondrial DNA analysis of past humans in the area suggests that, by ca. 1200 B.P., significant changes had occurred in the population from the high plains. Those changes included an increment in haplogroup B that modified the previously-dominant gene pool in the area (haplogroup C) . Moreover, different proxies for paleoclimate indicate an increase in humidity that started in the Middle Holocene, evidenced by a continuous replacement of C4 with C3 plants since ca. 3870 B.P. [35, 36]. These changes from open (grasses, C4) to denser vegetation (herbaceous or woody C3 species), probably affected faunal distribution because species had to adapt to these changing climate conditions. Accordingly, the causes of the decrease of guanacos in the archaeological record should be interpreted cautiously, since changes in both climate and human populations took place during the Late Holocene. Finally, in agreement with ( p. 84), “sampling bias and chronological gaps” should be eliminated by developing “regional scale studies”.
Fig 1 shows data taken from Rivero et al.  and Rivero & Medina  with the addition of samples from Alero Deodoro Roca site in Ongamira . Artiodactyl index (∑ Artiodactyl / (∑ Artiodactyls + ∑ small vertebrate) suggests a decrease in the human use of large ungulates (Lama sp. represents 77.49% of the ungulate number of identified species -NISP) throughout the Holocene.
Material and methods
During the second semester of 2015, we surveyed the 200,000 hectares of the Salinas Grande area, searching for guanacos remaining in Córdoba. We found one population on La Providencia ranch, where we recovered 413 complete bone elements belonging to a minimum of 27 skeletons (Fig 2). Nineteen specimens had been killed and discarded in the same area through illegal poaching. The remaining 8 were dispersed on the ranch, and from this sample, 5 individuals died caught in the wires delimiting the field (2 females, 1 male, and 2 specimens of unidentified sex). We were not able to determine the cause of death of the remaining 3 guanacos.
Upper right: map showing Córdoba province, its location in South America and the locations of the modern and archaeological sites discussed in this report. Left: Detail of the collection points in La Providencia ranch (30°56'54.44"S, 65°34'34.93"W).
Weathering conditions of the samples agree with those reported previously for juvenile and adult guanaco bones exposed to subaerial deterioration for periods no longer than 48 months [37–39]. S1 Table displays the maximum weathering stages  and their description for the 50 bone elements analyzed in this report. Cranial elements exhibited more advanced weathering stages of frontal and supraorbital bones, compared to maxillary bones. The measured phalanges and alveolar processes from maxilla and mandible bones showed no signs of weathering.
Age estimation through dental development, eruption, and wear is a common ageing method in the archaeozoology of camelids and in the biology of guanacos [1, 4, 41–45]. Guanacos have heterodont and diphyodont dentition, with 4 types of teeth: incisors (I), canines (C), premolars (P), and molars (M) [1, 43, 44].
We used Kaufmann’s  sequence of tooth development and wear for upper and lower guanaco teeth to characterize the age of 30 cranial and mandibular remains. This classification was based on observation of tooth (P, M, and deciduous premolars Pd) development and wear from Rio Negro, Argentina. The following categories were defined: unborn (10–11 months of gestation), offspring (0–12 months), juvenile (12–24 months), subadult (24–36 months), adult (3–10 years), and senile (over 10 years) .
It is accepted widely that South American camelids do not have sexual dimorphism [1, 4, 41]. Nonetheless, size of the canine teeth is one characteristic that can be determinant in assigning sex within species where only males must compete for territories [1, 43]. Raedeke ( p. 99) states that, to determine sex in guanacos, considering the overall mass of the canines yields better results than considering their length. The author proposes a “canine index”, which is calculated by multiplying the height of the canine by its maximum diameter at the alveolar rim .
Following Raedeke’s  suggestion, Lefèvre et al.  adapted the procedure to samples in which canines were not present. These authors took 2 measurements of the mandibular canine alveolar process, the maximum and minimum diameters ( p. 79). Using this technique, they were able to discriminate a group of males with a maximum diameter above 10 mm and a female group having this diameter below 9 mm . To determine the sex of individuals in our samples, we followed the proposal of Lefèvre et al.  for the specimens categorized as adults and, whenever possible, compared these results with the different characteristics of the male/female pelvis described by Kauffman [4, 47]. We calculated the geometric mean of the variables measured in the same units (mm), a well- discussed and commonly-used morphological proxy for skeletal size measurements that can be used to understand geometric similarity [3, 16]. Results are presented using bivariate graphs and mixture analysis [47, 48].
Determining morphotypes in artiodactyl populations allows us understand how they are adapted to their environment . For example, larger body size directly affects relationships with other species, influencing ability to compete for resources or to escape from predators . To characterize body size, we compared data from 5 osteometric variables: 1) maximum length of phalanges, taken parallel to the major axis based on the tangent formed by the proximal and end plantar condyles at the most distal point of the distal articular surface; 2) width of the proximal articular surface; 3) height of the proximal articular surface; 4): width of the distal articular surface; 5) height of the distal articular surface [41, 51]. This procedure was done with 10 first modern phalanges from Córdoba, having the same variables as those of 14 samples recovered from 4 regions of Argentina (Salta, Catamarca, San Juan, and Patagonia) . To determine differences over time, we added 10 phalanges from local archaeological sites (Fig 2) for comparison. We used only forelimb phalanges, since they were found to better discriminate the differences in body size of the specimens than hind limb phalanges . We performed multivariate cluster analysis and mixture analysis to characterize size differences among the study specimens [51–53]. For the statistical analysis we used the software Past version 3.14 .
The study area was located on the La Providencia ranch (Fig 2), an area situated in the Corredor Biogeográfico del Chaco Árido near the El Chacho locality (Córdoba, Argentina). According to Zak and Cabido , the area belongs to the lowland region, classified as Aspidosperma quebracho-blanco and Prosopis nigra forest, which is being displaced rapidly by cultural landscapes and shrublands. The soils are characterized by extreme salinity, with noticeable accumulation of carbonates or gypsum and saline layers .
The climate in the region is mild, according to the characteristics of a semiarid region. Temperature mean is about 25°C during summer and approximately 12°C in winter. Precipitation ranges between 130 mm in summer and is below 40 mm during the coldest months (data from the Argentina’s meteorological service for Villa de María de Río Seco, available at: http://www.smn.gov.ar/serviciosclimaticos/). Romero & Santa María  presented rainfall data recorded at La Providencia. According to the authors, precipitation was 165 mm between February and December 2013, 536 mm between January and December 2014, 607 mm between January and December 2015, and 349 mm from January to September 2016 ( p. 18).
The modern sample
Age estimates showed that most of the elements recovered (n = 20) belonged to adults aged from 36 to 96 months (Table 1). The classification used here is better suited to the mandibular sequence of tooth development and wear than to maxillary tooth sequence. This was evident in the comparison of the results of maxilla (CRNMF3) and mandibular (MRMMF2) bones belonging to a guanaco that died trapped in the fences of Molino Ferrarini (MF). The mandibular bone MRMMF2 exhibited better resolution of the estimated age of death (5 to 6 years) than the cranial bone (CRNMF3). Furthermore, 15% of the elements belonged to young adults (A1), 55% of the elements were guanacos that died at between 48 and 84 months of age (A2), 10% of the recovered bones aged from 5 to 6 years (A3). The remaining 20% were aged between 6 and 8 years (A4 and A5).
Age group according to Kauffman’s  categorization (J = juvenile; S = subadult; A = adult).
Table 1 also indicates the results from 10 elements categorized as subadult guanaco. Within this group, 3 elements (2 individuals) were aged between 12 and 19 months (J1). The estimated age at death of the remaining 7 elements was between 24 and 36 months. It should be noted that the only mandibular (MRCF16) element in the S age group showed an estimated age of 24–30 months (S1). Therefore, we considered that the element could belong to one of the cranial remains categorized as S2, even though we were not able to rejoin the cranial-mandibular pieces due to a trampling fracture of the coronoid process of the mandibular section.
Fig 3 displays a group of guanacos on La Providencia ranch (A). The mandibular teeth of a subadult (MRCF16) guanaco include deciduous premolars 3 and 4 (Dp) and the alveolar process with M3 inside. Likewise, the mandible seen in Fig 3B shows the 3 molars of an adult guanaco with an estimated age at death between 5 and 6 years (MRCF24). Comparing these two mandibles revealed the differences in molar wear. The infundibulum, the funnel-shaped cavity, is nearly lost in the adult’s M1. Moreover, the adult mandible lacks the deciduous premolars and M3 already is modified by attrition; the enamels clearly are separated from the dentin (Fig 3B below).
A: A group of reproductive guanacos. Fig 3B: (above) Mandibular teeth (S1 age group) reveals deciduous premolars (Dp) and molars (M); (below) mandibular molars of an adult guanaco (A3 age group). Fig 3C: (above) lower canines of a male specimen (MRMF2, A3 age group); (below) example of the differences in the lower canines; male on the left side of the scheme and female guanaco on the right (see also Kaufmann ).
Fig 3 also reveals qualitative information that contributes to sex discrimination (n = 19 elements); male canines are more robust and curved than female ones (C). Nonetheless, in osteological collections recovered after a few years of weathering exposure, some teeth tend to fall from the alveolar process (in our study, most of these were canines). Hence, whenever possible, the whole specimen (and/or other attributes such as pelvis) should be compared in any research.
The results obtained from the measurement of the alveolar process revealed a clear differentiation of the specimens into two groups. One group has larger dimensions (9.44 mm mean in both measurements) and is composed of 10 specimens identified as males (Fig 4). The other group has a mean of 6.04 mm, and is composed of 9 specimens that, following Lefèvre et al. , correspond to the measurement of females (Fig 4). Our results are similar to those reported previously, supporting the use of this technique when differentiating sex groups in a guanaco osteological collection. In addition, we compared our results with those described by other authors [4, 47] regarding the characteristics of the pelvis in specimen CRNMF3, and found the same results.
Results of sex categorization according to the diameter of the alveolar process.
We performed a mixture analysis of the geometric mean of both measurements described in Materials and Methods to corroborate the bivariate results and found the same distribution (Table 2). Therefore, we suggest that the technique presented by Lefèvre et al.  is accurate for separating males and females.
Characterizing variation in body size throughout the Holocene
According to results of body size (Table 3), the largest geometric mean (27.16 mm) corresponded to the modern specimens from Córdoba, with Patagonian specimens showing 25.72 mm and only one individual above 27 mm (MLP-G4). These results could reflect sampling, since Patagonian guanacos are expected to be larger (we are aware of body size differences among Patagonian specimens, but we have no precise data regarding site of origin of the latter). Northwestern specimens presented a geometric mean of 24.32, whereas the mean of specimens from San Juan was closer to that of Córdoba sample (26.29 mm).
Measurements in millimeters (1–5) and geometric mean of 34 forelimb first phalanges (for radiocarbon dates from Ongamira samples, see ).
The 10 archaeological modern samples from Córdoba had a geometric mean of 25.15 mm. Samples from Ongamira had a mean of 25.46 mm, with the element dated to 3600 B.P. measuring 23.76 mm, the lowest in the group. Elements 3810 (26.57 mm) and 60–172 (26.82 mm) from Ongamira had the closest geometric means compared to the mean of our modern samples.
The elements from San Alberto revealed the smallest (24.28 and 24.25 mm) means and presented similar dimensions, suggesting that the phalanges might belong to the same individual. The element found at Los Molinos had the smallest geometric mean (22.50 mm) in the database; the element found at Cerro Colorado had a mean of 26.28, closer to the mean of the phalanges from Ongamira, San Juan, and Córdoba than that of Los Molinos (Table 3).
Multivariate paired group (UPGMA) with Euclidean similarity index was used to create a cluster that separates the samples. Fig 5 shows 3 groups differing in body size. The small size group includes only one archaeological specimen from Los Molinos. The medium size assemblage includes 64% of the specimens we analyzed and can be divided into 2 subgroups. One of these gathers a smaller size class, and includes the modern samples from Catamarca, Salta, specifically 2 phalanges from the Patagonian sample (MLP-G3 and MLP-G5), and 2 phalanges from Ongamira (1535 and 3871). The other subgroup includes specimens from Patagonia (MLP-G1, MLP-G2, and MLP-G6), Ongamira (1357, 3810, 443, and 60–172), San Alberto (BPS-191 and BPS-192), San Juan (FPDG-1, FPDG-2, and FPDG-3), and the element from Cerro Colorado (AJPHF2). Finally, the large size group consists of modern phalanges from Córdoba (CF and MF3) and one recovered in Patagonia (MLP-G4).
UPGMA showing body size differences in Argentine guanacos.
Table 4 shows Mixture Analysis results using the geometric mean of the 5 measured variables. The maximum-likelihood method allowed us to segregate the samples into 2 groups. One group included 23 phalanges with larger dimensions: 18 modern samples including Patagonia (n = 5); all samples from San Juan and Córdoba; and 5 archaeological elements from Ongamira and Cerro Colorado. The other group included 11 elements with smaller dimensions: 1 phalange from the modern samples from Patagonian (MLP-G6) and all the phalanges from northwestern Argentina (Catamarca and Salta); and 2 phalanges from Ongamira (1357 and 1535), San Alberto, and Los Molinos.
The guanaco has nearly disappeared in the Gran Chaco, with only two or three relict populations currently surviving in the opposite extremes of the eco-region distribution: one or two in the north, between Bolivia and Paraguay , and the other in the south, as described in this report. The decline of the Chaco guanaco population results from multiple factors affecting wildlife in the region, such as habitat loss, interspecific competition with livestock, and hunting [59, 60].
Bioarchaeological studies indicate that ca. 1200 B.P, there was a process of human migration and change in way of life [36, 61]. This process might have been associated with environmental pressures, such as climate change, demographic increases in population sizes, and development of new social organizations, probably with the emergence of a more hierarchical structure . Regional archaeofaunal data suggest that despite the environmental and population changes, guanaco hunting remained an important economic activity [13–16].
Regarding the reasons for camelid decline in the archaeofaunal record of Gran Chaco province during pre-Hispanic times (as defined by the artiodactyl index ), 15 zooarchaeological assemblages should be interpreted cautiously. Even though not all of the 2017 recorded sites in the province  present comparable archaeofaunal samples, further research is needed to avoid sampling bias. Moreover, historical and ethnohistorical data also indicate that guanaco hunting persisted in the mountain chains until the beginning of the 20th century [21, 63], and still occurs in the southern Salinas Grandes.
Results from sex estimation in the extant population from Córdoba presented a similar number of adult males and females, with the number of adults being twice that of the subadults. However, most of our sample (n = 19) comes from illegal poaching activities that probably occurred between 3–4 years ago, according to information gathered from local dwellers and supported by the weathering stages of the specimens (S1 Table). Moreover, the mortality profile of the sample recovered from poaching activities shows that 6 elements belonged to subadults (24–36 months old), 13 elements belonged to adults (3–6 years old) and 5 elements belonged to older adults. Thus, the addition of individuals of different age groups (with a higher number of 3–6 years old adults) and of both sexes to the poaching sample suggests a hunting strategy that included guanaco family groups and young male groups, as discussed by other authors ( p. 389). In addition, the individuals that died caught in the fences tended to be younger (J1 and S2 age groups), as expected due to their lack of experience .
Guanaco mating is based on polygyny, for protection of the population. Puberty is reached around age 2 years in females and 3 years in males. However, due to the high competition in the wild, males under age 5 seldom reproduce under. Therefore, our study sample might contain more reproductively active females than males, since our estimated age for males included at least 5 (considering MX only) individuals that could be under reproductive age . It would be necessary to collect more specimens with more complete skeletons to estimate sex differences using other identifying metrics (such as pelvis shape). This would allow better characterizing of subadults, since the osteometric approach cannot be applied when bone development is incomplete. On the other hand, results from mixture analysis revealed the same distribution of sex estimation as that observed in the bivariate graph, suggesting that the technique can be an important tool for differentiating sex of fragmented skeletons.
Our results from body size analysis demonstrate that modern specimens from Córdoba have larger dimensions than those of modern and local archaeological specimens from other regions. Moreover, mixture analysis grouped the modern sample with specimens from Patagonia and San Juan, the specimens of largest dimensions in our database. Hence, we propose that the differences in body size might be related to some adaptation to the Chaco native forests in Córdoba. In addition, the archaeological samples from Córdoba showed higher variability in their dimensions than the modern sample from Chaco.
Late Holocene (ca. 1000 B.P) archaeological specimens from San Alberto and Los Molinos revealed smaller dimensions (geometric mean of 23.68 mm) than the one from Cerro Colorado (geometric mean of 26.28 mm, see Table 3). Phalanges from Ongamira mostly showed geometric means above 25 mm, except for two specimens dated to 2900 B.P. (1357) and 3600 B.P. (1535). A previous work in the regional characterization of archaeological camelids presented similar results. Despite the size variability, most specimens tended to be medium or large size [13, 16]. Finally, mitochondrial DNA data suggest the existence of a guanaco metapopulation that replaced the extinct Patagonian guanacos at ca. 10551 years ago, becoming ancestral to all modern guanacos . Thus, ancient guanacos from Córdoba probably bred with different populations, which may have increased size variability.
Even though there would be only two subspecies of guanacos, the Peruvian L. guanicoe cacsilensis and the remaining populations grouped in the clade recognized as L. g. guanicoe , our data suggest that guanacos from Chaco might represent a particular ecotype. This hypothesis must be tested with further anatomical, demographic, and genetic studies. Therefore, considering also that mammals play a particularly important role in the dynamics of the Chaco ecosystem, we propose that a species conservation status for these unique guanaco population should be established.
Additionally, it would be important to compare our data with those of other persisting Chaco guanaco populations from Bolivia and Paraguay . We should enlarge our database by adding samples from other archaeological or paleontological time periods to obtain better resolution for body size variation of guanacos in the Chaco region.
Our results demonstrate that the modern sample from Córdoba has the largest dimensions of the phalanges represented in our database. Nevertheless, our data should be compared with those from archaeofauna and paleontological guanaco remains in the area. Furthermore, new modern samples (especially from Chaco areas where the species is still present) should be added to the analysis if we are to fully understand the requirements for the conservation of the extant population.
The guanacos are important because they are the last remnant population in an area where guanacos historically were numerous . They now are in decline due to anthropogenic environmental and climate changes, particularly during recent decades, wherein habitat loss in the Chaco ecoregion has increased dramatically [19,20]. Therefore, it is essential to understand how colonial development with the introduction of European cattle, vegetation changes, and commercialization of native animal skins, could have affected guanacos in Córdoba ( p. 349, ). Moreover, historical data for Argentina indicate that native products incorporated to the capitalist system brought several faunal populations to the brink of extinction [67,68, 69].
Finally, although the archaeofaunal assemblages in Córdoba remain fragmentary, sampling and chronological bias tends to diminish as research advances. Improved temporal resolution from Holocene paleozoological collections should provide new insights into conservation biology . Accordingly, as Barnosky et al.  suggest, fostering conservation planning and practice requires the use of paleozoological and historical information.
We would like to thank the owners of La Providencia ranch, who allowed us to conduct research in their property. We would also like to thank Paul Quintero and Luis Garay, the managers of the field for guidance in the area. The editors (especially Dennis Lawler) and the anonymous reviewers made constructive comments that helped us improve the manuscript.
- 1. Raedeke KJ. Population dynamics and socioecology of the Guanaco (Lama guanicoe) of Magallanes. Chile. PhD dissertation. College of Forest Resources. University of Washington. Seattle (Ann Arbor, University Microfilms International). 1979. Available from: https://dlib.lib.washington.edu/researchworks/handle/1773/5460. Cited March 2016.
- 2. Mengoni Goñalons, GL. Cazadores de Guanacos de la estepa patagónica. Sociedad Argentina de Antropología, Colección Tesis Doctorales. Buenos Aires; 1999.
- 3. Izeta AD. Interspecific Differentiation of South American Camelids on Archaeofaunal Calchaquíes Valleys (Argentina). In: Gutiérrez M., Barrientos G., Mengoni-Goñalons G., Miotti y L. Salemme M., editors. Tafonomía y Zooarqueología Argentina. BAR International Series; 2007. pp. 47–57.
- 4. Kaufmann C. Estructura de sexo y edad en guanaco. Estudios actualísticos y arqueológicos en Pampa y Patagonia. Colección Tesis Doctorales, Sociedad Argentina de Antropología, Buenos Aires; 2009.
- 5. Martínez G, Gutiérrez M. Tendencias en la explotación humana de la fauna durante el Pleistoceno final y Holoceno en la Región Pampeana (Argentina). In Mengoni Goñalons G. editor. Zooarchaeology of South America 1298; 2004. pp.81–91.
- 6. Politis GG, et al. Distribution parameters of guanaco (Lama guanicoe), pampas deer (Ozotoceros bezoarticus) and marsh deer (Blastocerus dichotomus) in Central Argentina: Archaeological and paleoenvironmental implications. J of Arch Sci. 38. 7, 2011: 1405–1416.
- 7. Neme G, Wolverton S, Gil A. Modelo ecológico para evaluar la sobreexplotación de Ungulados: implicancias en los conjuntos zooarqueológicos de guanaco del sur de Mendoza. Archaeofauna 21. 2012: 207–218.
- 8. Otaola C, Franco NV. Procesamiento y consumo de guanaco en el sitio Chorillo Malo 2, Provincia de Santa Cruz, Argentina. Magallania. 2008, vol.36, n.2, pp.205–219. http://dx.doi.org/10.4067/S0718-22442008000200016.
- 9. De Nigris ME, Cata MP. Cambios en los patrones de representación ósea del guanaco en Cerro de los Indios 1 (Lago Posadas, Santa Cruz). Intersec en antropol. 2005, n 6. ISSN 1850-373X.
- 10. Yacobaccio H, et al. Caza, domesticación y pastoreo de camélidos en la Puna Argentina. Rela de la Soc Arg de Antropol. XXIl-XXIII; 1997–1998, 389–418.
- 11. Olivera D, Grant JL. Puestos de altura de la Puna Argentina: Zooarqueología de Real Grande 1 y 6 y Alero Tomayoc. Rev del Mus de Antropol, 2.1 2009, 151–168.
- 12. Rivero D, Medina ME, Recalde A, Pastor S. Variabilidad en la Explotación de Recursos Faunísticos durante el Holoceno en las Sierras de Córdoba (Argentina): Una aproximación Zooarqueológica. In: Gutierrez M., De Nigris M., Fernández P., Giardina M., Gil A., Izeta A., Neme y G. Yacobaccio H., editors. Zooarqueología a principios del siglo XXI: Aportes Teóricos, Metodológicos y Casos de Estudio. Ediciones del Espinillo. Buenos Aires; 2010. pp. 321–331.
- 13. Medina ME, Pastor S, Rivero DE. Osteometría y diferenciación de especies de camélidos en sitios arqueológicos de las Sierras Centrales (Argentina): Tendencias, problemas y perspectivas. Intersec en antropol. 2014; 15(2), 339–351.
- 14. Costa T. Una aproximación zooarqueológica a las prácticas de los cazadores-recolectores en el Alero Deodoro Roca (ca. 2970 AP), Valle de Ongamira, Córdoba. Rev del Mus de Antropol.;9(2):93–104.
- 15. Costa T. Zooarqueología en el Alero Deodoro Roca (ADR). Las interacciones entre personas y animales durante el Holoceno Tardío (1900–3600 AP). In Cattáneo G. R. & Izeta A. D., editors. Arqueología en el Valle de Ongamira, 2010–2015. Córdoba: Universidad Nacional de Córdoba; 2016. pp. 117–142
- 16. Costa T, Izeta A. Morphometric analysis of camelid remains from the Alero Deodoro Roca (ADR) site (Córdoba, Argentina). An attempt to characterize body size variability in Sierras Pampeanas Australes region. Int. J. Osteoarchaeol., 2016
- 17. Leynaud GC, Bucher EH. Restoration of Degraded Chaco woodlands: effects on reptile assemblages. For Eco and Manag. 2005. 213(1), 384–390.
- 18. Zak MR, Cabido M, Cáceres D, Díaz S. What Drives Accelerated Land Cover Change in Central Argentina? Synergistic Consequences of Climatic, Socioeconomic, and Technological Factors. Enviro Manag. 2008. 42, 181–189. 1.
- 19. Nori J, Lescano JN, Illoldi-Rangel P, Frutos N, Cabrera MR, Leynaud GC. The conflict between agricultural expansion and priority conservation areas: Making the right decisions before it is too late. Bio Cons. 2013. 159, 507–513.
- 20. Nori J, Torres R, Lescano JN, Cordier JM, Periago ME, Baldo D. Protected areas and spatial conservation priorities for endemic vertebrates of the Gran Chaco, one of the most threatened ecoregions of the world. Div and Dist. 2016. 22(12), 1212–1219.
- 21. Río M, Achával L. Geografía de la Provincia de Córdoba Vol II. Buenos Aires: Compañía Sudamericana de Billetes de Banco; 1905. pp.690. Available from: https://archive.org/details/geografadelapro02archgoog.
- 22. Kufner M, Giraudo L. Distribución de la diversidad y las extinciones de mamíferos de Córdoba en relación con la reducción del bosque y los cambios paleoclimáticos. Bol de la Ac Nac de Cien de Córd., 2001. 66. pp.109–116.
- 23. Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJ, Collen B. Defaunation in the anthropocene. Science; 2014. 345 (6195). pp. 401–406. pmid:25061202.
- 24. Ceballos G, Ehrlich PR, Barnosky AD, García A, Pringle RM, Palmer T. Accelerated modern human–induced species losses: Entering the sixth mass extinction. Sci. Adv. 2015. 1 (5): e1400253. pmid:26601195.
- 25. Bradshaw RH, Hannon GE, Lister AM. A long-term perspective on ungulate-vegetation interactions. Fo Eco and Manag. 2003. 181(1). pp. 267–280.
- 26. Acebes P, Traba J, Malo JE, Ovejero R, Borghi CE. Density and habitat use at different spatial scales of a guanaco population (Lama guanicoe) in the Monte desert of Argentina. Mammalia, 2010. 74(1), 57–62.
- 27. Flores CE, Cingolani AM, von Müller A, Barri FR. Habitat selection by reintroduced guanacos (Lama guanicoe) in a heterogeneous mountain rangeland of central Argentina. The Range J. 2013. 34(4). pp. 439–445.
- 28. Lyman RL. Paleozoology in the service of conservation biology. Evo Anthro: Issues, News, and Reviews. 2006. 15(1):11–19.
- 29. Lyman RL. A warrant for applied paleozoology. Bio Rev. 2012. 87:513–525. pmid:22032263
- 30. Rick TC, Lockwood R. Integrating Paleobiology, Archeology, and History to Inform Biological Conservation. Cons Bio. 2013. 27:45–54. pmid:22979917
- 31. Szabó P. Why history matters in ecology: an interdisciplinary perspective. Enviro Cons. 2010. 37(04), 380–387.
- 32. Barnosky AD, Hadly EA, Gonzalez P, Head J, Polly PD, Lawing AM, et al. Merging paleobiology with conservation biology to guide the future of terrestrial ecosystems. Science, 2017. 355(6325), eaah4787. pmid:28183912
- 33. Rivero D, Medina ME. Human Colonization, Diet Breadth and Niche Construction during Sierras of Córdoba Holocene (Argentina). In: Muscio H., Cardillo M., editors. Darwin’s Legacy: The State of Evolutionary Archaeology in Argentina. Oxford: Archaeopress. SAMAR Series 24, 2013. pp. 76–88.
- 34. Nores R, Fabra M, Demarchi DA. Variación temporal y espacial en poblaciones prehispánicas de Córdoba. Análisis de ADN antiguo. Rev del Mus de Antropol. 2011;4(1):187–94.
- 35. Silva LCR, Giorgis MA, Anand M. et al. Evidence of shift in C4 species range in central Argentina during the late Holocene. Plant and Soil. 2011. 349: 261–279.
- 36. Yanes Y, Izeta AD, Cattáneo GR, Costa T, Gordillo S. Holocene paleoenvironmental (~4.5–1.7 cal. kyr BP) conditions in central Argentina inferred from entire-shell and intra-shell stable isotope composition of land snails. The Holocene; 2014. 24 (10): 1193–1205.
- 37. Borrero LA. Longitudinal taphonomic studies in Tierra del Fuego, Argentina. In Gutiérrez MA, Miotti L, Barrientos G, Mengoni Goñalons G, Salemme M, editors. Taphonomy and Zooarchaeology in Argentina. BAR International Series 1601, Archaeopress, Oxford; 2007. pp. 219–233.
- 38. Massigoge A, González M, Kaufmann C, Gutiérrez MA. Observaciones actualísticas sobre meteorización ósea en restos esqueletales de guanaco. In: Berón M, Luna L, Bonomo M, Montalvo C, Aranda C, Carrera Aizpitarte M, editors. Mamül Mapu: Pasado Y Presente Desde La Arqueología Pampeana. Ediciones del Espinillo: Buenos Aires; 2010. pp.309–322.
- 39. González ME, Álvarez MC, Massigoge A, Gutiérrez MA, Kaufmann CA. Differential bone survivorship and ontogenetic development in Guanaco (Lama guanicoe). Int. J. Osteoarchaeol. 2012. 22(5):523–536.
- 40. Todd LC. Taphonomy of the Horner II bone bed. In: Frison GC, Todd LC, editors. The Horner Site, the type site of the Cody cultural complex. Elsevier; 2017 May 4. Academic Press, Orlando, Fla. 1987. pp 107–198.
- 41. Kent J. The Domestication and exploitation of the South American camelids: methods of analysis and their application to circum-lacustrine archaeological sites in Bolivia and Peru. Ph.D. Thesis. Washington University, St. Louis, Missouri; 1982.
- 42. Wheeler J. Ageing Llamas and Alpacas by their teeth. Llama World; 1982. 1: 12–17.
- 43. Hillson S. Teeth. 2nd ed. Cambridge University Press, 1986.
- 44. Oporto N, Bigatti R, Larrieu E. Determinación de edades en guanaco (Lama guanicoe) en base a su dentición. Rev Arg de prod ani. 1979. 4(9), 965–983.
- 45. Rivals F, Rindel D, Belardi JB. Dietary ecology of extant guanaco (Lama guanicoe) from Southern Patagonia: seasonal leaf browsing and its archaeological implications. J of Archaeo Sci. 2013. 40(7), 2971–2980.
- 46. Lefèvre C, Lepetz S, Legoupil D. ¿Cazadores terrestres, cazadores marítimos? Explotación de los recursos animales en el Locus 1. Cazadores-recolectores de Ponsonby (Patagonia austral) y su paleoambiente desde VI al III milenio A.C. Legoupil. Magallania; 2003. 31: 63–116.
- 47. Kaufmann CA, Álvarez MC, L'Heureux LG, Gutiérrez MA. Dimorfismo sexual en la pelvis de Lama guanicoe (Artiodactyla, Camelidae): un caso de aplicación en el sitio Paso Otero 1, Buenos Aires, Argentina. Mastozool. neotrop. 2013; 20(1): 47–59.
- 48. Monchot H. Mixture analysis and mammalian sex ratio among middle Pleistocene mouflon of Arago cave, France. Quater re. 1999. 52(2), 259–268.
- 49. Lindstedt SL, Boyce MS. Seasonality, fasting endurance, and body size in mammals. Ame Natu. 1985. 873–878.
- 50. Calder WA. Size, function and life history. Harvard University Press, Cambridge, Mass; 1984.
- 51. Izeta AD, Srur MG, Labarca Encina R. Guía Osteométrica de Camélidos Sudamericanos. 1st ed. Córdoba: Universidad Nacional de Córdoba; 2012.
- 52. Izeta AD, Otaola C, Gasco A. Estándares Métricos y Variabilidad en falanges proximales de Camélidos Sudaméricanos. Su importancia como conjunto comparativo para interpretaciones en arqueología. Rev del Mus de Antropol. 2009; 2(1):169–80.
- 53. Yacobaccio HD. Osteometría de llamas (Lama glama L.) y sus consecuencias arqueológicas. In: Gutiérrez M, De Nigris M, Fernández P, Giardina M, Gil A, Izeta A, Neme G, Yacobaccio H, editors. Zooarqueología a principios del siglo XXI. Aportes teóricos, metodológicos y casos de estudio. Del Espinillo: Buenos Aires; 2010. pp. 65–75.
- 54. Hammer Ø, Harper DAT, Ryan PD. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Paleo Elec. 2001. 4(1): 9. Available from: http://palaeo-electronica.org/2001_1/past/issue1_01.htm.
- 55. Zak M, Cabido M. Spatial patterns of the Chaco vegetation of central Argentina: Integration of remote sensing and phytosociology. App Vege Sci. 2002. 5: 213–226.
- 56. Romero J, Santa María G. Plan de Conservación del Bosque Nativo, Campo “La Providencia”–Puesto “La Nena”, Serrezuela, Córdoba, Argentina. Amb.Ar. (Ambiente Argentino). Unpublished Environmental Report; 2016. pp 55.
- 57. Cattáneo GR, Izeta AD, Takigami M. Primeros fechados radiocarbónicos para el Sector B del sitio Alero Deodoro Roca (Ongamira, Córdoba, Argentina). Rev Rel de la Soc Arg de Antropol. 2013. 38 (2):559–567.
- 58. Cuéllar E, Noss AJ. Diversidad de mamíferos y participación local en la conservación en el Gran Chaco Boliviano. Therya; 2014. 5(1):39–60.
- 59. Grau H. R., Torres R., Gasparri N. I., Blendinger P. G., Marinaro S., & Macchi L. (2015). Natural grasslands in the Chaco. A neglected ecosystem under threat by agriculture expansion and forest-oriented conservation policies. J of Ari Enviro. 123, 40–46.
- 60. Periago ME, Chillo V, Ojeda RA. Loss of mammalian species from the South American Gran Chaco: empty savanna syndrome? MamRev. 2015. 45(1): 41–53.
- 61. Fabra M, González CV, Salega MS. Modos de vida e historia biológica de poblaciones de las sierras y las llanuras de Córdoba (Argentina): aproximaciones desde el registro bioarqueológico. Rev Arg de Antropol Biol. 14, 2012.
- 62. Cattáneo GR, Izeta AD, Costa T. El patrimonio arqueológico de los espacios rurales de la provincia de Córdoba. 2nd ed.—Córdoba: Universidad Nacional de Córdoba; 2015.
- 63. Lafaille ME. Geografía y política. La gobernación de Tucumán en 1582, según la Relación de Pedro Sotelo Narváez. Anu Jurí y Econ Escu. 2012 Jan 1(45):581.
- 64. Franklin William L. "Contrasting socioecologies of South America’s wild camelids: the vicuna and the guanaco." Advances in the study of mammalian behavior (Eisenberg JF and Kleiman DG, eds.). Special Publication 7 1983: 573–629.
- 65. Metcalf JL, Turney C, Barnett R, Martin F, Bray SC, Vilstrup , et al. Synergistic roles of climate warming and human occupation in Patagonian megafaunal extinctions during the Last Deglaciation. Science adv. 2016. 2(6), e1501682.
- 66. González BA, Palma RE, Zapata B, Marín JC. Taxonomic and biogeographical status of guanaco Lama guanicoe (Artiodactyla, Camelidae). Mam Rev. 2006 Apr 1; 36(2):157–78.
- 67. Río ME, Achával L. Geografía de la Provincia de Córdoba Vol I. Buenos Aires: Compañía sud-americana de billetes de banco; 1904. pp. 570.
- 68. Mengoni Goñalons GL. Fur trade and guanaco hunting in Patagonia during historic times. In: Izeta AD, editor. Abstracts ICAZ 2014. 12th International Conference of Archaeozoology. San Rafael, Argentina. 1st ed: Córdoba. Universidad Nacional de Córdoba; 2014. pp. 108.
- 69. Nacuzzi LR. Los grupos nómades de la Patagonia y el Chaco en el siglo XVIII: identidades, espacios, movimientos y recursos económicos ante la situación de contacto. Una reflexión comparativa. Chungará (Arica), 2007. 39(2):221–234.