INTRODUCTION

In the Bolivian Gran Chaco, woody plant encroachment (WPE) is causing a structural change in grassland and savannah communities and consequently affecting animal species dependant on the quantity and quality of those habitats (Archer et al. 2017). Consequently, as WPE advances and the native grasslands give way to early and later stages of encroachment, animal species naturally adapted to an open habitat may require rapid adaptation to newer and denser environments or suffer habitat displacement (Grant et al. 2004; Sirami et al. 2009; Sauer & Link 2011; Sirami & Monadjem 2012; Archer et al. 2017). Despite its ecological relevance, and the long-term declines in the abundance and distribution of many grassland species (Skowno & Bond 2003; Coppedge 2004; Sirami & Monadjem 2012), very few studies have tackled the response effects of WPE-driven habitat transformation on animal species behaviour.

In general, habitat selection by herbivores should be influenced by the structure and composition of the vegetation, especially as a more vertical habitat structuring reduces visibility and hence capacity of said herbivores to detect a predator (Lima 1987). Therefore, if the vegetation structure is integral to the provision of effective visual scanning enabling, in turn, substantial rates of escape from predators (Elgar 1989; Laundre et al. 2001; Beauchamp 2003, 2008; Li & Jiang 2008; Riginos & Grace 2008), one expects that WPE will lower those probabilities for animals that inhabit affected areas (Mannan & Steidl 2013; Archer et al. 2017). Indeed, antipredator responses amongst ungulates vary greatly depending on several factors, among those are habitat structure and composition (Creel et al. 2014). Examples of the latter are altering their level of vigilance or patterns of aggregation (Prins & Iason 1989; Hunter & Skinner 1998; Caro 2005; Creel & Winnie 2005; Taraborelli et al. 2014) under high and low levels of predation risk, such as in the case of a large ungulate in South America, the guanaco Lama guanicoe (Marino 2010). In general, guanacos like other ungulates that depends on their visibility to avoid predators are expected to favour open habitats with low vegetation (Sarno et al. 2008). Furthermore, even in Tierra del Fuego Island, at the southernmost tip of the species distribution (Muñoz & Simonetti 2013) where guanacos use the forest comparatively more extensively than in other areas of its distribution, guanacos are mainly grazers and only become browsers due to competition with domestic sheep (Raedeke 1980).

We studied a relict and almost extinct population of guanacos, in the north-eastern fringe of the species range in the Gran Chaco (Cuéllar & Núñez 2009). Whilst the Chacoan population of guanacos persists in an area characterized by a mosaic of vegetation cover with various extents of WPE (Navarro & Fuentes 1999; Pinto & Cuéllar Soto 2017), their distribution is analogous to that of two top guanaco predators, the jaguar (Panthera onca), and puma (Puma concolor) (Maffei et al. 2004; Kelly et al. 2008).

We tested whether guanacos: 1) modify their vigilance behaviour in relation to vegetation structure and 2) vary their escape response according to group size and composition; larger groups being expected to exhibit a lowered tendency for flight than lone individuals or groups with offspring, and 3) responded differently to observers (these approaching either on foot or horseback). We analysed the response of guanacos to human presence as an antipredator response (Taraborelli et al. 2014). Our assumption was that both habitat structure and group size would influence alert response of guanacos living in groups in this changing environment.

MATERIALS AND METHODS

Study area

The study area extends from 19°45’ to 20°30’ S and from 62°00’ to 63°00’ W, on the fluvial megafans of the Río Grande and the Río Parapetí in the Bolivian Gran Chaco (May et al. 2008), in the extreme south of Santa Cruz department, Bolivia. The study area includes the southwest corner of the Kaa-Iya National Park and part of the Indigenous Isoseño Communal Land (see Cuéllar Soto et al. 2020; for a detailed description of the study site). The climate is predominantly semi-arid (Peel et al. 2007), with annual rainfall ranging from 200 to 350 mm (Taber et al. 1997).

Data collection

In a time period of five years (2004-2009), we conducted 693 transect surveys (between 06:00 and 18:00 h) within a survey area of 791km², of which 454 yielded successful observations. Mean transect length was 10.5 km (range: 7-14km), and transects were travelled on foot or on horseback. In addition, we followed Navarro’s classification to deter- mine of stages of WPE in the study area (Navarro & Fuentes 1999; Navarro 2002). We assigned two habitat categories according to vegetation structure: 1) open grassland and scrub constitutes low vegetation cover [heigh around 0.40 m and dominated mainly by Lippia sp. (Verbenaceae), Pappophorum krapovickasii (Poaceae), and Aristida mendocina (Poaceae)]; and 2) shrubland or woody vegetation [heigh around 4 m, dominated by Pithecellobium chacoense (Fabaceae)].

Once the guanacos were encountered we recorded the structure and size of the groups, presence/absence of offspring (chulengos) and their response from the first moment of visual contact. Their responses were classified into two main categories: 1) continuing activity or passive response; and 2) alert response (standing in a vigilant position, alarm call and evasion either by walking or running).

Data analysis

We analysed data gathered on foot and on horseback separately, as we initially detected an observer effect on guanaco response. We performed a logistic regression with three independent predictors: group size, habitat coverage and presence/absence of offspring.

For the statistical analysis, we considered group size as a continuous variable, and we categorised guanaco groups into two categories according to the presence or absence of offspring.

We tested for a relationship between type of alert response (dependent variable) and group size, presence or absence of offspring, and habitat cover (predictor independent variables).

Then we performed logistic regressions to assess the influence of a few factors on the likelihood that guanacos would show an alert response to our presence as an indication of predator avoidance behaviour. We included interaction terms to test, for example, if the effect of group size on the response depended on habitat structure. The statistical analyses were performed with SPSS software (version 18.0; Chicago: SPSS Inc. 2009).

RESULTS

Guanacos appeared to react differently to observers approaching on foot to those approaching on horseback. There was a significant association between observation method and guanaco vigilance response (χ2=44.60, df=1, p=0.00). An alert response was significantly more likely when the approach was on foot than on horseback.

Vigilance response vs. social and habitat variables

The model made significant predictions of an alert response (χ²= 8.73, df=3, p < 0.033). It explained between 3.2% (Cox & Snell R Square) and 4.3% (Nagelkerke R Square) of the variance in guanaco response, and correctly classified 58.1% of cases. Only vegetation structure made a statistically significant contribution to the model (Table 1). The odds ratio for habitat cover was 2.02, indicating that the alert response of guanacos encountered in relatively lower vegetation coverage was about twice as likely as that for high vegetation cover. The odds ratio of 0.90 for the predictor “group size” was <1, indicating that for every additional individual in the group, individual guanacos were 0.9 times less likely to show an alert response, controlling for other factors in the model. There was no evidence that the effect of habitat depended on group size: the interaction term was not statistically significant (χ²=0.01, df=1, p=0. 92). Group size and habitat were not confounded predictors: mean group sizes in both open and closed habitat are similar (Mean_(low)=3.10, SE=0.15; Mean_(high)= 3.02, SE=0.21). The model made no significant predictions of an alert response on a set of 164 observations made on horseback (χ²= 3.95, df=3, p=0.266).

Social structure

From the accumulated observations we identified three forms of guanaco social organisation: adults only, family groups (with one or two offspring), and solitary individuals (male or female). The mean group size was 2.8 (SD±1.8). Solitary adults andsolitary juveniles (female or male) were observedmore often than larger groups (Fig. 1).

DISCUSSION

In our study, we found vegetation cover to be the strongest predictor of an alert response which, in turn, was not affected by whether guanacos were alone or in groups. Contrary to our expectation, guanacos were twice as responsive in what we classified as open areas, these being relatively scarce and forming a patchwork surrounded by areas of dense cover.

Cuéllar Soto et al. (2020) have previously reported that, for guanacos, forage areas of preference were limited to patches of open vegetation. Perhaps guanacos in our study area have greater perceptions of risk in open habitats, because there were surrounded by thick vegetation. Therefore, represent a high risk for guanacos due to potential ambush from predators (Bank et al. 2002, 2003). Consequently, guanacos may consider these open areas to be more dangerous than denser areas, which could be perceived as counter- intuitive due to heightened anxiety when nearer cover, potential ambush sites, in proper grasslands. Furthermore, if poor visibility, associated with high vegetation cover, increases risk of predation then this should drive adaptations for increased vigilance regardless of group size. This latter point contrasts with the general ecological concept that group size is an important factor determining vigilance patterns in mammalian herbivores (Elgar 1989; Lima & Dill 1990; Childress & Lung 2003; Lung & Childress 2006; Marino & Baldi 2008). However, additional, and specific information need to be collected in order to confirm whether the current small groups and solitary individuals have a similar response (Taraborelli et al. 2019).

During the course of our investigation, we encountered solitary individuals, both males and females, more frequently than groups (Fig. 1). Given the polygynous nature typical to guanacos (Franklin 1983), and the importance of territoriality and site fidelity (Young & Franklin 2004), lone males are unlikely to secure mating opportunities with females. Although they are sometimes seen briefly with solitary territorial males after the end of the mating period, females are thought to be receptive only to territorial males within family groups (Franklin 1982, 1983). However, additional data is required to confirm mating success, birth rates, juvenile mortality rates, and emigration or dispersal rates related to the lack of open areas from WPE.

Establishing a guanaco alertness rating gives us a proxy for how anxious they may feel or how they perceive risk in a changing landscape. Regardless of the method used, guanacos invariably moved away within two minutes of being sighted. This contrasts with observations in open habitats of Argentina, where guanacos do not flee after having detected observers (Marino & Baldi 2008; Taraborelli et al. 2014) or become rapidly habituated if harassment ceases as reported in a guanaco population inhabiting Argentinean Patagonian arid lands (Marino & Johnson 2012). However, the response from Chacoan guanacos could be just different given their unique current woody environment, or natural history as mentioned by Stankowich (2008). Our method of searching for guanacos in open environments dif- fered greatly from the standard transect methods used elsewhere, such as Patagonian steppe (Novaro et al. 2000; Franklin & Grigione 2005; Marino & Baldi 2008; Schroeder et al. 2013), Andean foothills (Bank et al. 2003), or Puna plateaux (Lucherini 1996), or the Monte desert (Acebes et al. 2010). Overall visibility and access, in all these latter cases, were very much greater compared to our study site where we observed that within 5m of relatively open areas, there could be several intermediate stages of WPE, each offering various amounts of cover. Therefore, the dominant category, in our observations (a low vegetation mix of open grass and scrubland) is likely to have been considered as high vegetation cover, by guanacos, in other distinct areas of their distribution range.

Although hunting had stopped in the study area by 2001, guanacos responded differently to human observers depending on whether they were approached on foot or on horseback. Apparently, guanacos were still very much wary of human presence, as they are reported to be elsewhere when subjected to strong hunting pressure (Donadio & Buskirk 2006). We conclude that this difference in response was based on the history of harassment as reported for other species by Stankowich (2008) by sport hunters rather than the presence of domestic ungulates which are becoming more frequently in the guanaco distribution range. Aside from people, the guanaco’s only other important predator, outside the Gran Chaco region, is the puma (Wilson 1984; Bank & Franklin 1998; Novaro et al. 2000; Bank et al. 2003; Marino & Baldi 2008). Although we have no specific data to show that the response behaviour of guanacos was linked to predation, we found evidence that both jaguars and pumas occurred within the same study area, and that, similar to guanacos, were diurnally active (Cuéllar Soto & Noss 2014).

The combination of facts that, in the last few decades, the Chacoan population of guanacos has been severely reduced to a small number and its potential primary habitat transformed due to WPE (Cuéllar Soto et al. 2017) deserves attention and action for rigorous protection and conservation ef- forts. Furthermore, specific parallel studies need to be conducted to test whether management of WPE may improve visibility and benefit guanacos in their detection of predators given that, even within relatively open environments, guanacos concentrated in areas with the sparsest vegetation cover.

Acknowledgments

U.F.J Pardiñas kindly reviewed the Spanish abstract and D. Voglino helped with the edition of the FIgure. A. J Noss, and L. James contributed in different phases of the project. We are grateful to several institutions for providingfunds, The Wildlife Conservation Society, The Gordonand Betty Moore Foundation within the Amazon-Andes Conservation Program (AACP), The Shared EarthFoundation, Whitley Fund for nature, and Kaa-IyaFoundation. We also thank the para-biologists and parkrangers from the Kaa-Iya national park. Carlos Galliari and U.F.J Pardiñas kindly reviewed the Spanish abstract and D. Voglino helped with the edition of the figure. A. J Noss, and L. James contributed in different phases of the project.

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Información adicional

Editor asociado: C. A. Galliari

Cite as: Cuéllar Soto, E. & J. Segundo. 2021. Alert response of guanacos in the Bolivian Gran Chaco is affected by a changing environment driven by woody plant encroachment. Mastozoología Neotropical, 28(1):e0555. https://doi.org/10.31687/saremMN.21.28.1.0.27