Skip to main content
SpringerLink
Log in

Different factors that modify anti-predator behaviour in guanacos (Lama guanicoe)

  • Original Paper
  • Published:
Acta Theriologica Aims and scope Submit manuscript

Abstract

Animals optimize the trade-off between the cost of not fleeing and the benefits of staying because the factors that influence flight decisions and the disturbance level of a particular stimulus can vary both spatially and temporally. Different factors (human impact and habitat characteristics) likely to modify anti-predator behaviour in different types of guanaco social groups were analysed. We found that group size was conditioned by high poaching, vehicle traffic, predation risk and vegetation density. Solitary adult males showed shorter alert and flight initiation distances than bachelor and mixed groups. Alert distance was greater during the summer season, and assessment times were shorter when young were present in the groups. In high-predation-risk environments, guanacos detected threats at greater distances and flight initiation distance was longer. Alert distances were shorter on steeper sloped hills and assessment times were shorter in areas with irregular topography than on flat sites. In high traffic areas, flight initiation distance was longer and assessment times were shorter. And in areas with low poaching intensity, assessment times were greater than in those with high poaching levels. Therefore, guanacos may be able to evaluate a true threat. Social group and anti-predator responses were conditioned by habitat characteristics and human impact. We consider that plasticity of responses could be key to the survival of guanacos.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aastrup P (2000) Responses of West Greenland caribou to the approach of humans on foot. Polar Res 19:83–90

    Article  Google Scholar 

  • Akaike H (1974) A new look at statistical model identification. IEEE Trans Autom Control AU 19:716–722

    Article  Google Scholar 

  • Alcock J (2005) Animal behavior. An evolutionary approach. Sinauer Associates, Inc. Arizona State University, Arizona

    Google Scholar 

  • Aros LA, Quiroga LE (2012) Protección integral de la fauna silvestre desde las Áreas protegidas, sistematización y análisis de la información, áreas naturales protegidas de zona sur de Mendoza, Argentina. X Congreso Internacional de Manejo de Fauna Silvestre en la Amazonia y América Latina. Ciudad de Salta, Salta, Argentina

  • Bank MS, Franklin WL (1998) Puma (Puma concolor patagonica) feeding observations and attacks on guanacos (Lama guanicoe). Mammalia 62:599–605

    Google Scholar 

  • Bank MS, Sarno RJ, Campbell NK, Franklin WL (2002) Predation of guanacos (Lama guanicoe) by southernmost mountain lions (Puma concolor) during a historically severe winter in Torres del Paine National Park, Chile. J Zool 258:215–222

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B (2011) lme4: linear mixed-effects models using S4 classes. R package version 0.999375-42

  • Benhaiem S, Delon M, Lourtet B, Cargnelutti B, Aulagnier S, Hewison AJM, Morellet N, Verheyden H (2008) Hunting increases vigilance levels in roe deer and modifies feeding site selection. Anim Behav 76:611–618

    Article  Google Scholar 

  • Beyer HL, Merrill EH, Varley N, Boyce M (2007) Willow on Yellowstone’s northern range: evidence for a trophic cascade? Ecol Appl 17:1563–1571

    Article  PubMed  Google Scholar 

  • Birke L, Hockenhull J, Creighton E, Pinno L, Mee J, Mills D (2011) Horses’ responses to variation in human approach. Appl Anim Behav Sci 134:56–63

    Article  Google Scholar 

  • Blumstein DT (2003) Flight-initiation distance in birds is dependent on intruder starting distance. J Wildl Manag 67:852–857

    Article  Google Scholar 

  • Bolgeri MJ, Novaro A (2010) Patrones de depredación (Puma concolor) sobre una población de guanacos (Lama guanicoe) en Payunia, Mendoza. IV Reunión Binacional de Ecología. Buenos Aires, Argentina

  • Bolker B (2012) Package “bbmle”. http://cran.r-project.org/web/packages/bbmle/bbmle.pdf

  • Cajal JL, Lopez NE (1987) El puma como depredador de camélidos silvestres en la Reserva San Guillermo, San Juan, Argentina. Rev Chil Hist Nat 60:87–91

    Google Scholar 

  • Candia R, Puig S, Dalmasso A, Videla F, Martínez Carretero E (1993) Plan de Manejo de la Reserva La Payunia. Multequina 2:5–87

    Google Scholar 

  • Carmanchahi PDA, Ovejero RA, Marull CC, López GCD (2011) Physiological response of wild guanacos to capture for live shearing. Wildl Res 38:61–68

    Article  Google Scholar 

  • Caro TM, Graham CM, Stoner CJ, Vargas JK (2004) Adaptive significance of antipredator behaviour in artiodactyls. Anim Behav 67:205–228

    Article  Google Scholar 

  • Carranza J (2000) Etología. Introducción a la Ciencia del Comportamiento. Universidad de Extremadura, Madrid

    Google Scholar 

  • Colman JE, Lilleeng MS, Tsegaye D, Vigeland MD, Reimers E (2012) Responses of wild reindeer (Rangifer tarandus tarandus) when provoked by a snow-kiter or skier: a model approach. Appl Anim Behav Sci 142:82–89

    Article  Google Scholar 

  • Cooper WE, Frederick WG (2007) Optimal flight initiation distance. J Theor Biol 244:59–67

    Article  PubMed  Google Scholar 

  • de Boer HY, van Breukelen L, Hootsmans MJM, van Wieren SE (2004) Flight distance in roe deer Capreolus capreolus and fallow deer Dama dama as related to hunting and other factors. Wildl Biol 10:35–41

    Google Scholar 

  • Dirección de Recursos Naturales Renovables (2012) Informe Programa de Control y Vigilancia Zona Sur 2011-PCV. Secretaría de Ambiente y Desarrollo sustentable

  • Donadio E, Buskirk SW (2006) Flight behavior in guanacos and vicuñas in areas with and without poaching in western Argentina. Biol Conserv 127:139–214

    Article  Google Scholar 

  • Donadio E, Novaro AJ, Buskirk SW, Wurstten A, Vitali MS, Monteverde MJ (2010) Evaluating a potentially strong trophic interaction: pumas and wild camelids in protected areas of Argentina. J Zool 280:33–40

    Article  Google Scholar 

  • Dwyer CM (2004) How has the risk of predation shaped the behavioural responses of sheep to fear and distress? Anim Welf 13:269–281

    CAS  Google Scholar 

  • Fiori SM, Zalba SM (2003) Potential impacts of petroleum exploration and exploitation on biodiversity in a Patagonian Nature Reserve, Argentina. Biodivers Conserv 12:1261–1270

    Article  Google Scholar 

  • Fortin D, Andruskiw M (2003) Behavioral response of free-ranging bison to human disturbance. Wildl Soc B 31:804–813

    Google Scholar 

  • Franklin WL (1982) Lama language. Modes of communication in the South American camelids. Llama World 1:5–11

    Google Scholar 

  • Franklin WL (1983) Contrasting socioecologies of South America’s wild camelids: the vicuña and the guanaco. In: Eisenberger SF, Kleinman DG (eds) Advances in the study of mammalian behavior. American Society of Mammals, USA, N7, pp 573–629

  • Frid A (1997) Vigilance by female Dall’s sheep: interactions between predation risk factors. Anim Behav 53:799–808

    Article  Google Scholar 

  • Frid A, Dill L (2002) Human-caused disturbance stimuli as a form of predation risk. Conservation Ecology, 6, Online article #11: http://www.consecol.org/vol16/iss11/art11

  • Gabrielsen GW, Smith EN (1995) Physiological responses of wildlife to disturbance. In: Gabrielsen GW, Smith EN (eds) Wildlife and recreationists: coexistence through management and research. Island Press, Washington, DC, pp 95–107

    Google Scholar 

  • González Díaz EF (1972) Descripción geológica de la Hoja 30-d, Payún Matru (Mendoza). Carta Geológica Económica de la República Argentina, Boletín 130. Dirección Nacional de Geología y Minería, Buenos Aires

  • Hoogland JL (1981) The evolution of coloniality in white-tailed and black-tailed prairie dogs (Sciuridae: Cynomys leucurus and C. ludovicianus). Ecology 62:252–272

    Article  Google Scholar 

  • Ims RA, Yaccoz NG (1997) Ecological methodology: study design and statistical analysis. University of Oslo, Norway

    Google Scholar 

  • Jeppesen JL (1987) Impact of human disturbance on home range movements and activity of red deer Cervus elaphus in a Danish environment. Dan Rev Game Biol 13:1–38

    Google Scholar 

  • Kilgo JC, Labisky RF, Fritzen DE (1998) Influences of hunting on the behavior of white-tailed deer: implications for conservation of the Florida panther. Conserv Biol 12:1359–1364

    Article  Google Scholar 

  • Kufeld RC, Bowden DC, Schrupp DL (1988) Influence of hunting on movements of female mule deer. J Range Manag 41:70–72

    Article  Google Scholar 

  • LaGory KE (1987) The influence of habitat and group characteristics on the alarm and flight response of white-tailed deer. Anim Behav 35:20–25

    Article  Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  • Lingle S, Pellis SM (2002) Fight or flight? Antipredator behavior and the escalation of coyote encounters with deer. Oecologia 131:154–164

    Article  Google Scholar 

  • Lingle S, Wilson WF (2001) Detection and avoidance of predators in white-tailed deer (Odocoileus virginianus) and mule deer (O. hemionus). Ethology 107:125–147

    Article  Google Scholar 

  • Maki AW (1992) Of measured risk: the environmental impacts of the Prudhoe Bay, Alaska, oil field. Annu Rev Environ Toxicol Chem 11:1691–1707

    Article  CAS  Google Scholar 

  • Malo JE, Acebes P, Traba J (2011) Measuring ungulate tolerance to human with flight distance: a reliable visitor management tool? Biodivers Conserv 20:3477–3488

    Article  Google Scholar 

  • Marino A, Baldi R (2008) Vigilance patterns of territorial guanacos (Lama guanicoe): the role of reproductive interests and predation risk. Ethology 114:413–423

    Article  Google Scholar 

  • Marino A, Johnson A (2012) Behavioural response of free-ranging guanacos (Lama guanicoe) to land-use change: habituation to motorised vehicles in a recently created reserve. Wildl Res 39:503–511

    Google Scholar 

  • Martínez Carretero E (2004) Provincia Fitogeográfica de la Payunia. Bol Soc Argent Bot 39:195–223

    Google Scholar 

  • Martínez E, Dalmasso A (1993) Flora y vegetación. Diseño del plan de manejo para la Reserva La Payunia (Mendoza, Argentina). Multequina 2:19–22

  • Miller KA, Garner JP, Mench JA (2006) Is fearfulness a trait that can be measured with behavioural tests? A validation of four fear tests for Japanese quail. Anim Behav 71:1323–1334

    Article  Google Scholar 

  • Pearce JM (2008) Animal learning & cognition. An introduction, 3rd edn. Psychology Press, Hove

    Google Scholar 

  • Picton HD (1999) Energetic cost of wildlife displacement by winter recreationists. In: Olliff T, Legg K, Kaeding B (eds) Effects of winter recreation on wildlife of the Greater Area: a literature review and assessment. Report to the Greater Yellowstone Coordinating Committee. Yellowstone National Park, Wyoming, pp 135–144

    Google Scholar 

  • Pomerantz GA, Decker DJ, Goff GR, Purdy KG (1988) Assessing impact of recreation on wildlife: a classification scheme. Wildl Soc B 16:58–62

    Google Scholar 

  • Puig S, Videla F, Cona MI, Monge SA (1996) Use of food availability by guanaco (Lama guanicoe) and livestock in Northern Patagonia (Mendoza, Argentina). J Arid Environ 47:291–308

    Article  Google Scholar 

  • Puig S, Videla F, Cona M (1997) Diet and abundance of the guanaco (Lama guanicoe) in four habitats of northern Patagonia, Argentina. J Arid Environ 36:343–357

    Article  Google Scholar 

  • Puig S, Videla F, Cona MI, Monge SA (2001) Use of food availability by guanacos (Lama guanicoe) and livestock in Northern Patagonia (Mendoza, Argentina). J Arid Environ 47:291–308

    Article  Google Scholar 

  • Puig S, Ferraris G, Superina M, Videla F (2003) Distribución de densidades de guanacos (Lama guanicoe) en el norte de la Reserva La Payunia y su área de influencia (Mendoza, Argentina). Multequina 12:37–48

    Google Scholar 

  • Recarte JM, Vincent JP, Hewison AJM (1998) Flight responses of park fallow deer to the human observer. Behav Process 14:65–72

    Article  Google Scholar 

  • Ripple JW, Beschta RL (2008) Trophic cascades involving cougar, mule deer, and black oaks in Yosemite National Park. Biol Conserv 141:1249–1256

    Article  Google Scholar 

  • Sarno RJ, Grigione MM, Arvidson LD (2008) Lack of response of an open-habitat ungulate to the presence of predator urine. Rev Chil Hist Nat 81:179–183

    Article  Google Scholar 

  • Sawyer H, Nielson R, Lindzey F, Mcdonald LL (2006) Winter habitat selection of mule deer before and during development of a natural gas field. J Wildl Manag 70:396–403

    Article  Google Scholar 

  • Sawyer H, Kauffman M, Nielson RM (2009) Influence of well pad activity on winter habitat selection patterns of mule deer. J Wildl Manag 73:1052–1061

    Article  Google Scholar 

  • Schroeder N (2013) Interacción entre el guanaco (Lama guanicoe) y herbívoros domésticos en el paisaje de La Payunia (sur de Mendoza, Argentina). PhD thesis, Universidad Nacional de Cuyo, Mendoza, Argentina

  • Schroeder N, Ovejero R, Moreno P, Gregorio P, Taraborelli P, Matteucci S, Carmanchahi P (2013) Including species interactions in resource selection of guanacos and livestock in Northern Patagonia. J Zool 291:213–225

    Article  Google Scholar 

  • Stankowich T (2008) Ungulate flight responses to human disturbance: a review and meta-analysis. Biol Conserv 141:2159–2173

    Article  Google Scholar 

  • Stankowich T, Blumstein DT (2005) Fear in animals: a review and meta-analysis of risk assessment. P Roy Soc B Biol Sci 272:2627–2634

    Article  Google Scholar 

  • Stankowich T, Coss RG (2006a) Effects of predator behavior and proximity on risk assessment by Columbian black-tailed deer. Behav Ecol 17:246–254

    Article  Google Scholar 

  • Stankowich T, Coss RG (2006b) Effects of risk assessment, predator behavior, and habitat on escape behavior in Columbian black-tailed deer. Behav Ecol 18:358–367

    Article  Google Scholar 

  • Stankowich T, Coss RG (2007) The re-emergence of felid camouflage with the decay of predator recognition in deer under relaxed selection. P Roy Soc B Biol Sci 274:175–182

    Article  Google Scholar 

  • Steneck RS (2005) An ecological context for the role of large carnivores in conserving biodiversity. In: Ray JC, Redford KH, Steneck RS, Berger J (eds) Large carnivores and the conservation of biodiversity. Island Press, Washington, DC, pp 9–33

    Google Scholar 

  • Swenson JE (1982) Effects of hunting on habitat use by mule deer on mixed-grass prarie in Montana. Wildl Soc B 10:115–120

    Google Scholar 

  • Taraborelli P, Gregorio P, Moreno P, Novaro A, Carmanchahi P (2012) Cooperative vigilance: the guanaco’s (Lama guanicoe) key antipredator mechanism. Behav Process 91:82–89

    Article  Google Scholar 

  • Taylor AR, Knight RL (2003) Wildlife responses to recreation and associated visitor perceptions. Ecol Appl 13:951–963

    Article  Google Scholar 

  • Wilson P (1984) Puma predation on guanacos in Torres del Paine National Park, Chile. Mammalia 48:515–522

    Article  Google Scholar 

  • Wirsing AJ, Cameron KE, Heithaus MR (2010) Spatial responses to predators vary with prey escape mode. Anim Behav 79:531–537

    Article  Google Scholar 

Download references

Acknowledgments

This study was partially financed by CONICET, PIP 11220100100100386, Agencia-FONCYT, PICT-2010-1305 and PICT-2011-2304. Equipment was partially financed by IDEA WILD. The authors wish to express their thanks to the park rangers of the natural protected areas of the southern zone (Malargüe Department, Mendoza, Argentina) for information regarding poaching index. Thanks also to ME Periago and N Horak for the English version of the manuscript. Special thanks to MJ Bolgeri for information about predation risk at La Payunia Reserve.

Author information

Authors and Affiliations

  1. Laboratorio de Desertificación y Ordenamiento Territorial (LaDyOT), IADIZA, CCT-Mendoza, CONICET, Av. Ruiz Leal s/n, Parque General San Martín, Mendoza ciudad, CC 507, 5500, Argentina

    P. Taraborelli

  2. Grupo de Investigación en Ecofisiología de Fauna Silvestre (GIEFAS), AUSMA–INIBIOMA–CONICET–UNCo, San Martín de los Andes, Neuquén, Argentina

    P. Taraborelli, R. Ovejero, N. M. Schroeder, P. Moreno, P. Gregorio, A. Marozzi & P. Carmanchahi

  3. Grupo de Investigaciones de la Biodiversidad (GIB), IADIZA, CCT-Mendoza, CONICET, Mendoza, Argentina

    M. E. Mosca Torres

  4. Lab. de Interacciones Ecológicas, IADIZA, CCT-Mendoza, CONICET, Mendoza, Argentina

    N. M. Schroeder

  5. Lab. de Ecología de Enfermedades, Fac. Cs. Veterinarias, Universidad Nacional del Litoral, Esperanza, Santa Fe, Argentina

    P. Moreno

  6. Unidad de Dendrocronología, IANIGLA, CCT-Mendoza, CONICET, Mendoza, Argentina

    E. Marcotti

Authors
  1. P. Taraborelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Ovejero
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. E. Mosca Torres
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. M. Schroeder
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P. Moreno
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. P. Gregorio
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. E. Marcotti
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. A. Marozzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. P. Carmanchahi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. Taraborelli.

Additional information

Communicated by: Rafał Kowalczyk

Appendix

Appendix

Table 5 A priori generalized linear mixed-effects models for group size, alert distance, flight initiation distance, and assessment time in guanacos. Only fixed effects are presented. The most parsimonious model is presented first (i.e. models are ranked in descending order after AIC value)
Full size table

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Taraborelli, P., Ovejero, R., Mosca Torres, M.E. et al. Different factors that modify anti-predator behaviour in guanacos (Lama guanicoe). Acta Theriol 59, 529–539 (2014). https://doi.org/10.1007/s13364-014-0186-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13364-014-0186-9

Keywords

Search

Navigation