Advertisement

Home Range and Daily Traveled Distances of Highland Colombian Woolly Monkeys (Lagothrix lagothricha lugens): Comparing Spatial Data from GPS Collars and Direct Follows

  • Leidy Carolina García-ToroEmail author
  • Andrés Link
  • Elsy Johanna Páez-Crespo
  • Pablo R. Stevenson
Chapter

Abstract

Space requirements are essential to assess population ecology especially for endangered species. The goal of this study was to estimate home range size and daily traveled distances (DTD) of two groups of woolly monkeys using two different sampling methods: direct observations of focal animals using handheld GPS devices and GPS collars located on four individuals. Our research questions were: (1) Are there differences in the estimates of home range size and DTD between methods? (2) In case of differences, are topography and trail locations associated with sampling bias? (3) What is the appropriate sampling interval to obtain statistically independent data? Highland woolly monkey home ranges and their DTD were underestimated by direct observations of focal animals using handheld GPS devices. Direct observations were affected by the rugged topography of the study site and were infrequent away from the trail system. In contrast, the use of GPS collars, it was costly but useful to obtain reliable data on space use by highland woolly monkeys. By using GPS collar was possible to track both study groups continuously with high quality and precision and covering broad geographic areas. Finally, our results demonstrated that the independence of observations for statistical purposes was reached after a 5-h sampling.

Keywords

Highland woolly monkey Lagothrix lagothricha Daily Traveled distances 

References

  1. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267CrossRefGoogle Scholar
  2. Boyle SA, Lourenço WC, Da Silva LR, Smith AT (2009) Travel and spatial patterns change when Chiropotes satanas chiropotes inhabit forest fragments. Int J Primatol 30:515–531CrossRefGoogle Scholar
  3. Buckland ST, Plumptre AJ, Thomas L, Rexstad EA (2010) Design and analysis of line transect surveys for primates. Int J Primatol 31:833–847CrossRefGoogle Scholar
  4. Camus PA, Lima M (1995) El uso de la experimentación en ecología: supuestos, limitaciones, fuentes de error y su status como herramienta explicativa. Rev Chil Hist Nat 68:19–42Google Scholar
  5. Cifuentes E, Ramírez M, León J, Galvis N, Vargas S, Stevenson P (2013) Dieta de los churucos colombianos (Lagothrix lagothricha lugens) en relación con la productividad de frutos en el Parque nacional natural Cueva de Los Guácharos. In: Defler TR, Stevenson PR, Bueno ML, Guzmán-Caro DC (eds) Primates colombianos en peligro de extinción. Asociación primatológica colombiana Bogotá, pp 294–312Google Scholar
  6. Cresswell WJ, Smith GC (1992) The effects of temporally autocorrelated data on methods of home range analysis. In: Priede IG, Swift SM (eds) Wildlife telemetry: remote monitoring and tracking of animals. Ellis Horwood, Chichester, pp 272-284Google Scholar
  7. Cunningham EP, Unwin S, Setchell JM (2015) Darting primates in the field: a review of reporting trends and a survey of practices and their effect on the primates involved. Int J Primatol 36(5):894–915CrossRefGoogle Scholar
  8. Cuthill IC (1991) Field experiments in animal behavior: methods and ethics. Anim Behav 42:1007–1101CrossRefGoogle Scholar
  9. D’Eon RG, Serrouya R, Smith G, Kochanny CO (2002) GPS radiotelemetry error and bias in mountainous terrain. Wildl Soc Bull 30:430–439Google Scholar
  10. Defler TR (1996) Aspects of the ranging pattern in a group of wild woolly monkeys (Lagothrix lagothricha). Am J Primatol 38(4):289–302CrossRefGoogle Scholar
  11. Defler TR (2010) Historia natural de los primates colombianos. Universidad Nacional de Colombia, BogotáGoogle Scholar
  12. Di Fiore A (2003) Ranging behavior and foraging ecology of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in Yasuni National Park, Ecuador. Am J Primatol 59:47–66CrossRefGoogle Scholar
  13. Di Fiore A, Fleischer RC (2005) Social behavior, reproductive strategies, and population genetic structure of Lagothrix poeppigii. Int J Primatol 26(5):1137–1173CrossRefGoogle Scholar
  14. Di Fiore A, Rodman PS (2001) Time allocation patterns of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in a neotropical terra firma forest. Int J Primatol 22(3):449–480CrossRefGoogle Scholar
  15. Di Fiore A, Suarez SA (2007) Route-based travel and shared routes in sympatric spider and woolly monkeys: cognitive and evolutionary implications. Anim Cogn 10:317–329CrossRefGoogle Scholar
  16. Di Fiore A, Link A, Schmitt CA, Spehar SN (2009) Dispersal patterns in sympatric woolly and spider monkeys: integrating molecular and observational data. Behaviour 146(4):437–470CrossRefGoogle Scholar
  17. Di Orio AP, Callas R, Schaefer RJ (2003) Performance of two GPS telemetry collars under different habitat conditions. Wildl Soc Bull 31:372–379Google Scholar
  18. Fedigan LM (2010) Ethical issues faced by field primatologists: asking the relevant questions. Am J Primatol 72(9):754–771CrossRefGoogle Scholar
  19. Fedigan LM, Fedigan L, Chapman C, Glander KE (1988) Spider monkey home ranges: a comparison of radio telemetry and direct observation. Am J Primatol 16(1):19–29CrossRefGoogle Scholar
  20. Fernandez-Duque M, Chapman CA, Glander KE, Fernandez-Duque E (2017) Darting primates: steps toward procedural and reporting standards. Int J Primatol 39:1–8CrossRefGoogle Scholar
  21. Fernandez-Duque E, Rotundo M (2003) Field methods for capturing and marking Azarai night monkeys. Int J Primatol 24(5):1113–1120CrossRefGoogle Scholar
  22. Fleagle JG (1999) Primate adaptation and evolution. Academic, San DiegoGoogle Scholar
  23. González M, Stevenson PR (2010) Comparación de los patrones de movimiento diario, actividad y dieta, reportados para los micos churucos (Lagothrix lagothricha): diferencias producto de la oferta de frutos y de la metodología usada. In: Pereira-Bengoa V, Stevenson PR, Bueno ML, Nassar-Montoya F (eds) Primatología en Colombia: avances al principio del milenio. Fundación Universitaria San Martín, Bogotá, pp 3–18Google Scholar
  24. Harris S, Cresswell WJ, Forde PG, Trewhella WJ, Woollard T, Wray S (1990) Home-range analysis using radio-tracking data–a review of problems and techniques particularly as applied to the study of mammals. Mammal Rev 20(2–3):97–123CrossRefGoogle Scholar
  25. Hebblewhite M, Haydon DT (2010) Distinguishing technology from biology: a critical review of the use of GPS telemetry data in ecology. Philos Trans R Soc B 365(1550):2303–2312CrossRefGoogle Scholar
  26. Hilpert AL, Jones CB (2005) Possible costs of radio-tracking a young adult female mantled howler monkey (Alouatta palliata) in deciduous habitat of Costa Rican tropical dry forest. J Appl Anim Welf Sci 8(3):227–232CrossRefGoogle Scholar
  27. Holyoak E, Casagrandi R, Nathan R, Revilla E, Spiegel O (2008) Trends and missing parts in the study of movement ecology. Proc Natl Acad Sci 105(49):1060–19065CrossRefGoogle Scholar
  28. Hopkins ME, Milton K (2016) Adverse effects of ball-chain radio-collars on female mantled howlers (Alouatta palliata) in Panama. Int J Primatol 37(2):213–224CrossRefGoogle Scholar
  29. Janmaat KR, Olupot W, Chancellor RL, Arlet ME, Waser PM (2009) Long-term site fidelity and individual home range shifts in Lophocebus albigena. Int J Primatol 30:443–466CrossRefGoogle Scholar
  30. Juarez CP, Rotundo MA, Berg W, Fernández-Duque E (2011) Costs and benefits of radio-collaring on the behavior, demography, and conservation of owl monkeys (Aotus azarai) in Formosa, Argentina. Int J Primatol 32(1):69–82CrossRefGoogle Scholar
  31. Kenward RE (1992) Quantity versus quality: programmed collection and analysis of radio-tracking data. In: Priede IG, Swift SM (eds) Wildlife telemetry: remote monitoring and tracking of animals. Ellis Horwood, New York, pp 231–245Google Scholar
  32. Kernohan BJ, Gitzen RA, Millspaugh JJ (2001) Analysis of animal space use and movements. In: Millspaugh JJ, Marzluff JM (eds) Radio tracking and animal populations. Academic, New York, pp 15–166Google Scholar
  33. Legendre P (1993) Spatial autocorrelation: trouble or new paradigm? Ecology 74(6):1659–1673CrossRefGoogle Scholar
  34. Lewis JS, Rachlow JL, Garton EO, Vierling LA (2007) Effects of habitat on GPS collar performance: using data screening to reduce location error. J Appl Ecol 44:663–671CrossRefGoogle Scholar
  35. Lizcano DJ, Ahumanda JA, Nishimura A, Stevenson PR (2014) Population viability analysis of woolly monkeys in western amazonia; the woolly monkey developments in primatology. Prog Prospects 39:267–282Google Scholar
  36. Manly BFJ, McDonald LL, Thomas DL (1993) Resource selection by animals: statistical desing and analysis for field studies. Chapman and Hall, London, p 177CrossRefGoogle Scholar
  37. Markham AC, Altmann J (2008) Remote monitoring of primates using automated GPS technology in open habitats. Am J Primatol 70:495–499CrossRefGoogle Scholar
  38. Moen R, Pastor J, Cohen Y, Schwartz CC (1996) Effects of moose movement and habitat use on GPS collar performance. J Wildl Manag 60:659–668CrossRefGoogle Scholar
  39. Moorcroft PR, Lewis MA (2006) Mechanistic home range analysis. Monographs in population biology. Princeton University Press, PrincetonGoogle Scholar
  40. Müller KH, Schildger J (1994) Capture and radio-telemetry of masked titi monkeys, Callicebus personatus melanochir. Neotropical Primates 2(4):7–8Google Scholar
  41. Nathan R, Getz WM, Revilla E, Holyoak M, Kadmon R, Saltz D, Smouse PE (2008) A movement ecology paradigm for unifying organismal movement research. Proc Natl Acad Sci 105(49):19052–19059CrossRefGoogle Scholar
  42. Nishimura A (1990) A sociological and behavioral study of woolly monkeys, Lagothrix lagothricha in the upper Amazon. Sci Eng Rev Doshiosha Univ 31:1–121Google Scholar
  43. Nishimura A (1994) Social interaction patterns of woolly monkeys (Lagothrix lagotricha): a comparison among the atelines. Sci Eng Rev Doshisha Univ 35:236–254Google Scholar
  44. Nishimura A (2003) Reproductive parameters of wild female Lagothrix lagotricha. Int J Primatol 24(4):707–772CrossRefGoogle Scholar
  45. Nishimura A, Izawa K (1975) The group characteristics of woolly monkeys (Lagothrix lagothricha) in the upper Amazonian basin. Contemporary primatol. Karger, Basel, pp 351–357Google Scholar
  46. Parga JA (2011) Nocturnal ranging by a diurnal primate: are ring-tailed lemurs (Lemur catta) cathemeral? Primates 52:201–205CrossRefGoogle Scholar
  47. Pebsworth PA, Morgan HR, Huffman MA (2012) Evaluating home range techniques: use of global positioning system (GPS) collar data from chacma baboons. Primates 53(4):345–355CrossRefGoogle Scholar
  48. Peres CA (1994) Diet and feeding ecology of gray woolly monkeys (Lagothrix lagotricha) in central Amazonia; comparisons with other Atelines. Int J Primatol 15(3):333–372CrossRefGoogle Scholar
  49. Peres CA (1996) Use of space, spatial group structure, and foraging group size of gray woolly monkeys (Lagothrix lagotricha cana) at Urucu, Brazil. In: Marilyn A, Norconk AL, Rosenberger, Paul AG (eds) Adaptive radiations of neotropical primates. Plenum Press, New York, pp 467–488CrossRefGoogle Scholar
  50. Pierce L, Kellndorf J, Walker W, Barros O (2006) Evaluation of the horizontal resolution of SRTM elevation data. Photogramm Eng Remote Sens 72(11):1235–1124CrossRefGoogle Scholar
  51. Powell RA (2000) Animal home ranges and territories and home range estimators. In: Boitani L, Fuller TK (eds) Research techniques in animal ecology: controversies and consequences. Columbia University Press, New York, pp 65-110Google Scholar
  52. Prada CM, Stevenson PR (2016) Plant composition associated with environmental gradients in tropical montane forest (Cueva de Los Guácharos National Park, Huila, Colombia). Biotropica 48(5):568–576CrossRefGoogle Scholar
  53. Ramos-Fernández G, Aguilar SES, Schaffner CM, Vick LG, Aureli F (2013) Site fidelity in space use by spider monkeys (Ateles geoffroyi) in the Yucatan Peninsula, Mexico. PLoS One 8(5):e62813CrossRefGoogle Scholar
  54. Ren B, Li M, Long Y, Grueter CC, Wei F (2008) Measuring daily ranging distances of Rhinopithecus bieti via a global positioning system collar at Jinsichang, China: a methodological consideration. Int J Primatol 29:783–794CrossRefGoogle Scholar
  55. Rodgers AR (2001) Tracking animals with GPS: the first 10 years. Tracking animals with GPS. The Macaulay Institute, Aberdeen, pp 1–10Google Scholar
  56. Schmitt CA, Di Fiore A (2014) Life history, behavior, and development of wild immature lowland woolly monkeys (Lagothrix poeppigii) in Amazonian Ecuador. In: Defler T, Stevenson PR (eds) The woolly monkey: behavior, ecology, systematics, and captive research. Springer, New York, pp 113–146CrossRefGoogle Scholar
  57. Shanee N, Shanee S (2014) Yellow-tailed woolly monkey (Lagothrix favicauda): conservation status, anthropogenic threats, and conservation initiatives. In: Defler TR, Stevenson PR (eds) The woolly monkey: Behavior, ecology, systematics and captive research. Springer, New York, pp 283–299CrossRefGoogle Scholar
  58. Soini P (1986) A synecological study of a primate community in the Pacaya-Samiria National. Reserve, Peru. Primate Conserv 7:63–71Google Scholar
  59. Solla DE, Shane R, Bonduriansky R, Brooks RJ (1999) Eliminating autocorrelation reduces biological relevance of home range estimates. J Anim Ecol 68(2):221–234CrossRefGoogle Scholar
  60. Stark DJ, Vaughan IP, Saldivar DAR, Nathan SK, Goossens B (2017) Evaluating methods for estimating home ranges using GPS collars: a comparison using proboscis monkeys (Nasalis larvatus). PLoS One 12(3):e0174891CrossRefGoogle Scholar
  61. Stevenson PR (1998) Proximal spacing between individuals in a group of woolly monkeys (Lagothrix lagothricha) in Tinigua National Park, Colombia. Int J Primatol 19(2):299–311CrossRefGoogle Scholar
  62. Stevenson PR (2000) Seed dispersal by woolly monkeys (Lagothrix lagotricha) at Tinigua National Park, Colombia: dispersal distance, germination rates, and dispersal quantity. Am J Primatol 50:275–289CrossRefGoogle Scholar
  63. Stevenson PR (2006) Activity and ranging patterns of Colombian woolly monkeys in noth-western Amazonia. Primates 47(3):239–247CrossRefGoogle Scholar
  64. Stevenson PR, Castellanos MC (2000) Feeding rates and daily path range of the colombian woolly monkeys as evidence for between-and within-group competition. Folia Primatol 71:399–408CrossRefGoogle Scholar
  65. Stevenson PR, Link A (2011) Lagothrix lugens. IUCN Red list of threatened species. VersionGoogle Scholar
  66. Stevenson PR, Quiñones MJ, Ahumada JA (1994) Ecological strategies of woolly monkeys (Lagothrix lagotricha) at Tinigua National Park, Colombia. Am J Primatol 32(2):123–140CrossRefGoogle Scholar
  67. Stevenson PR, Zárate DA, Ramírez MA, Henao-Díaz F (2015) Social interactions and proximal spacing in woolly monkeys: lonely females looking for male friends. In: Furuichi T, Yamagiwa J, Aureli F (eds) Dispersing primate females. Springer, Tokyo, pp 45–71CrossRefGoogle Scholar
  68. Strier KB (1992) Atelinae adaptations: behavioral strategies and ecological constraints. Am J Phys Anthropol 88:515–524CrossRefGoogle Scholar
  69. Swihart RK, Slade NA (1985) Testing for independence of observations in animal movements. Ecology 66(4):1176–1184CrossRefGoogle Scholar
  70. Trayford HR, Farmer KH (2012) An assessment of the use of telemetry for primate reintroductions. J Nat Conserv 20(6):311–325CrossRefGoogle Scholar
  71. Vargas SA, León J, Ramírez M, Galvis N, Cifuentes E, Stevenson PR (2014) Population density and ecological traits of highland woolly monkeys at Cueva de los Guácharos National Park, Colombia. High Altitude Primates, Springer New York, pp 85–102Google Scholar
  72. Walter WD, Fischer JW, Baruch-Mordo S, VerCauteren KC (2011) What is the proper method to delineate home range of an animal using today’s advanced GPS telemetry systems: the initial step. In: Krejcar O (ed) Modern telemetry. In Tech, Rijeka, pp 249–268Google Scholar
  73. White GC, Garrott RA (1990) Analysis of wildlife radio-tracking data. Academic, Toronto, p 383Google Scholar
  74. Zárate D, Stevenson PR (2014) Behavioral ecology and Interindividual distance of woolly monkeys (Lagothrix lagothricha) in a rainforest fragment in Colombia. In: Defler T, Stevenson PR (eds) The woolly monkey. Developments in primatology: progress and prospects. Springer, New York, pp 227–245CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Leidy Carolina García-Toro
    • 1
    Email author
  • Andrés Link
    • 1
  • Elsy Johanna Páez-Crespo
    • 1
  • Pablo R. Stevenson
    • 1
  1. 1.Laboratorio de Ecología de Bosques Tropicales y Primatología, Departamento de Ciencias BiológicasUniversidad de Los AndesBogotáColombia

Personalised recommendations