Skip to main content
Log in

Use of photogrammetry as a means to assess hybrids of rhesus (Macaca mulatta) and long-tailed (M. fascicularis) macaques

  • Original Article
  • Published:
Primates Aims and scope Submit manuscript

Abstract

Rhesus (Macaca mulatta) and long-tailed (M. fascicularis) macaques are the most commonly used non-human primate models for biomedical research, but it is difficult to identify these two species in the hybrid zone (15–20°N). In this work, we used morphological values obtained via photogrammetry to assess hybrids of rhesus and long-tailed macaques at Khao Khieow Open Zoo (KKZ; 13°21′N, 101°06′E), eastern Thailand. Long-tailed and rhesus macaques have species-specific tail lengths and contrasts of their yellowish pelages. The accuracy and precision of the relative tail length (%RTL) and the contrast of the yellow hue (Cb*) of the pelage, as obtained from photographs, were compared with the corresponding direct measurements (morphometrics). The photogrammetric and morphometric measurements of %RTL and Cb* were highly significantly correlated (r = 0.989 and 0.980, p < 0.001), and there were no significant differences between the two datasets (t test, p = 0.13 and 0.41; n = 42 and 17 for %RTL and Cb*, respectively). The reproducibilities of the %RTL and Cb* measurements (calculated in the photogrammetric case by taking photographs of the same macaques in two different environments) were significantly correlated between the datasets (r = 0.983 and 0.914, p < 0.001 and 0.005), and there were no significant differences between the datasets (t test, p = 0.539 and 0.344; n = 30 each for %RTL and Cb*, respectively). The %RTL and Cb* data were combined with data on the crown and cheek hair patterns and sex skin reddening of the macaques, and this combined data set was then analyzed by multiple correspondence analysis and agglomerative hierarchical cluster analysis, leading to the categorization of the rhesus macaques, long-tailed macaques, and hybrids at KKZ into five groups. Thus, photogrammetry can be utilized to identify macaque species or hybrids when species identification relies mainly on tail length and pelage color.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4a–e
Fig. 5

Similar content being viewed by others

References

  • Berger J (2012) Estimation of body-size traits by photogrammetry in large mammals to inform conservation. Conserv Biol 5:769–777

    Article  Google Scholar 

  • Biswas J, Borah DK, Das A, Das J, Bhattacharjee PC, Mohnot SM, Horwich RH (2011) The enigmatic Arunachal macaque: its biogeography, biology and taxonomy in northeastern India. Am J Primatol 73:458–473

  • Bonhomme M, Cuartero S, Blancher A, Crouau-Roy B (2009) Assessing natural introgression in 2 biomedical model species, the rhesus macaque (Macaca mulatta) and the long-tailed macaque (Macaca fascicularis). J Hered 100:158–169

    Article  CAS  PubMed  Google Scholar 

  • Breuer T, Robbins MM, Boesch C (2007) Using photogrammetry and color scoring to assess sexual dimorphism in wild western gorillas (Gorilla gorilla). Am J Phys Anthropol 134:369–382

    Article  PubMed  Google Scholar 

  • Breuer T, Robbins AM, Boesch C, Robbins MM (2012) Phenotypic correlates of male reproductive success in western gorillas. J Hum Evol 62:466–472

    Article  PubMed  Google Scholar 

  • Chiari Y, Claude J (2011) Study of the carapace shape and growth in two Galápagos tortoise lineages. J Morphol 272:379–386

    Article  PubMed  Google Scholar 

  • Deschner T, Heistermann M, Hodges K, Boesch C (2004) Female sexual swelling size, timing of ovulation and male behavior in wild West African chimpanzees. Horm Behav 46:204–215

    Article  CAS  PubMed  Google Scholar 

  • Engelhardt A, Hodges JK, Niemitz C, Heistermann M (2005) Female sexual behavior, but not sex skin swelling, reliably indicates the timing of the fertile phase in wild long-tailed macaques (Macaca fascicularis). Horm Behav 47:195–204

    Article  CAS  PubMed  Google Scholar 

  • Farkas LG, Bryson W, Klotz J (1980) Is photogrammetry of the face reliable? Plast Reconstr Surg 66:346–355

    Article  CAS  PubMed  Google Scholar 

  • Ferguson B, Street SL, Wright H, Pearson C, Jia Y, Thompson SL, Allibone P, Dubay CJ, Spindel E, Norgren RB (2007) Single nucleotide polymorphisms (SNPs) distinguish Indian-origin and Chinese-origin rhesus macaques (Macaca mulatta). BMC Genom 8:43

    Article  Google Scholar 

  • Fooden J (1980) Classification and distribution of living macaques. In: Lindburg DG (ed) The macaques: studies in ecology, behavior, and evolution. Van Nostrand Reinhold, New York, pp 1–9

    Google Scholar 

  • Fooden J (1995) Systematic review of Southeast Asian long-tailed macaques, Macaca fascicularis (Raffles, 1821). Fieldiana Zool 81:1–206

    Google Scholar 

  • Fooden J (1997) Tail length variation in Macaca fascicularis and M. mulatta. Primates 38:221–231

    Article  Google Scholar 

  • Fooden J (1999) Tail length evolution in Fascicularis-group macaques (Cercopithecidae: Macaca). Int J Primatol 20:331–443

    Article  Google Scholar 

  • Fooden J (2000) Systematic review of the rhesus macaque, Macaca mulatta (Zimmermann, 1780). Fieldiana Zool 96:1–180

    Google Scholar 

  • Gibbs RA, Rogers J, Katze MG, Bumgarner R, Weinstock GM, Mardis ER, Remington KA, Strausberg RL, Venter JC, Wilson RK (2007) Evolutionary and biomedical insights from the rhesus macaque genome. Science 316:222–234

    Article  CAS  PubMed  Google Scholar 

  • Hamada Y, Watanabe T, Chatani K, Hayasawa S, Iwamoto M (2005a) Morphometrical comparison between Indian- and Chinese-derived rhesus macaques (Macaca mulatta). Anthropol Sci 113:183–188

    Article  Google Scholar 

  • Hamada Y, Hadi I, Urasopon N, Malaivijitnond S (2005b) Preliminary report on yellow long-tailed macaques (Macaca fascicularis) at Kosumpee Forest Park, Thailand. Primates 46:269–273

    Article  PubMed  Google Scholar 

  • Hamada Y, Urasopon N, Hadi I, Malaivijitnond S (2006) Body size and proportions and pelage color of free-ranging Macaca mulatta from a zone of hybridization in northern Thailand. Int J Primatol 27:497–513

    Article  Google Scholar 

  • Hamada Y, Suryobroto B, Goto S, Malaivijitnond S (2008) Morphological and body color variation in Thai Macaca fascicularis fascicularis north and south of the Isthmus of Kra. Int J Primatol 29:1271–1294

    Article  Google Scholar 

  • Hoogeboom B, Alberink I, Goos M (2009) Body height measurements in images. J Forensic Sci 54:1365–1375

    Article  PubMed  Google Scholar 

  • Karsli F, Atasoy M, Yalcin A, Reis S, Demir O, Gokceoglu C (2009) Effects of land-use changes on landslides in a landslide-prone area (Ardesen, Rize, NE Turkey). Environ Monit Assess 156:241–255

    Article  CAS  PubMed  Google Scholar 

  • Koopmans M, Wijffels RH (2008) Seasonal growth rate of the sponge Haliclona oculata (Demospongiae: Haplosclerida). Mar Biotechnol (NY) 10:502–510

    Article  CAS  Google Scholar 

  • Kurita H, Suzumura T, Kanchi F, Hamada Y (2012) A photogrammetric method to evaluate nutritional status without capture in habituated free-ranging Japanese macaques (Macaca fuscata): a pilot study. Primates 53:7–11

    Article  PubMed  Google Scholar 

  • Machatschke IH, Dittami J, Wallner B (2006) Morphometric and hormonal changes during chimpanzee menstrual cycle. J Med Primatol 35:331–340

    Article  CAS  PubMed  Google Scholar 

  • Malaivijitnond S, Hamada Y (2008) Current situation and status of long-tailed macaques (Macaca fascicularis) in Thailand. Nat Hist J Chulalongkorn Univ 8:185–204

    Google Scholar 

  • Malaivijitnond S, Hamada Y, Suryobroto B, Takenaka O (2007a) Female long-tailed macaques with scrotum-like structure. Am J Primatol 69:1–15

    Google Scholar 

  • Malaivijitnond S, Takenaka O, Kawamoto Y, Urasopon N, Hadi I, Hamada Y (2007b) Anthropogenic macaque hybridization and genetic pollution of a threatened population. Nat Hist J Chulalongkorn Uni 7:11–23

    Google Scholar 

  • Malaivijitnond S, Sae-Low W, Hamada Y (2008) The human-ABO blood groups of free-ranging long-tailed macaques (Macaca fascicularis) and parapatric rhesus macaques (M. mulatta) in Thailand. J Med Primatol 37:31–37

    PubMed  Google Scholar 

  • Malaivijitnond S, Vazquez Y, Hamada Y (2011) Human impact on long-tailed macaques in Thailand. In: Jones-Engel L, Gumert M, Fuentes A (eds) Managing commensalism in long-tailed macaques. Cambridge University Press, Cambridge, pp 118–158

  • Metzler P, Bruegger LS, Kruse Gujer AL, Matthews F, Zemann W, Graetz KW, Leubbers H-T (2012) Craniofacial landmarks in young children: how reliable are measurements based on 3-dimensional imaging? J Craniofac Surg 23:1790–1795

  • Migot-Nabias F, Ollomo B, Dubreuil G, Morelli A, Domarle O, Nabias R (1999) Plasmodium coatneyi: differential clinical and immune responses of two population of Macaca fascicularis from different origins. Exp Parasitol 91:30–39

    Article  CAS  PubMed  Google Scholar 

  • Moor-Jankowski J, Socha WW (1979) Blood groups of Old World monkeys, evolutionary and taxonomic implications. J Human Evol 8:445–451

    Article  Google Scholar 

  • Mori Y, Shimoda K, Kobayashi H, Hayaska I, Hamada Y (2007) Development of the sexual skin with pubertal maturation in female chimpanzees. Primates 48:97–101

    Article  PubMed  Google Scholar 

  • Pilgrim LJ (1992) History of photogrammetry in medicine. Australas Phys Eng Sci Med 15:1–8

    CAS  PubMed  Google Scholar 

  • Rohner CA, Richardson AJ, Marshall AD, Weeks SJ, Pierce SJ (2011) How large is the world’s largest fish? Measuring whale sharks Rhincodon typus with laser photogrammetry. J Fish Biol 78:378–385

    Article  CAS  PubMed  Google Scholar 

  • Rothman JM, Chapman CA, Twinomugisha D, Wasserman MD, Lambert JE, Goldberg TL (2008) Measuring physical traits of primates remotely: the use of parallel lasers. Am J Primatol 70:1191–1195

    Article  PubMed  Google Scholar 

  • Schmidt LH, Fradkin R, Harrison J, Rossan RN (1977) Differences in the virulence of Plasmodium knowlesi for Macaca irus (fascicularis) of Philippine and Malayan origins. Am J Trop Med Hygiene 26:612–622

    CAS  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Meth 9:671–675

    Article  CAS  Google Scholar 

  • Sinha A, Datta A, Madhusudan MD, Mishra C (2005) Macaca munzala: a new species from western Arunachal Pradesh, northeastern India. Int J Primatol 26:977–989

  • Tosi AJ, Morales JC, Melnick DJ (2002) Y-chromosome and mitochondrial markers in Macaca fascicularis indicate introgression with Indochinese M. mulatta and a biogeographic barrier in the Isthmus of Kra. Int J Primatol 23:161–178

    Article  Google Scholar 

  • Wong JY, Oh AK, Ohta E, Hunt AT, Rogers GF, Mulliken JB, Deutsch CK (2008) Validity and reliability of craniofacial anthropometric measurement of 3D digital photogrammetric images. Cleft Palate-Craniofac J 45:232–239

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. Visit Arsaithamkul and his team for field assistance, and Dr. Robert Butcher, Faculty of Science, Chulalongkorn University, for proofreading the manuscript. We are grateful to the Khao Khieow Open Zoo for the permission to collect field data. This study was financially supported by the Ratchadapisek Sompoch Endowment Fund, Chulalongkorn University (Sci-Super 2014–021) and the Ministry of Science and Technology of Thailand.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Suchinda Malaivijitnond.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jadejaroen, J., Hamada, Y., Kawamoto, Y. et al. Use of photogrammetry as a means to assess hybrids of rhesus (Macaca mulatta) and long-tailed (M. fascicularis) macaques. Primates 56, 77–88 (2015). https://doi.org/10.1007/s10329-014-0450-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10329-014-0450-2

Keywords

Navigation