Parasitology Research

, Volume 111, Issue 2, pp 909–919 | Cite as

Ectoparasite infestation patterns of domestic dogs in suburban and rural areas in Borneo

  • Konstans WellsEmail author
  • Jean-Claude Beaucournu
  • Lance A. Durden
  • Trevor N. Petney
  • Maklarin B. Lakim
  • Robert B. O’Hara
Original Paper


Domestic dogs, Canis lupus, have been one of the longest companions of humans and have introduced their own menagerie of parasites and pathogens into this relationship. Here, we investigate the parasitic load of 212 domestic dogs with fleas (Siphonaptera) chewing lice (Phthiraptera), and ticks (Acarina) along a gradient from rural areas with near-natural forest cover to suburban areas in Northern Borneo (Sabah, Malaysia). We used a spatially-explicit hierarchical Bayesian model that allowed us to impute missing data and to consider spatial structure in modelling dog infestation probability and parasite density. We collected a total of 1,968 fleas of two species, Ctenocephalides orientis and Ctenocephalides felis felis, from 195 dogs (prevalence, 92 %). Flea density was higher on dogs residing in houses made of bamboo or corrugated metal (increase of 40 % from the average) compared to timber or stone/compound houses. Host-dependent and landscape-level environmental variables and spatial structure only had a weak explanatory power. We found adults of the invasive chewing louse Heterodoxus spiniger on 42 dogs (20 %). The effect of housing conditions was opposite to those for fleas; lice were only found on dogs residing in stone or timber houses. We found ticks of the species Rhipicephalus sanguineus as well as Haemaphysalis bispinosa gp., Haemaphysalis cornigera, Haemaphysalis koenigsbergi, and Haemaphysalis semermis on 36 dogs (17 %). The most common tick species was R. sanguineus, recorded from 23 dogs. Tick infestations were highest on dogs using both plantation and forest areas (282 % increase in overall tick density of dogs using all habitat types). The infestation probability of dogs with lice and ticks decreased with elevation, most infestations occurred below 800 m above sea level. However, the density of lice and ticks revealed no spatial structure; infestation probability of dogs with these two groups revealed considerable autocorrelation. Our study shows that environmental conditions on the house level appeared to be more influential on flea and lice density whereas tick density was also influenced by habitat use. Infestation of dogs with Haemaphysalis ticks identified an important link between dogs and forest wildlife for potential pathogen transmission.


Credible Interval Tick Species Tick Infestation Salb Spatial Random Effect 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Sabah Parks for permission and for providing various kind of support during field work. We are especially thankful to all dog owners and families in Sabah who allowed as to examine their dogs and provided helpful hands. Fred Tuh Yit Yuh, Ibas Dungol, and Jorimia Molubi kindly helped in the field. Eva-Maria Gerstner contributed to GIS data preparation. Field work was funded by the “Landesoffensive zur Entwicklung wissenschaftlich-ökonomischer Exzellenz” (LOEWE) of the state of Hesse in Germany through the Biodiversity and Climate Research Centre (Bik-F).

Supplementary material

436_2012_2917_MOESM1_ESM.doc (34 kb)
ESM 1 DOC 34 kb


  1. Adler GH, Suntsova NI, Suntsov VV, Mangan SA (2001) Fleas (Siphonaptera) collected from small mammals in southern Vietnam in 1997–1998. J Med Entomol 38:210–213PubMedCrossRefGoogle Scholar
  2. Alexander KA, McNutt JW (2010) Human behavior influences infectious disease emergence at the human–animal interface. Front Ecol Environ 8:522–526CrossRefGoogle Scholar
  3. Allan BF, Keesing F, Ostfeld RS (2003) Effect of forest fragmentation on Lyme disease risk. Conserv Biol 17:267–272CrossRefGoogle Scholar
  4. Banerjee S, Carlin BP, Gelfand AE (2004) Hierarchical modeling and analysis for spatial data. Chapman & Hall/CRC, Boca RatonGoogle Scholar
  5. Barbara KA, Farzeli A, Ibrahim IN, Antonjaya U, Yunianto A, Winoto I, Ester PD, Widjaya S, Richards AL, Williams M, Blair PJ (2010) Rickettsial infections of fleas collected from small mammals on four islands in Indonesia. J Med Entomol 47:1173–1178PubMedCrossRefGoogle Scholar
  6. Barutzki D, Schaper R (2003) Endoparasites in dogs and cats in Germany 1999–2002. Parasitol Res 90:S148–S150PubMedCrossRefGoogle Scholar
  7. Beaucournu JC, Jouan R, Menier K (2001) Insectes ectoparasites du chien au Laos. Rev Med Vet—Toulouse 152:77–82Google Scholar
  8. Bhaduri B, Bright E, Coleman P, Urba ML (2007) Landscan USA: a high-resolution geospatial and temporal modeling approach for population distribution and dynamics. GeoJournal 69:103–117CrossRefGoogle Scholar
  9. Chaisiri K, Chaeychomsri W, Siruntawineti J, Bordes F, Herbreteau V, Morand S (2010) Human-dominated habitats and helminth parasitism in Southeast Asian murids. Parasitol Res 107:931–937PubMedCrossRefGoogle Scholar
  10. Collinge SK, Johnson WC, Ray C, Matchett R, Grensten J, Cully JFJ, Gage KL, Kosoy MY, Loye JE, Martin AP (2005) Landscape structure and plague occurrence in black-tailed prairie dogs on grasslands of the western USA. Landsc Ecol 20:941–955CrossRefGoogle Scholar
  11. Dantas-Torres F (2010) Biology and ecology of the brown dog tick, Rhipicephalus sanguineus. Parasites & Vectors 3:26CrossRefGoogle Scholar
  12. Dantas-Torres F et al (2010) Detection of Leishmania infantum in Rhipicephalus sanguineus ticks from Brazil and Italy. Parasitol Res 106:857–860PubMedCrossRefGoogle Scholar
  13. Daszak P, Cunningham AA, Hyatt AD (2001) Anthropogenic environmental change and the emergence of infectious disease in wildlife. Acta Trop 78:103–116PubMedCrossRefGoogle Scholar
  14. Durden LA, Musser GG (1994) The sucking lice (Insecta, Anoplura) of the world: a taxonomic checklist with records of mammalian hosts and geographical distributions. Bull Am Mus Nat Hist 218:1–90Google Scholar
  15. Estrada-Peña A (2001) Distribution, abundance, and habitat preferences of Ixodes ricinus (Acari: Ixodidae) in northern Spain. J Med Entomol 38:361–370PubMedCrossRefGoogle Scholar
  16. Farkas R, Gyurkovszky M, Solymosi N, Beugnet F (2009) Prevalence of flea infestation in dogs and cats in Hungary combined with a survey of owner awareness. Med Vet Entomol 23:187–194PubMedCrossRefGoogle Scholar
  17. Friggens MM, Beier P (2010) Anthropogenic disturbance and the risk of flea-borne disease transmission. Oecologia 164:809–820PubMedCrossRefGoogle Scholar
  18. Gelman A, Carlin JB, Stern HS, Rubin DB (2005) Bayesian data analysis. Chapman & Hall/CRC, Boca RatonGoogle Scholar
  19. Gilbert L (2010) Altitudinal patterns of tick and host abundance: a potential role for climate change in regulating tick-borne diseases? Oecologia 162:217–225PubMedCrossRefGoogle Scholar
  20. Gracia MJ, Calvete C, Estrada R, Castillo JA, Peribanez MA, Lucientes J (2008) Fleas parasitizing domestic dogs in Spain. Vet Parasitol 151:312–319PubMedCrossRefGoogle Scholar
  21. Hoogstraal H, Kim KC (1985) Tick and mammal coevolution, with emphasis on Haemaphysalis. In: Kim KC (ed) Coevolution of parasitic arthropods and mammals. Wiley, New York, pp 505–568Google Scholar
  22. Irwin PJ, Jefferies R (2004) Arthropod-transmitted diseases of companion animals in Southeast Asia. Trends Parasitol 20:27–34PubMedCrossRefGoogle Scholar
  23. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990–994PubMedCrossRefGoogle Scholar
  24. Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk. Ecol Lett 9:485–498PubMedCrossRefGoogle Scholar
  25. Kernif T, Socolovschi C, Wells K, Lakim MB, Inthalad S, Slesak G, Boudebouch N, Beaucournu J-C, Newton PN, Raoult D, Parola P (2012) Bartonella and Rickettsia in arthropods from the Lao PDR and from Borneo, Malaysia. Comp Immunol Microbiol 35:51–57CrossRefGoogle Scholar
  26. Klimpel S, Heukelbach J, Pothmann D, Ruckert S (2010) Gastrointestinal and ectoparasites from urban stray dogs in Fortaleza (Brazil): high infection risk for humans? Parasitol Res 107:713–719PubMedCrossRefGoogle Scholar
  27. Kohl GM (1957) Malaysian parasites. 18. Ticks (Ixodidea) of Borneo and Malaya. Stud Inst Med Res Malaysia 28:65–94Google Scholar
  28. Krasnov BR (2008) Functional and evolutionary ecology of fleas: a model for ecological parasitology. Cambridge University Press, New YorkCrossRefGoogle Scholar
  29. Lafferty KD (2009) The ecology of climate change and infectious diseases. Ecology 90:888–900PubMedCrossRefGoogle Scholar
  30. Lunn D, Spiegelhalter D, Thomas A, Best N (2009) The BUGS project: evolution, critique and future directions. Stat Med 28:3049–3067PubMedCrossRefGoogle Scholar
  31. Macpherson CNL, Meslin FX, Wandeler AI (2000) Dogs, zoonoses and public health. CABI Pub, WallingfordCrossRefGoogle Scholar
  32. Marshall AG (1981) The ecology of ectoparasitic insects. Academic, LondonGoogle Scholar
  33. Mehlhorn H, Hansen O, Mencke N (2001) Comparative study on the effects of three insecticides (fipronil, imidacloprid, selamectin) on developmental stages of the cat flea (Ctenocephalides felis Bouche 1835): a light and electron microscopic analysis of in vivo and in vitro experiments. Parasitol Res 87:198–207PubMedCrossRefGoogle Scholar
  34. Mehlhorn H, Walldorf V, Abdel-Ghaffar F, Al-Quraishy S, Al-Rasheid KAS, Mehlhorn J (2012) Biting and bloodsucking lice of dogs- treatment by means of a neem seed extract (MiteStopA (R), Wash Away Dog). Parasitol Res 110:769–773PubMedCrossRefGoogle Scholar
  35. McCallum H, Dobson A (2002) Disease, habitat fragmentation and conservation. Proc R Soc Lond B Biol 269:2041–2049CrossRefGoogle Scholar
  36. Miettinen J, Shi CH, Liew SC (2011) Deforestation rates in insular Southeast Asia between 2000 and 2010. Global Change Biol 17:2261–2270CrossRefGoogle Scholar
  37. Morgan ER, Milner-Gulland EJ, Torgerson PR, Medley GF (2004) Ruminating on complexity: macroparasites of wildlife and livestock. Trends Ecol Evol 19:181–188PubMedCrossRefGoogle Scholar
  38. O’Hara RB (2009) How to make models add up—a primer on GLMMs. Ann Zool Fenn 46:124–137Google Scholar
  39. Ostfeld RS, Holt RD (2004) Are predators good for your health? Evaluating evidence for top-down regulation of zoonotic disease reservoirs. Front Ecol Environ 2:13–20CrossRefGoogle Scholar
  40. Petney TN, Keirans JE (1996) Ticks of the genera Boophilus, Dermacentor, Nosomma and Rhipicephalus (Acari: Ixodidae) in South East Asia. Trop Biomed 13:73–84Google Scholar
  41. Petney TN, Kolonin GV, Robbins RG (2007) Southeast Asian ticks (Acari: Ixodida): a historical perspective. Parasitol Res 101:S201–S205PubMedCrossRefGoogle Scholar
  42. Price RD, Hellenthal RA, Palma RL, Johnson KP, Clayton DH (2003) The chewing lice: world checklist and biological overview. Illinois Natural History Survey, Special Publication No. 24Google Scholar
  43. R Development Core Team (2011) R: A language and environment for statistical computing. In. R Foundation for Statistical Computing, Vienna, Austria.
  44. Rinaldi L, Spera G, Musella V, Carbone S, Veneziano V, Iori A, Cringoli G (2007) A survey of fleas on dogs in Southern Italy. Vet Parasitol 148:375–378PubMedCrossRefGoogle Scholar
  45. Salb AL, Barkema HW, Elkin BT, Thompson RCA, Whiteside DP, Black SR, Dubey JR, Kutz SJ (2008) Dogs as sources and sentinels of parasites in humans and wildlife, Northern Canada. Emerg Infect Dis 14:60–63PubMedCrossRefGoogle Scholar
  46. Smith FD, Ballantyne R, Morgan ER, Wall R (2011) Prevalence, distribution and risk associated with tick infestation of dogs in Great Britain. Med Vet Entomol 25:377–384PubMedCrossRefGoogle Scholar
  47. Sodhi NS, Koh LP, Clements R, Wanger TC, Hill JK, Hamer KC, Clough Y, Tscharntke T, Posa MRC, Lee TM (2010) Conserving Southeast Asian forest biodiversity in human-modified landscapes. Biol Conserv 143:2375–2384CrossRefGoogle Scholar
  48. Tanskul P, Stark HE, Inlao L (1986) A checklist of ticks in Thailand (Acari: Metastigmata: Ixodidaea). J Med Entomol 20:330–341Google Scholar
  49. Thamm S, Kalko EKV, Wells K (2010) Ectoparasite infestations of hedgehogs (Erinaceus europaeus) are associated with small-scale landscape structures in an urban–suburban environment. EcoHealth 6:404–413CrossRefGoogle Scholar
  50. Traub RJ, Robertson ID, Irwin PJ, Mencke N, Thompson R (2005) Canine gastrointestinal parasitic zoonoses in India. Trends Parasitol 21:42–48PubMedCrossRefGoogle Scholar
  51. Wang CR, Qiu JH, Zhao JP, Xu LM, Yu WC, Zhu XQ (2006) Prevalence of helminthes in adult dogs in Heilongjiang Province, the people’s republic of China. Parasitol Res 99:627–630PubMedCrossRefGoogle Scholar
  52. Wells K, Kalko EKV, Lakim MB, Pfeiffer M (2007) Effects of rain forest logging on species richness and assemblage composition of small mammals in Southeast Asia. J Biogeogr 34:1087–1099CrossRefGoogle Scholar
  53. Wells K, Lakim MB, Beaucournu JC (2011) Host specificity and niche partitioning in flea–small mammal networks in Bornean rainforests. Med Vet Entomol 25:311–319PubMedCrossRefGoogle Scholar
  54. Xhaxhiu D, Kusi I, Rapti D, Visser M, Knaus M, Lindner T, Rehbein S (2009) Ectoparasites of dogs and cats in Albania. Parasitol Res 105:1577–1587PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Konstans Wells
    • 1
    • 2
    • 3
    Email author
  • Jean-Claude Beaucournu
    • 4
  • Lance A. Durden
    • 5
  • Trevor N. Petney
    • 6
  • Maklarin B. Lakim
    • 2
  • Robert B. O’Hara
    • 1
  1. 1.Biodiversity and Climate Research Centre (Bik-F)Frankfurt (Main)Germany
  2. 2.Kota KinabaluMalaysia
  3. 3.Institute of Experimental EcologyUniversity of UlmUlmGermany
  4. 4.Laboratoire de Parasitologie et de Zoologie AppliqueeFaculté de MédecineRennesFrance
  5. 5.Department of BiologyGeorgia Southern UniversityStatesboroUSA
  6. 6.Karlsruhe Institute of Technology, Zoological InstituteKarlsruheGermany

Personalised recommendations