Skip to main content
Log in

Host selection and niche differentiation in sucking lice (Insecta: Anoplura) among small mammals in southwestern China

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Understanding factors that shape host selection has been a classic issue in ecology, evolutionary biology, and epidemiological investigation. During the survey from 2000 to 2009, a total of 11,216 individuals of small mammals were captured from Yunnan Province in southwestern China. The captured small mammalian hosts belong to five orders, ten families, 35 genera, and 65 species and from their body surface, 38,885 individuals of ectoparasitic sucking lice were collected, which represent five families, seven genera, and 31 species. Based on niche overlap of dominant sucking lice on their primary hosts, we used hierarchical cluster analysis to sort different sucking louse species’ resource utilizations of similar kind into respective categories. Given λ < 5, there are only two groups clustered, however, sucking louse species’ resource utilization was sorted into eight respective categories at λ = 15. The results revealed that most species of sucking lice usually had high host specificity and a certain species of sucking louse usually restricted to one or few small mammalian species as their dominant hosts. Correspondence analysis was used to visualize associations between parasitic sucking lice and their small mammalian hosts, which suggested three different patterns of host resource utilization: species specialists, genera generalists, and multiple selections. For example, Sathrax durus (Johnson) only parasitized on species of Tupaia belangeri (Wagner), Hoplopleura edentula (Fahredholz) predominatly on genus of Eothenomys, and Polyplax reclinata (Nitzsch) on Family of Soricidae. Our results demonstrate that sucking lice have high host specificity and this might be due to coevolution between sucking lice and their hosts.

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

Similar content being viewed by others

References

  • Adler PH, Wills W (2003) Legacy of death: the history of arthropod-borne human diseases in South Carolina. Am Entomol 49:216–229

    Google Scholar 

  • Arganaraz E, Hubbard G, Ramos L, Ford A, Nitz N, Leland M, Vandeberg JL, Teixeira ARL (2001) Blood-sucking lice may disseminate Trypanosoma cruzi infection in baboons. Rev Inst Med trop S Paulo 43:271–276

    Article  PubMed  CAS  Google Scholar 

  • Bittencourt EB, Rocha CFD (2003) Host-ectoparasite specificity in a small mammal community in an area of Atlantic Rain Forest (Ilha Grande, State of Rio de Janeiro), Southeastern Brazil. Mem Inst Oswaldo Cruz 98:793–798

    Article  PubMed  Google Scholar 

  • Bossi DEP, Linhares AX, Bergallo HG (2002) Parasitic arthropods of some wild rodents from Juréia-Itatins Ecological Station, state of São Paulo, Brazil. Mem Inst Oswaldo Cruz 97:959–963

    Article  PubMed  Google Scholar 

  • Brouqui P, Raoult D (2006) Arthropod-borne diseases in homeless. Ann NY Acad Sci 1078:223–235

    Article  PubMed  Google Scholar 

  • Burgess IF (2004) Human lice and their control. Annu Rev Entomol 49:457–481

    Article  PubMed  CAS  Google Scholar 

  • Deng GF, Wang DQ, Gu YM, Meng YC (1993) Economic insect fauna of China Fasc 40. Acari: Dermanyssoidea. Science Press, Beijing, China, in Chinese

    Google Scholar 

  • Desjardins CA, Perfectti F, Bartos JD, Enders LS, Werren JH (2010) The genetic basis of interspecies host preference differences in the model parasitoid Nasonia. Heredity 104:270–277

    Article  PubMed  CAS  Google Scholar 

  • Diaz J (2006) The epidemiology, diagnosis, management, and prevention of ectoparasitic diseases in travelers. J Travel Med 13:100–111

    Article  PubMed  Google Scholar 

  • Durden LA, Hu R, Oliver JH, Cilek JE (2000) Rodent ectoparasites from two locations in northwestern Florida. J Vector Ecol 25:222–228

    PubMed  CAS  Google Scholar 

  • Durden LA, Gomez MS (2000) Abrocomaphthirus chilensis (Gomez), new combination (Phthiraptera-Anoplura), an ectoparasite of the Chilean rodent Abrocoma bennetti (Abrocomidae). Parasite 7:331–332

    PubMed  CAS  Google Scholar 

  • Fellenberg K, Hauser NC, Brors B, Neutzner A, Hoheisel JD, Vingron M (2001) Correspondence analysis applied to microarray data. Proc Natl Acad Sci USA 98:10781–10786

    Article  PubMed  CAS  Google Scholar 

  • Geervliet JBF, Vreugdenhil AI, Dicke M, Vet LEM (1998) Learning to discriminate between infochemicals from different plant–host complexes by the parasitoids Cotesia glomerata and C. rubecula. Entomol Exp App 86:241–252

    Article  CAS  Google Scholar 

  • Genchi C (1992) Arthropoda as zoonoses and their implications.Vet Parasitol 44:21-33

    Article  PubMed  CAS  Google Scholar 

  • Guo XG (1998) Host-specificity and host-selection of gamasid mites (Acari: Gamasina). Syst Appl Acarol 3:29–34

    Google Scholar 

  • Guo XG, Qian TJ, Guo LJ, Wang J, Dong WG, Zhang L, Ma ZM, Li W (2004) Species diversity and community structure of sucking lice in Yunnan, China. Entom Sin 1:61–70

    Google Scholar 

  • Guo XG, Gong ZD, Qian TJ, Feng XG, Duan XD, Li W, Zhang XK (2008) Host-specificity and host-selection of fleas in foci of human plague in Yunnan China. Entom Sin 6:370–377

    Google Scholar 

  • Henry LM, Roitberg BD, Gillespie DR (2006) Covariance of phenotypically plastic traits induces an adaptive shift in host selection behaviour. Proc Biol Sci 273:2893–2899

    Article  PubMed  Google Scholar 

  • Hoogstraal H, Aeschlimann A (1982) Tick-host specificity. Bull Soc Entomol Suisse 55:5–32

    Google Scholar 

  • Huang LQ, Guo XG, Wu D, Zhou DH (2010) Distribution and ecological niches of gamasid mites (Acari: Mesostigmata) on small mammals in Southwest China. Psyche 2010:1–12

    Article  Google Scholar 

  • Hulcr J, Mogia M, Isua B, Novotny V (2007) Host specificity of ambrosia and bark beetles (Col., Curculionidae: Scolytinae and Platypodinae) in a New Guinea rainforest. Ecol Entomol 32:762–772

    Article  Google Scholar 

  • Inciardi JF, Stijnen T, McMahon K (2002) Using correspondence analysis in pharmacy practice. Am J Health System Ph 59:968–972

    Google Scholar 

  • Jaenike J (1990) Host specialization in phytophagous insects. Annu Rev Ecol Syst 21:243–273

    Article  Google Scholar 

  • Jin DX (1999) Taxonomy and index of sucking lice of China. Science Press, Beijing, China, In Chinese

    Google Scholar 

  • Kakar M, Kakarsulemankhel J (2009) Prevalence of lice species on cows and buffaloes of Quetta, Pakistan. Pak Vet J 29:49–50

    Google Scholar 

  • Kerdelhué C, Rossi JP, Rasplus JY (2000) Comparative community ecology studies on old world figs and fig wasps. Ecology 81:2832–2849

    Google Scholar 

  • Khokhlova IS, Spinu M, Krasnov BR, Degen AA (2004) Immune responses to fleas in two rodent species differing in natural prevalence of infestation and diversity of flea assemblages. Parasitol Res 94:304–311

    Article  PubMed  Google Scholar 

  • Krasnov BR, Khokhlova IS, Shenbrot GI (2003) Density-dependent host selection in ectoparasites: an application of isodar theory to fleas parasitizing rodents. Oecologia 134:365–372

    PubMed  Google Scholar 

  • Krasnov BR, Khokhlova IS, Burdelova NV, Mirzoyan NS, Degen AA (2004) Fitness consequences of host selection in ectoparasites: testing reproductive patterns predicted by isodar theory in fleas parasitizing rodents. J Anim Ecol 73:815–820

    Article  Google Scholar 

  • Krasnov BR, Poulin R, Shenbrot GI, Mouillot D, Khokhlova IS (2005) Host specificity and geographic range in haematophagous ectoparasites. Oikos 108:449–456

    Article  Google Scholar 

  • Krasnov BR, Khokhlova IS, Shenbrot GI, Poulin R (2008) How are the host spectra of hematophagous parasites shaped over evolutionary time? Random choice vs selection of a phylogenetic lineage. Parasitol Res 102:1157–1164

    Article  PubMed  Google Scholar 

  • Krasnov BR, Mouillot D, Shenbrot GI, Khokhlova IS, Poulin R (2010a) Beta-specificity: the turnover of host species in space and another way to measure host specificity. Int J Parasitol. doi:10.1016/j.ijpara.2010.1006.1001

    Google Scholar 

  • Krasnov BR, Matthee S, Lareschi M, Korallo-Vinarskaya NP, Vinarski MV (2010b) Co-occurrence of ectoparasites on rodent hosts: null model analyses of data from three continents. Oikos 119:120–128

    Article  Google Scholar 

  • Krasnov BR, Stanko M, Morand S (2010c) Competition, facilitation or mediation via host? Patterns of infestation of small European mammals by two taxa of haematophagous arthropods. Ecol Entomol 35:37–44

    Article  Google Scholar 

  • Larsen K, Eydal M, Mencke N, Siguresson H (2005) Infestation of Werneckiella equi on Icelandic horses, characteristics of predilection sites and lice dermatitis. Parasitol Res 96:398–401

    Article  PubMed  CAS  Google Scholar 

  • Li JC, Wang DQ, Chen XB (1997) Trombiculid mites of China. Guangdong Science & Technology Press, Guangzhou, China, in Chinese

    Google Scholar 

  • Light J, Hafener M (2007) Phylogenetics and host associations of Fahrenholzia sucking lice (Phthiraptera: Anoplura). Syst Entomol 32:359–370

    Article  Google Scholar 

  • Light J, Reed D (2009) Multigene analysis of phylogenetic relationships and divergence times of primate sucking lice (Phthiraptera: Anoplura). Mol Phylogenet Evol 50:376–390

    Article  PubMed  CAS  Google Scholar 

  • Magalhães S, Forbes M, Skoracka A, Osakabe M, Chevillon C, McCoy K (2007) Host race formation in the Acari. Exp Appl Acarol 42:225–238

    Article  PubMed  Google Scholar 

  • Malenke JR, Johnson KP, Clayton DH (2009) Host specialization differentiates cryptic species of feather-feeding lice. Evolution 63:1427–1438

    Article  PubMed  Google Scholar 

  • McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, Fry B, Giblin AE, Kielland K, Kwiatkowski BL, Laundre JA, Murray G (2002) Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415:68–71

    Article  PubMed  CAS  Google Scholar 

  • Mehlhorn H, Walldorf V, Klimpel S, Schmahl G (2008) Outbreak of bluetongue disease (BTD) in Germany and the danger for Europe. Parasitol Res 103:S79–S86

    Article  PubMed  Google Scholar 

  • Mehlhorn H, Al-Rasheid K, Abdel-Ghaffar F, Klimpel S, Pohle H (2010) Life cycle and attacks of ectoparasites on ruminants during the year in Central Europe: recommendations for treatment with insecticides (e.g., Butox®). Parasitol Res 107:425–431

    Article  PubMed  Google Scholar 

  • Meng YF, Guo XG, Men XY, Wu D (2007) Numerical classification of communities of sucking lice and their coevolutionary relationship with small mammal hosts in Yunnan. Acta Entom Sin 11:1140–1145 (In Chinese)

    Google Scholar 

  • Meng YF, Guo XG, Men XY, Wu D (2008) Ecological niches of sucking lice (Phthiraptera: Anoplura) and their coevolution relationship with small mammal hosts in Yunnan, China. Chin J Parasitol Parasit Dis 26:25–29 (In Chinese)

    Google Scholar 

  • Mey E (2010) The Pedicinus species (Insecta, Phthiraptera, Anoplura, Pedicinidae) on douc langurs (Pygathrix spp.). Vietnamese J Primatol 4:57–68

    Google Scholar 

  • Mota JC, Vasconcelos AGG, Assis SG (2008) Correspondence analysis: a method for classifying similar patterns of violence against women. Cad Saúde Pública 24:1397–1406

    Article  PubMed  Google Scholar 

  • Mumcuoglu KY, Zias J, Tarshis M, Lavi M, Stiebel GD (2003) Body louse remains found in textiles excavated at Masada, Israel. J Med Entomol 40:585–587

    Article  PubMed  CAS  Google Scholar 

  • Munoz G, Cortes Y (2009) Parasite communities of a fish assemblage from the intertidal rocky zone of central Chile: similarity and host specificity between temporal and resident fish. Parasitology 136:1291–1303

    Article  PubMed  CAS  Google Scholar 

  • Nava S, Lareschi M, Voglino D (2003) Interrelationship between ectoparasites and wild rodents from northeastern Buenos Aires Province, Argentina. Mem Inst Oswaldo Cruz 98:45–49

    Article  PubMed  Google Scholar 

  • Novotny V, Basset Y (2000) Rare species in communities of tropical insect herbivores: pondering the mystery of singletons. Oikos 89:564–572

    Article  Google Scholar 

  • Oguge NO, Durden LA, Keirans JE, Balami HD, Schwan TG (2009) Ectoparasites (sucking lice, fleas and ticks) of small mammals in southeastern Kenya. Med Vet Entomol 23:387–392

    Article  PubMed  CAS  Google Scholar 

  • Pianka E (1973) The structure of lizard communities. Annu Rev Ecol Syst 4:53–74

    Article  Google Scholar 

  • Pittendrigh B, Clark J, Johnston J, Lee S, Romero-Severson J, Dasch G (2006) Sequencing of a new target genome: the Pediculus humanus humanus (Phthiraptera: Pediculidae) genome project. J Med Entomol 43:1103–1111

    Article  PubMed  CAS  Google Scholar 

  • Poulin R, Mouillot D (2005) Combining phylogenetic and ecological information into a new index of host specificity. J Parasitol 91:511–514

    Article  PubMed  CAS  Google Scholar 

  • Poulin R, Krasnov BR, Shenbrot GI, Mouillot D, Khokhlova IS (2006) Evolution of host specificity in fleas: is it directional and irreversible? Int J Parasitol 36:185–191

    Article  PubMed  Google Scholar 

  • Rand DM (2009) 'Why genomes in pieces?' revisited: sucking lice do their own thing in mtDNA circle game. Genome Res 19:700–702

    Article  PubMed  CAS  Google Scholar 

  • Raoult D, Dutour O, Houhamdi L, Jankauskas R, Fournier PE, Ardagna Y, Drancourt M, Signoli M, La VD, Macia Y (2006) Evidence for louse-transmitted diseases in soldiers of Napoleon's Grand Army in Vilnius. J Infect Dis 193:112–120

    Article  PubMed  CAS  Google Scholar 

  • Raymond KM, Chapman LL, Lanciani CA (2006) Host, macrohabitat, and microhabitat specificity in the gill parasite Afrodiplozoon polycotyleus (Monogenea). J Parasitol 92:1211–1217

    Article  PubMed  Google Scholar 

  • Reinhard KJ, Buikstra J (2003) Louse infestation of the Chiribaya culture, southern Peru: variation in prevalence by age and sex. Mem Inst Oswaldo Cruz 98:173–179

    Article  PubMed  Google Scholar 

  • Rousse P, Gourdon F, Roubaud M, Chiroleu F, Quilici S (2009) Biotic and abiotic factors affecting the flight activity of Fopius arisanus, an egg-pupal parasitoid of fruit fly pests. Environ Entomol 38:896–903

    Article  PubMed  CAS  Google Scholar 

  • Schneider K, Migge S, Norton R, Scheu S, Langel R, Reineking A, Maraun M (2004) Trophic niche differentiation in soil microarthropods (Oribatida, Acari): evidence from stable isotope ratios (15 N/14 N). Soil Biol Biochem 36:1769–1774

    Article  CAS  Google Scholar 

  • Shao RF, Kirkness EF, Barker SC (2009) The single mitochondrial chromosome typical of animals has evolved into 18 minichromosomes in the human body louse, Pediculus humanus. Genome Res 19:904–912

    Article  PubMed  CAS  Google Scholar 

  • Shenbrot GI, Krasnov BR, Lu L (2007) Geographical range size and host specificity in ectoparasites: a case study with Amphipsylla fleas and rodent hosts. J Biogeogr 34:1679–1690

    Article  Google Scholar 

  • Suzuki H, Brown CJ, Forney LJ, Top EM (2008) Comparison of correspondence analysis methods for synonymous codon usage in bacteria. DNA Res 15:357–365

    Article  PubMed  CAS  Google Scholar 

  • Stefka J, Hypsa V (2008) Host specificity and genealogy of the louse Polyplax serrata on field mice, Apodemus species: a case of parasite duplication or colonisation? Int J Parasitol 38:731–741

    Article  PubMed  Google Scholar 

  • Taylor MA, Andrews AH, Alzieu JP, Holzhauer M, Kaske M, Willemsen M (2010) Role of immunity in the management and control of bovine coccidiosis. Vet Rec 166:831–832

    Article  PubMed  CAS  Google Scholar 

  • Thompson RC, Lymbery AJ, Smith A (2010) Parasites, emerging disease and wildlife conservation. Int J Parasitol 40:1163–1170

    Article  PubMed  CAS  Google Scholar 

  • Toloza A, Vassena C, Gallardo A, González-Audino P, Picollo MI (2009) Epidemiology of Pediculosis capitis in elementary schools of Buenos Aires, Argentina. Parasitol Res 104:1295–1298

    Article  PubMed  Google Scholar 

  • Vinson SB (1998) The general host selection behavior of parasitoid hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biol Control 11:79–96

    Article  Google Scholar 

  • Yassina B, Christian C, Jean-Louis M, Didier R (2008) Epidemic typhus. Lancet Infect Dis 8:417–426

    Article  Google Scholar 

Download references

Acknowledgements

We are very grateful to some of our colleagues—Mr. Sheng-yong Zhang, Ms. Yan-fen Meng, Mr. Ti-jun Qian, Mr. Wei Li, and Mr. Li-jun Guo, and others—for their contribution and kind help in field investigation, specimen making, identification of sucking lice, and some other related works. We also thank some college students for their contribution and help in the field investigation. Special thanks go to reviewers for their critical review of the manuscript and kind useful suggestions and comments. This study was supported by the Yunnan Provincial Foundation for Key Scientific Projects (grant no. 2007C0005Z2 to XG Guo) and the National Nature Science Foundation of China (grant no. 30060078 to XG Guo).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xian-Guo Guo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zuo, XH., Guo, XG., Zhan, YZ. et al. Host selection and niche differentiation in sucking lice (Insecta: Anoplura) among small mammals in southwestern China. Parasitol Res 108, 1243–1251 (2011). https://doi.org/10.1007/s00436-010-2173-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-010-2173-7

Keywords

Navigation