Hostname: page-component-7dd5485656-hw7sx Total loading time: 0 Render date: 2025-10-31T08:05:28.976Z Has data issue: false hasContentIssue false
  • English
  • Français

Analysis of large new South African dataset using two host-specificity indices shows generalism in both adult and larval ticks of mammals

Published online by Cambridge University Press:  22 December 2015

MARCELA P. A. ESPINAZE Open the ORCID record for MARCELA P. A. ESPINAZE [Opens in a new window] ,
ELÉONORE HELLARD ,
IVAN G. HORAK  and
GRAEME S. CUMMING
MARCELA P. A. ESPINAZE*
Affiliation:
Percy FitzPatrick Institute, DST-NRF Centre of Excellence, University of Cape Town, Private Bag X3, Rondebosch 7701, South Africa
ELÉONORE HELLARD
Affiliation:
Percy FitzPatrick Institute, DST-NRF Centre of Excellence, University of Cape Town, Private Bag X3, Rondebosch 7701, South Africa
IVAN G. HORAK
Affiliation:
Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University of Pretoria, Private Bag X04, Onderstepoort 0110, South Africa
GRAEME S. CUMMING
Affiliation:
Percy FitzPatrick Institute, DST-NRF Centre of Excellence, University of Cape Town, Private Bag X3, Rondebosch 7701, South Africa ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland 4811, Australia
*
*Corresponding author: Percy FitzPatrick Institute, DST-NRF Centre of Excellence, University of Cape Town, Private Bag X3, Rondebosch 7701, South Africa. Phone: 0027-84-634-1612. fax: 0027-21-650-3295. E-mail: mares027@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

Ticks and tick-borne pathogens can have considerable impacts on the health of livestock, wildlife and people. Knowledge of tick–host preferences is necessary for both tick and pathogen control. Ticks were historically considered as specialist parasites, but the range of sampled host species has been limited, infestation intensity has not been included in prior analyses, and phylogenetic distances between hosts have not been previously considered. We used a large dataset of 35 604 individual collections and two host-specificity indices to assess the specificity of 61 South African tick species, as well as distinctions between adult and juvenile ticks, for 95 mammalian hosts. When accounting for host phylogeny, most adult and juvenile ticks behaved as generalists, with juveniles being significantly more generalist than adults. When we included the intensity of tick infestation, ticks exhibited a wider diversity of specificity in all life stages. Our results show that ticks of mammals in South Africa tend to behave largely as generalists and that adult ticks are more host-specific. More generally, our analysis shows that the incorporation of life-stage differences, infestation intensity and phylogenetic distances between hosts, as well as the use of more than one specificity index, can all contribute to a deeper understanding of host–parasite interactions.

Keywords

Host–parasite interactiontickshost specificitySouth AfricaIxodidae

Information

Type
Research Article
Information
Parasitology , Volume 143 , Issue 3 , March 2016 , pp. 366 - 373
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

REFERENCES

Altizer, S., Harvell, D. and Friedle, E. (2003). Rapid evolutionary dynamics and disease threats to biodiversity. Trends in Ecology and Evolution 18, 589–596.Google Scholar
Belan, I. and Bull, C. M. (1995). Host-seeking behaviour by Australian ticks (Acari: Ixodidae) with differing host specificities. Experimental & Applied Acarology 19, 221–232.Google Scholar
Bininda-Emonds, O. R. P., Cardillo, M., Jones, K. E., MacPhee, R. D. E., Beck, R. M. D., Grenyer, R., Price, S. A., Vos, R. A., Gittleman, J. L. and Purvis, A. (2007). The delayed rise of present-day mammals. Nature 446, 507–512.Google Scholar
Caira, J. N., Jensen, K. and Holsinger, K. E. (2003). On a new index of host specificity. In Taxonomy, ecology and evolution of metazoan parasites (ed. Combes, C. and Jourdane, J.), pp. 161–201. University of Perpignan Press, Perpignan, France.Google Scholar
Cumming, G. S. (1998). Host preference in African ticks (Acari: Ixodida): a quantitative data set. Bulletin of Entomological Research 88, 379–406.CrossRefGoogle Scholar
Cumming, G. S. (2000). Host use does not clarify the evolutionary history of African ticks (Acari: Ixodoidea). African Zoology 35, 43–50.Google Scholar
Cumming, G. S. (2004). On the relevance of abundance and spatial pattern for interpretations of host–parasite association data. Bulletin of Entomological Research 94, 401–409.CrossRefGoogle ScholarPubMed
Cumming, G. S. and Van Vuuren, D. P. (2006). Will climate change affect ectoparasite species ranges? Global Ecology and Biogeography 15, 486–497.Google Scholar
Driscoll, C. A., Menotti-Raymond, M., Roca, A. L., Hupe, K., Johnson, W. E., Geffen, E., Harley, E. H., Delibes, M., Pontier, D., Kitchener, A. C., Yamaguchi, N., O'Brien, S. J. and Macdonald, D. W. (2007). The Near Eastern origin of cat domestication. Science 317, 519–523.Google Scholar
Hiendleder, S., Lewalski, H. and Janke, A. (2008). Complete mitochondrial genomes of Bos taurus and Bos indicus provide new insights into intra-species variation, taxonomy and domestication. Cytogenetic and Genome Research 120, 150–156.Google Scholar
Hoogstraal, H. and Aeschlimann, A. (1982). Tick-host specificity. Bulletin de la Société Entomologique Suisse 55, 5–32.Google Scholar
Hoogstraal, H. and Kim, K. C. (1985). Tick and mammal coevolution, with emphasis on Haemaphysalis . In Coevolution of Parasitic Arthropods and Mammals (ed. Kim, K. C.), pp. 505–568. Wiley & Sons, New York.Google Scholar
Hoogstraal, H., Clifford, C. M. and Keirans, J. E. (1973). Argas (Microargas) transversus (Ixodoidea: Argasidae) of Galapagos giant tortoises: description of the female and nymph. Annals of the Entomological Society of America 66, 727–732. http://dx.doi.org/10.1093/aesa/66.4.727 CrossRefGoogle Scholar
Horak, I. G., Braack, L. E., Fourie, L. J. and Walker, J. B. (2000). Parasites of domestic and wild animals in South Africa. XXXVIII. Ixodid ticks collected from 23 wild carnivore species. The Onderstepoort Journal of Veterinary Research 67, 239–250.Google Scholar
James, A. and Oliver, J. H. (1990). Feeding and host preference of immature Ixodes dammini, I. scapularis, and I. pacificus (Acari: Ixodidae). Journal of Medical Entomology 27, 324–330.CrossRefGoogle ScholarPubMed
Jensenius, M., Fournier, P., Kelly, P., Myrvang, B. and Raoult, D. (2003). African tick bite fever. The Lancet Infectious Diseases 3, 557–564.Google Scholar
Jongejan, F. and Uilenberg, G. (2004). The global importance of ticks. Parasitology 129, S3–S14.Google Scholar
Karesh, W. B., Cook, R. A., Bennett, E. L. and Newcomb, J. (2005). Wildlife trade and global disease emergence. Emerging Infectious Diseases 11, 1000–1002.CrossRefGoogle ScholarPubMed
Klompen, J. S. H., Black, W. C., Keirans, J. E. and Oliver, J. H. Jr. (1996). Evolution of ticks. Annual Review of Entomology 41, 141–161.CrossRefGoogle ScholarPubMed
Koh, L. P., Dunn, R. R., Sodhi, N. S., Colwell, R. K., Proctor, H. C. and Smith, V. S. (2004). Species coextinctions and the biodiversity crisis. Science 305, 1632–1634.Google Scholar
Lymbery, A. J. (1989). Host specificity, host range and host preference. Parasitology Today 5, 298.Google Scholar
Margolis, L., Esch, G. W., Holmes, J. C., Kuris, A. M. and Schad, G. A. (1982). The use of ecological terms in parasitology (report of an ad hoc committee of the American society of parasitologists). Journal of Parasitology 68, 131–133.Google Scholar
Marques Lisbôa Lopes, C., Cerequeira Leite, R., Bahia Labruna, M., de Oliveira, P. R., Miranda Ferreira Borges, L., Batista Rodrigues, Z., Avila de Carvalho, H., Vianna de Freitas, C. M. and Vieira Junior, C. R. (1998). Host specificity of Amblyomma cajennense (Fabricius, 1787) (Acari: Ixodidae) with Comments on the drop-off rhythm. Memorias Do Instituto Oswaldo Cruz 93, 347–351.Google Scholar
Moyo, B. and Masika, P. J. (2009). Tick control methods used by resource-limited farmers and the effect of ticks on cattle in rural areas of the Eastern Cape Province, South Africa. Tropical Animal Health and Production 41, 517–523.Google Scholar
Muchenje, V., Dzama, K., Chimonyo, M., Raats, J. G. and Strydom, P. E. (2008). Tick susceptibility and its effects on growth performance and carcass characteristics of Nguni, Bonsmara, and Angus steers raised on natural pasture. Animal 2, 298–304.CrossRefGoogle ScholarPubMed
Nava, S. and Guglielmone, A. A. (2013). A meta-analysis of host specificity in Neotropical hard ticks (Acari: Ixodidae). Bulletin of Entomological Research 103, 216–224.CrossRefGoogle ScholarPubMed
Oliver, J. H. (1989). Biology and systematics of ticks (Acari: Ixodida). Annual Review of Ecology and Systematics 20, 397–430.Google Scholar
Ostfeld, R. S., Cepeda, O. M., Hazler, K. R. and Miller, M. C. (1995). Ecology of Lyme disease: habitat associations of ticks (Ixodes scapularis) in a rural landscape. Ecological Applications 5, 353–361.CrossRefGoogle Scholar
Paradis, E., Claude, J. and Strimmer, K. (2004). APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290.Google Scholar
Petney, T. N., Kolonin, G. V. and Robbins, R. G. (2007). Southeast Asian ticks (Acari: Ixodida): a historical perspective. Parasitology Research 101, 201–205.CrossRefGoogle ScholarPubMed
Poulin, R. and Mouillot, D. (2003). Parasite specialization from a phylogenetic perspective: a new index of host specificity. Parasitology 126, 473–480.Google Scholar
Poulin, R. and Mouillot, D. (2004). The relationship between specialization and local abundance: the case of helminth parasites of birds. Oecologia 140, 372–378.Google Scholar
Poulin, R. and Mouillot, D. (2005). Combining phylogenetic and ecological information into a new index of host specificity. Journal of Parasitology 91, 511–514.Google Scholar
Poulin, R. and Keeney, D. B. (2007). Host specificity under molecular and experimental scrutiny. Trends in Parasitology 24, 24–28.CrossRefGoogle ScholarPubMed
Power, A. G. and Mitchell, C. E. (2004). Pathogen spillover in disease epidemics. The American Naturalist 164, S79–S89.Google Scholar
R Core Team (2014). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Randolph, S. E. and Storey, K. (1999). Impact of microclimate on immature tick-rodent host interactions (Acari: Ixodidae): implications for parasite transmission. Journal of Medical Entomology 36, 741–748.http://dx.doi.org/10.1093/jmedent/36.6.741 Google Scholar
Rohde, K. (1980). Host specificity indices of parasites and their application. Experientia 36, 1369–1371.Google Scholar
Rohde, K. (1993). Ecology of Marine Parasites. CAB International, Wallingford, U.K.Google Scholar
Rohde, K. (2002). Ecology and biogeography of marine parasites. Advances in Marine Biology 43, 1–86.Google Scholar
Siegel, S. and Castellan, N. J. Jr. (1998). The case of one sample, two measures or paired replicates. In Nonparametric Statistic for the Behavioral Sciences (ed. Siegel, S. and Castellan, N. J. Jr.), pp. 87–95. McGraw Hill, New York.Google Scholar
Sonenshine, D. E. (1991). Introduction. In Biology of Ticks (ed. Sonenshine, D. E.), pp. 3–12. Oxford University Press, New York.Google Scholar
Sonenshine, D. E. (1993). Tick-borne and tick-caused diseases. In Biology of Ticks (ed. Sonenshine, D. E.), pp. 107–330. Oxford University Press, New York.Google Scholar
Stone, B. F., Binnington, K. C., Gauci, M. and Aylward, J. H. (1989). Tick/host interactions for Ixodes holocyclus: Role, effects, biosynthesis and nature of its toxic and allergenic oral secretions. Experimental and Applied Acarology 7, 59–69.Google Scholar
Uilenberg, G. (1995). International collaborative research: significance of tick-borne hemoparasitic diseases to world animal health. Veterinary Parasitology 57, 19–41.Google Scholar
Supplementary material: File

Espinaze supplementary material

Espinaze supplementary material 1

Download Espinaze supplementary material(File)
File 79 KB
Supplementary material: PDF

Espinaze supplementary material

Espinaze supplementary material 2

Download Espinaze supplementary material(PDF)
PDF 138.6 KB