Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-26T19:01:27.536Z Has data issue: false hasContentIssue false
  • English
  • Français

The diversity and distribution of chigger mites associated with rodents in the South African savanna

Published online by Cambridge University Press:  04 May 2020

Sonja Matthee Open the ORCID record for Sonja Matthee [Opens in a new window] ,
Alexandr A. Stekolnikov ,
Luther van der Mescht ,
Götz Froeschke  and
Serge Morand Open the ORCID record for Serge Morand [Opens in a new window]
Sonja Matthee*
Affiliation:
Department of Conservation Ecology and Entomology, Stellenbosch University, 7602 Stellenbosch, South Africa
Alexandr A. Stekolnikov
Affiliation:
Zoological Institute of the Russian Academy of Sciences, Saint Petersburg, Russia
Luther van der Mescht
Affiliation:
Department of Conservation Ecology and Entomology, Stellenbosch University, 7602 Stellenbosch, South Africa
Götz Froeschke
Affiliation:
Department of Conservation Ecology and Entomology, Stellenbosch University, 7602 Stellenbosch, South Africa
Serge Morand
Affiliation:
CNRS – ISEM Montpellier University, Montpellier, France CIRAD – Faculty of Veterinary Technology, Katsetsart University, Bangkok, Thailand
*
Author for correspondence: Sonja Matthee, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Chigger mites (Trombiculidae) are temporary habitat-specific ectoparasites that often occur on rodents. Little ecological data are available on chiggers associated with rodents in South Africa. The study aims were to (1) record the chigger species associated with rodents in the savanna, (2) assess if chigger species display parasitope preference on the rodent body and (3) compare the distribution of chigger species in natural, agricultural and urban habitats. Rodents (n = 314) belonging to eight genera were trapped in the savanna biome during 2014 and 2015. Twelve chigger species, of which five are recently described species, were recorded from 161 rodent hosts. The data include three new country locality records. Microtrombicula mastomyia was the most prevalent species across sampling seasons and habitat types. Significant parasitope preference was recorded for two species, with the ear, face and tail base some of the preferred attachment sites. Sampling season and habitat type had a significant effect on chigger communities with summer and agricultural habitats recording the highest species richness, while the highest species diversity was recorded in natural habitats. The study contributes to our current knowledge regarding rodent-associated chigger diversity and distribution in South Africa and further highlights the importance of environmental characteristics in shaping chigger communities.

Keywords

Habitat typeparasitoperodentsSouth AfricaTrombiculidae
Type
Research Article
Information
Parasitology , Volume 147 , Issue 9 , August 2020 , pp. 1038 - 1047
Check for updates
Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

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.)

References

Allred, MA (1954) Observations on the stylostome (feeding tube) of some Utah chiggers. Proceedings of the Utah Academy of Sciences, Arts and Letters 31, 61–63.Google Scholar
Apesteguía, MA, Portell, JBA, Kassab, NH and Salinas, MJG (2019) Severe Trombiculiasis in hunting dogs infested with Neotrombicula inopinata (Acari: Trombiculidae). Journal of Medical Entomology 56, 1389–1394.CrossRefGoogle Scholar
Barnard, K, Krasnov, BR, Goff, ML and Matthee, S (2015) Infracommunity dynamics of chiggers (Trombiculidae) parasitic on a rodent. Parasitology 142, 1605–1611.CrossRefGoogle ScholarPubMed
Bastos, AD, Nair, D, Taylor, PJ, Brettschneider, H, Kirsten, F, Mostert, E, von Maltitz, E, Lamb, JM, van Hooft, P, Belmain, SR, Contrafatto, G, Downs, S and Chimimba, CT (2011) Genetic monitoring detects an overlooked cryptic species and reveals the diversity and distribution of three invasive Rattus congeners in South Africa. BMC Genetics 12, 26.CrossRefGoogle ScholarPubMed
Burnham, KP and Anderson, DR (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, 2nd Edn.New York, NY: Springer.Google Scholar
Calcagno, V and de Mazancourt, C (2010) Glmulti: an R package for easy automated model selection with (Generalized) Linear Models. Journal of Statistical Software 34, 12. Available at http://www.jstatsoft.org/.CrossRefGoogle Scholar
Chaisiri, K, Stekolnikov, AA, Makepeace, BL and Morand, S (2016) A revised checklist of chigger mites (Acari: Trombiculidae) from Thailand, with the description of three new species. Journal of Medical Entomology 53, 321–342.CrossRefGoogle ScholarPubMed
Choi, MB, Lee, W-G, Kang, HJ, Yang, S-C, Song, BG, Shin, E-H and Kwon, O (2017) Seasonal prevalence and species composition of mosquitoes and chigger mites collected from Daegu, Gunwi and Sangju in South Korea, 2014. Journal of Ecology and Environment 41, 15.CrossRefGoogle Scholar
Clopton, RE and Gold, RE (1993) Distribution and seasonal and diurnal activity patterns of Eutrombicula alfreddugesi (Acari: Trombiculidae) in a forest edge ecosystem. Journal of Medical Entomology 30, 47–53.CrossRefGoogle Scholar
Cramer, MJ and Willig, MR (2005) Habitat heterogeneity, species diversity and null models. OIKOS 108, 209–218.CrossRefGoogle Scholar
Cunha-Barros, M, Van Sluys, M, Vrcibradic, D, Galdino, CAB, Hatano, FH and Rocha, CFD (2003) Patterns of infestation by chigger mites in four diurnal lizard species from a restinga habitat (Jurubatiba) of Southeastern Brazil. Brazilian Journal of Biology 63, 393–399.CrossRefGoogle ScholarPubMed
Domrow, R and Lester, LN (1985) Chiggers of Australia (Acari: Trombiculidae): an annotated checklist, keys and bibliography. Australian Journal of Zoology, Supplementary Series 114, 1–111.CrossRefGoogle Scholar
Fagir, DM, Ueckermann, EA, Horak, IG, Bennett, NC and Lutermann, H (2014) The Namaqua rock mouse (Micaelamys namaquensis) as a potential reservoir and host of arthropod vectors of diseases of medical and veterinary importance in South Africa. Parasites & Vectors 7, 366.CrossRefGoogle ScholarPubMed
Fagir, DM, Horak, IG, Ueckermann, EA, Bennett, NC and Lutermann, H (2015) Ectoparasite diversity in the eastern rock sengi (Elephantulus myurus): the effect of seasonality and host sex. African Zoology 50, 109–117.CrossRefGoogle Scholar
Fernandes, S and Kulkarni, SM (2003) Studies on the trombiculid mite fauna of India. Records of the Zoological Survey of India. Occasional Paper 212, 1–539.Google Scholar
Froeschke, G and Matthee, S (2014) Landscape characteristics influence helminth infestations in a peri-domestic rodent – implications for possible zoonotic disease. Parasites & Vectors 7, 393.CrossRefGoogle Scholar
Froeschke, G, van der Mescht, L, McGeoch, M and Matthee, S (2013) Life history strategy influences parasite responses to habitat fragmentation. International Journal for Parasitology 43, 1109–1118.CrossRefGoogle ScholarPubMed
Goff, ML (1979) Host exploitation by chiggers (Acari: Trombiculidae) infesting Papua New Guinea land mammals. Pacific Insects 20, 321–353.Google Scholar
Goijman, AP, Conroy, MJ, Bernardos, JN and Zaccagnini, ME (2015) Multi-season regional analysis of multi-species occupancy: implications for bird conservation in agricultural lands in East-Central Argentina. PLoS ONE 10, e0130874.CrossRefGoogle ScholarPubMed
Guo, XG, Dong, WG, Men, XY, Qian, TJ, Wu, D, Ren, TG, Qin, F, Song, WY, Yang, ZH and Fletcher, QE (2016) Species abundance distribution of ectoparasites on Norway rats (Rattus norvegicus) from a localized area in Southwest China. Journal of Arthropod-Borne Diseases 10, 192–200.Google ScholarPubMed
Janion, C (2013) Springtail diversity in the Cape Floristic Region (PhD thesis). Stellenbosch University, Stellenbosch, South Africa.Google Scholar
Kalúz, S, Hung, NM, Čapek, M and Literák, I (2016) Two new species and new records of chiggers (Acari: Leeuwenhoekiidae, Trombiculidae) from birds in Vietnam. Zootaxa 4061, 483–503.CrossRefGoogle ScholarPubMed
Kitaoka, M, Okubo, K, Asanuma, K and Otsuji, J (1972) Birds in the ecology of scrub typhus. Journal of Medical Entomology 9, 594.Google Scholar
Kitaoka, M, Asanuma, K and Otsuji, J (1976) Experiments on chickens placed on ground endemic of classical scrub typhus in Akita prefecture, Japan. Journal of Hygiene, Epidemiology, Microbiology, and Immunology 21, 195–200.Google ScholarPubMed
Klukowski, M (2004) Seasonal changes in abundance of host-seeking chiggers (Acari: Trombiculidae) and infestations on fence lizards, Sceloporus undulates. Journal of Herpetology 38, 141–144.CrossRefGoogle Scholar
Kudryashova, NI (1998) Chigger Mites (Acariformes, Trombiculidae) of East Palaearctics. Moscow: KMK Scientific Press.Google Scholar
Kuo, CC, Huang, JL, Ko, CY, Lee, PF and Wang, HC (2011) Spatial analysis of scrub typhus infection and its association with environmental and socioeconomic factors in Taiwan. Acta Tropica 120, 52–58.CrossRefGoogle ScholarPubMed
Kweka, EJ, Zhou, G, Munga, S, Lee, MC, Atieli, HE, Nyindo, M, Githeko, AK and Yan, G (2012) Anopheline larval habitats seasonality and species distribution: a prerequisite for effective targeted larval habitats control programmes. PLoS ONE 7, e52084.CrossRefGoogle ScholarPubMed
Lawrence, R (1949) The larval trombiculid mites of South African vertebrates. Annals of the Natal Museum 11, 405–486.Google Scholar
Leinaas, HP, Bengtsson, J, Janion-Scheepers, C and Chown, SL (2015) Indirect effects of habitat disturbance on invasion: nutritious litter from a grazing resistant plant favors alien over native collembola. Ecology and Evolution 5, 3462–3471.Google ScholarPubMed
Maharaj, R, Raman, J, Morris, N, Moonasar, D, Durrheim, DN, Seocharan, I, Kruger, P, Shandukani, B and Kleinschmidt, I (2013) Epidemiology of malaria in South Africa: from control to elimination. South African Medical Journal 103, 779–783.Google Scholar
Malan, K (2015) Taxonomy and ecology of parasitic chigger mites (Acari: Trombiculidae) on small mammals in South Africa (MSc dissertation). Stellenbosch University, Stellenbosch, South Africa.Google Scholar
Massawe, AW, Mulungu, LS, Makundi, RH, Dlamini, N, Eiseb, SJ, Kirsten, F, Mahlaba, T, Malebane, P, Von Maltitz, E, Monadjem, A, Taylor, P, Tutjavi, V and Belmain, SR (2011) Spatial and temporal population dynamics of rodents in three geographically different regions in Africa : implication for ecologically-based rodent management. African Zoology 46, 393–405.Google Scholar
Mohr, CO (1947) Notes on chiggers, rats and habitats on New Guinea and Luzon. Ecology 28, 194–199.CrossRefGoogle Scholar
Moniuszko, H and Mąkol, J (2016) Host-parasite association in trombiculid mites (Actinotrichida: Trombiculidae) of temperate zone – the case of Hirsutiella zachvatkini (Schluger, 1948); are we dealing with prolonged contact with the host? Parasites & Vectors 9, 61.CrossRefGoogle ScholarPubMed
Moniuszko, H, Felska, M and Mąkol, J (2018) Evidence for co-invasion events: different chigger species (Actinotrichida. Trombidioidea: Trombiculidae) share a host. Experimental and Applied Acarology 76, 29.CrossRefGoogle ScholarPubMed
Mucina, L and Rutherford, MC (2006) The Vegetation of South Africa, Lesotho and Swaziland, Strelitzia 19, Pretoria. South Africa: South African National Biodiversity Institute.Google Scholar
Mullen, GR and OConnor, BM (2019) Mites (Acari). In Mullen, GR and Durden, LA (eds), Medical and Veterinary Entomology, 3rd Edn.London: Elsevier Academic Press, pp. 533–602.CrossRefGoogle Scholar
Munhenga, G, Brooke, BD, Spillings, B, Essop, L, Hunt, RH, Midzi, S, Govender, D, Braack, L and Koekemoer, LL (2014) Field study site selection, species abundance and monthly distribution of anopheline mosquitoes in the northern Kruger National Park, South Africa. Malaria Journal 13, 27.CrossRefGoogle ScholarPubMed
Murray, MD (1987) Effects of host grooming on louse populations. Parasitology Today 3, 276–278.Google ScholarPubMed
Mutuku, FM, Bayoh, MN and Gimnig, JE (2006) Pupal habitat productivity of Anopheles gambiae complex mosquitoes in a rural village in western Kenya. American Journal of Tropical Medicine and Hygiene 74, 54–61.CrossRefGoogle Scholar
Nadchatram, M (1970) Correlation of habitat, environment and colour of chiggers and their potential significance in the epidemiology of scrub typhus in Malaya. Journal of Medical Entomology 7, 131–144.CrossRefGoogle ScholarPubMed
Nelson, BC and Murray, MD (1971) The distribution of mallophaga on the domestic pigeon (Columba livia). International Journal for Parasitology 1, 21–29.CrossRefGoogle Scholar
Oksanen, J, Blanchet, FG, Friendly, M, Kindt, R, Legendre, P, McGlinn, D, Minchin, PR, O'Hara, RB, Simpson, GL, Solymos, P, Stevens, MHH, Szoecs, E and Wagner, H (2018) vegan: Community Ecology Package (R package version 2.5-2). Available at https://CRAN.R-project.org/package=vegan.Google Scholar
Pardini, R, Nichols, E and Püttker, T (2018) Biodiversity response to habitat loss and fragmentation. In Dellasala, DA and Goldstein, MI (eds), Encyclopedia of the Anthropocene. Oxford: Elsevier, Oxford, pp. 229–239.CrossRefGoogle Scholar
Pearson, R (2016) GoodmanKruskal: association analysis for categorical variables. Available at https://CRAN.R-project.org/package=GoodmanKruskal.Google Scholar
R Development Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org/.Google Scholar
Reddy, MV and Venkataiah, B (1990) Seasonal abundance of soil-surface arthropods in relation to some meteorological and edaphic variables of the grassland and tree-planted areas in a tropical semi-arid savanna. International Journal of Biometeorology 34, 49–59.CrossRefGoogle Scholar
Reeves, WK, Durden, LA and Wrenn, WJ (2004) Ectoparasitic chiggers (Acari: Trombiculidae, Leeuwenhoekiidae), lice (Phthiraptera), and Hemiptera (Cimicidae and Reduviidae) from South Carolina, USA. Zootaxa 647, 1–20.CrossRefGoogle Scholar
Roux, PW (1963) The descending-point method of vegetation survey: a point-sampling method for the measurement of semi-open grasslands and karoo vegetation in South Africa. South African Journal of Agricultural Science 6, 273–288.Google Scholar
Rutherford, MC, Mucina, L and Powrie, LW (2006) Biomes and bioregions of Southern Africa. In Mucina, L and Rutherford, MC (eds), Vegetation of South Africa, Lesotho and Swaziland. Pretoria, South Africa: South African National Biodiversity Institute, pp. 30–51.Google Scholar
Sasa, M (1961) Biology of chiggers. Annual Review of Entomology 6, 221–244.CrossRefGoogle Scholar
Sasal, P, Morand, S and Guégan, JF (1997) Determinants of parasite species richness in Mediterranean marine fishes. Marine Ecology Progress Series 149, 61–71.CrossRefGoogle Scholar
Shatrov, AB and Kudryashova, NI (2006) Taxonomy, life cycles and the origin of parasitism in trombiculid mites. In Morand, S, Krasnov, BR and Poulin, R (eds), Micromammals and Macroparasites: From Evolutionary Ecology to Management. London: Churchill Livingstone Elsevier, Tokyo, Japan: Springer-Verlag, pp. 119–140.CrossRefGoogle Scholar
Shatrov, AB and Stekolnikov, AA (2011) Redescription of a human-infesting European trombiculid mite Kepkatrombicula desaleri (Acari: Trombiculidae) with data on its mouthparts and stylostome. International Journal of Acarology 37, 176–193.CrossRefGoogle Scholar
Singh, SR and van Emden, HF (1979) Insect pests of grain legumes. Annual Review of Entomology 24, 255–278.CrossRefGoogle Scholar
Skinner, JD and Chimimba, CT (2005) The Mammals of the Southern African Sub-Region. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Stekolnikov, AA (2002) Variability of chigger mites of the N. talmiensis group, genus Neotrombicula Hirst, 1925 (Acari, Trombiculidae) in areas of sympatry in the Western Caucasus. Entomological Review 82, 1178–1189.Google Scholar
Stekolnikov, AA (2018) Taxonomy and distribution of African chiggers (Acariformes, Trombiculidae). European Journal of Taxonomy 395, 1–233.Google Scholar
Stekolnikov, AA and Matthee, S (2019) Six new and one little known species of chigger mites (Acariformes: Trombiculidae) from South Africa. Systematic & Applied Acarology 24, 435–466.CrossRefGoogle Scholar
Stekolnikov, AA, Kessler, SE, Matthee, S, Hasiniaina, AF, Radespiel, U, Zimmermann, E and Durden, LA (2019) A new species of Schoutedenichia Jadin & Vercammen-Grandjean, 1954 from Madagascar and a re-description of S. dutoiti (Radford, 1948) from South Africa (Acariformes: Trombiculidae). Systematic Parasitology 96, 703–713.CrossRefGoogle Scholar
Stuart, C and Stuart, M (2001) Stuart's Field Guide to Mammals of Southern Africa. Cape Town, South Africa: Struik Nature.Google Scholar
Teitelbaum, CS, Huang, S, Hall, RJ and Altizer, S (2018) Migratory behaviour predicts greater parasite diversity in ungulates. Proceedings. Biological Sciences 285, 20180089.Google ScholarPubMed
Traub, R and Morrow, ML (1955) A revision of the chiggers of the subgenus Gahrliepia (Acarina: Trombiculidae). Smithsonian Miscellaneous Collections 128, 1–89.Google Scholar
Traub, R and Wisseman, CL (1968) Ecological considerations on scrub typhus. 2. Vector species. Bulletin of the World Health Organization 39, 219–230.Google ScholarPubMed
Traub, R and Wisseman, CL (1974) The ecology of chigger-borne rickettsiosis (scrub typhus). Journal of Medical Entomology 11, 237–303.CrossRefGoogle Scholar
Van Niekerk, JH (2017) Orange River Francolins (Scleroptila levaillantoides) persist in fragmented Highveld farming landscapes, South Africa. Avian Research 8, 11.CrossRefGoogle Scholar
Vercammen-Grandjean, PH (1958) Revision du genre Schoutedenichia Jad. et Verc. Annales du Musée royal du Congo belge, série in 8, 1–103.Google Scholar
Vercammen-Grandjean, PH (1960) Trombiculidae larvaires de l'Afrique septentrionale et centrale. Huit espèces nouvelles et six sous-genres nouveaux (Acarina). Archives de l'Institut Pasteur d'Algérie 38, 50–69.Google Scholar
Vercammen-Grandjean, PH (1965a) Revision of the genera: Eltonella Audy, 1956 and Microtrombicula Ewing, 1950, with descriptions of fifty new species and transferal of subgenus Chiroptella to genus Leptotrombidium (Acarina, Trombiculidae). Acarologia 7 (suppl.), 34–257.Google Scholar
Vercammen-Grandjean, PH (1965b) Trombiculinae of the World: Synopsis with Generic, Subgeneric, and Group Diagnoses. San Francisco, CA: George Williams Hooper Foundation, University of California.Google Scholar
Vercammen-Grandjean, PH (1966) Revision of the genus Herpetacarus Vercammen-Grandjean, 1960 (Trombiculidae – Acarina). Acarologia 8, 631–674.Google Scholar
Vercammen-Grandjean, PH and Langston, RL (1976) The Chigger Mites of the World (Acarina: Trombiculidae et Leeuwenhoekiidae). Vol. III. Leptotrombidium Complex. San Francisco, CA: George Williams Hooper Foundation, University of California.Google Scholar
Waage, JK (1979) The evolution of insect/vertebrate associations. Biological Journal of the Linnean Society 12, 187–224.CrossRefGoogle Scholar
Walter, DE and Krantz, GW (2009) Collection, rearing, and preparing specimens. In Krantz, GW and Walter, DE (eds), A Manual of Acarology. Texas Tech University Press, Lubbock, Texas, pp. 83–96.Google Scholar
Weedon, D (2010) Arthropod induced diseases. In Weedon's Skin Pathology, 3rd Edn.London: Churchill Livingstone Elsevier, pp. 651–663.CrossRefGoogle Scholar
Wharton, G (1946) Observations on Ascoschongastia Indica (Hirst 1915) (Acarinida: Trombiculidae). Ecological Monographs 16, 152–184.CrossRefGoogle Scholar
Williams, RW (1946) A contribution to our knowledge of bionomics of the common North American chigger, Eutrombicula alfreddugesi (Oudemans) with a description of a rapid collecting method. The American Journal of Tropical Medicine and Hygiene 26, 243–250.CrossRefGoogle Scholar
Zhan, YZ, Guo, XG, Speakman, JR, Zuo, XH, Wu, D, Wang, QH and Yang, ZH (2013) Abundances and host relationships of chigger mites in Yunnan Province, China. Medical and Veterinary Entomology 27, 194–202.CrossRefGoogle ScholarPubMed
Zumpt, F (1961) The Arthropod Parasites of Vertebrates in Africa South of the Sahara. Vol. I (Chelicerata). Publications of the South African Institute for Medical Research. Johannesburg, South Africa: South African Institute for Medical Research, p. 457.Google Scholar
Supplementary material: Image

Matthee et al. Supplementary Materials

Matthee et al. Supplementary Materials 1
Download Matthee et al. Supplementary Materials(Image)
Image 118.3 KB
Supplementary material: Image

Matthee et al. Supplementary Materials

Matthee et al. Supplementary Materials 2

Download Matthee et al. Supplementary Materials(Image)
Image 1.5 MB