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Nematodes and cestodes of rodents in South Africa: baseline data on diversity and geographic distribution

Published online by Cambridge University Press:  30 August 2019

A. Spickett ,
K. Junker Open the ORCID record for K. Junker [Opens in a new window] ,
G. Froeschke ,
V. Haukisalmi  and
S. Matthee Open the ORCID record for S. Matthee [Opens in a new window]
A. Spickett
Affiliation:
Agricultural Research Council-Onderstepoort Veterinary Institute, Private Bag X05, Onderstepoort 0110, South Africa Department of Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa
K. Junker
Affiliation:
Agricultural Research Council-Onderstepoort Veterinary Institute, Private Bag X05, Onderstepoort 0110, South Africa
G. Froeschke
Affiliation:
Department of Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa
V. Haukisalmi
Affiliation:
Jaakontie 1 B 15, 33950 Pirkkala, Finland
S. Matthee*
Affiliation:
Department of Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa
*
Author for correspondence: S. Matthee, E-mail: smatthee@sun.ac.za
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Abstract

Currently, descriptive information on the host range and geographic distribution of helminth parasites associated with naturally occurring rodents in South and southern Africa is scant. Therefore, we embarked on a countrywide study to: (1) identify gastrointestinal helminths and their host range, and (2) provide baseline data on the geographic distribution of helminths across the country. Altogether, 55 helminth taxa were recovered from at least 13 rodent species (n = 1030) at 26 localities across South Africa. The helminth taxa represented 25 genera (15 nematodes, nine cestodes and one acanthocephalan). Monoxenous nematodes were the most abundant and prevalent group, while the occurrence of heteroxenous nematodes and cestodes was generally lower. The study recorded several novel helminth–host associations. Single-host-species infections were common, although multiple-host-species infections by helminth species were also recorded. Monoxenous nematodes and some cestodes were recovered countrywide, whereas heteroxenous nematodes were restricted to the eastern regions of South Africa. The study highlights the as yet unexplored diversity of helminth species associated with naturally occurring rodent species and provides initial data on their geographical distribution in South Africa.

Keywords

Helminthshost rangegeographic distributionrodentsSouth Africa
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e81
Copyright
Copyright © Cambridge University Press 2019 

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References

Anderson, RC (2000) Nematode parasites of vertebrates. Their development and transmission. p. 650. Wallingford, CABI Publishing.Google Scholar
Archer, CE, Appleton, CC, Mukaratirwa, S, Lamb, J and Schoeman, MC (2017) Endo-parasites of public-health importance recovered from rodents in the Durban metropolitan area, South Africa. South African Journal of Infectious Diseases 32, 57–66.Google Scholar
Barnard, CJ, Sayed, E, Barnard, LE, Behnke, JM, Abdel Nabi, I, Sherif, N, Shutt, A and Zalat, S (2003) Local variation in helminth burdens of Egyptian spiny mice (Acomys cahirinus dimidiatus) from ecologically similar sites: relationships with hormone concentrations and social behaviour. Journal of Helminthology 77, 197–207.Google Scholar
Baylis, H (1928) On a collection of nematodes from Nigerian mammals (chiefly rodents). Parasitology 20, 280–304.Google Scholar
Behnke, JM, Barnard, CJ, Mason, N, Harris, PD, Sherif, NE, Zalat, S and Gilbert, FS (2000) Intestinal helminths of spiny mice (Acomys cahirinus dimidiatus) from St Katherine's Protectorate in the Sinai, Egypt. Journal of Helminthology 74, 31–43.Google Scholar
Behnke, JM, Harris, PD, Bajer, A, et al. (2004) Variation in the helminth community structure in spiny mice (Acomys dimidiatus) from four montane wadis in the St Katherine region of the Sinai Peninsula in Egypt. Parasitology 129, 379–398.Google Scholar
Boomker, J, Horak, IG, Watermeyer, R and Booyse, DG (2000) Parasites of South African wildlife. XVI. Helminths of some antelope species from the eastern and western Cape Provinces. Onderstepoort Journal of Veterinary Research 67, 31–41.Google Scholar
Botha, M, Siebert, SJ and van den Berg, J (2016) Do arthropod assemblages fit the grassland and savanna biomes of South Africa? South African Journal of Science 112(9–10), 1–10.Google Scholar
Brouat, C, Kane, M, Diouf, M, Bâ, K, Sall-Dramé, R and Duplantier, JM (2007) Host ecology and variation in helminth community structure in Mastomys rodents from Senegal. Parasitology 134, 437–450.Google Scholar
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.Google Scholar
Carlberg, KA and Lang, BZ (2004) Infection with pinworms (Syphacia obvelata) does not affect the plasma corticosterone concentration in male, nonpregnant female and pregnant female rats. Contemporary Topics in Laboratory Animal Science 43, 46–49.Google Scholar
Collins, HM (1972) Cestodes from rodents in the Republic of South Africa. Onderstepoort Journal of Veterinary Research 39, 25–50.Google Scholar
Cramer, MD and Hoffman, MT (2015) The consequences of precipitation seasonality for Mediterranean–Ecosystem vegetation of South Africa. PLoS One 10, e0144512.Google Scholar
Dobson, A and Carper, R (1992) Global warming and potential changes in host–parasite and disease–vector relationships. pp. 201–214 in Peters, RL and Lovejoy, TE (Eds) Global warming and biodiversity. New Haven, Yale University Press.Google Scholar
Du Toit, N, Jansen van Vuuren, B, Matthee, S and Matthee, CA (2012) Biome specificity of distinct genetic lineages within the four-striped mouse Rhabdomys pumilio (Rodentia: Muridae) from southern Africa with implications for taxonomy. Molecular Phylogenetics and Evolution 65, 75–86.Google Scholar
Durette-Desset, MC and Digiani, MC (2005) The systematic position of some Ethiopian Nippostrongylinae (Nematoda, Trichostrongylina, Heligmosomoidea) from the National Collection of Animal Helminths. Onderstepoort, South Africa. Onderstepoort Journal of Veterinary Research 72, 55–65.Google Scholar
Dybing, NA, Fleming, PA and Adams, J (2013) Environmental conditions predict helminth prevalence in red foxes in Western Australia. International Journal for Parasitology: Parasites and Wildlife 2, 165–172.Google Scholar
Feliú, C, Renaud, F, Catzeflis, F, Hugot, J-P, Durand, P and Morand, S (1997) A comparative analysis of parasite species richness of Iberian rodents. Parasitology 115, 453–466.Google Scholar
Feliú, C, Ventura, J, Segovia, JM, Jiménez, L, Ribas, A and Gisbert, J (2009) Helminths of Microtus lusitanicus (Gerbe, 1879) (Rodentia: Cricetidae) in the Iberian Peninusla: faunistic and ecological considerations. Revista Ibero-Latinoameriricana de Parasitologia 68, 159–166.Google Scholar
Fichet-Calvet, E, Wang, J, Jomaa, I, Ismail, RB and Ashford, RW (2003) Patterns of the tapeworm Railliettina trapezoides infection in the fat sand rat Psammomys obesus in Tunisia: season, climatic conditions, host age and crowding effects. Parasitology 126, 481–492.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.Google Scholar
Froeschke, G, Harf, R, Sommer, S and Matthee, S (2010) Effects of precipitation on parasite burden along a natural climatic gradient in southern Africa – implications for possible shifts in infestation patterns due to global changes. Oikos 119, 1029–1039.Google 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.Google Scholar
Fuentes, MV, Cerezuela, AM and Galan-Puchades, MT (2000) A helminthological survey of small mammals (insectivores and rodents) in the Serra Calderona mountain (Valencian Community, Spain). Research and Reviews in Parasitology 60, 25–35.Google Scholar
Fuentes, MV, Sáez, S, Trelis, M, Galán-Puchades, MT and Esteban, JG (2004) The helminth community of the wood mouse, Apodemus sylvaticus, in the Sierra Espuna, Murcia, Spain. Journal of Helminthology 78, 219–223.Google Scholar
Fuentes, MV, Sainz-Elipe, S and Galan-Puchades, MT (2005a) Comparative analysis of the helminth community of the common shrew, Crocidura russula, of three western Mediterranean enclaves and the inland of the Iberian Peninsula. Research and Reviews in Parasitology 65, 37–42.Google Scholar
Fuentes, MV, Sainz-Elipe, S and Galan-Puchades, MT (2005b) The helminth community of the common shrew in a post–fire regenerated Mediterranean ecosystem. Helminthologia 42, 31–34.Google Scholar
Galbreath, KE and Hoberg, EP (2012) Return to Beringia: parasites reveal cryptic biogeographic history of North American pikas. Proceedings of the Royal Society B 279, 371–378.Google Scholar
Ganzorig, S, Batsaikhan, N, Samiya, R, Morishima, Y, Oku, Y and Kamiya, M (1999) A second record of adult Ascarops strongylina (Rudolphi, 1819) (Nematoda: Spirocercidae) in a rodent host. Journal of Parasitology 85, 283–285.Google Scholar
Georgiev, BB, Bray, RA and Littlewood, DTJ (2006) Cestodes of small mammals: taxonomy and life cycles. pp. 29–62 in Morand, S, Krasnov, BR and Poulin, R (Eds) Micromammals and macroparasites: from evolutionary ecology to management. Tokyo, Springer.Google Scholar
Gregory, RD (1990) Parasites and host geographic range as illustrated by waterfowl. Functional Ecology 4, 645–654.Google Scholar
Haukisalmi, V (1989) Intestinal helminth communities of Sorex shrews in Finland. Annales Zoologici Fennici 26, 401–409.Google Scholar
Haukisalmi, V (2008) Review of Anoplocephaloides species from African rodents, with the proposal of Afrobaeria n. g. (Cestoda: Anoplocephalidae). Helminthologia 45, 57–63.Google Scholar
Haukisalmi, V and Henttonen, H (1993) Coexistence in helminths of the bank vole Clethrionomys glareolus. I. Patterns of co-occurrence. Journal of Animal Ecology 62, 221–229.Google Scholar
Haukisalmi, V and Henttonen, H (2001) Biogeography of helminth parasitism in Lemmus Link (Arvicolinae), with the description of Paranoplocephala fellmani n. sp. (Cestoda: Anoplocephalidae) from the Norwegian lemming L. lemmus (Linnaeus). Systematic Parasitology 49, 7–22.Google Scholar
Haukisalmi, V, Henttonen, H and Tenora, F (1988) Population dynamics of common and rare helminths in cyclic vole populations. The Journal of Animal Ecology 57, 807–825.Google Scholar
Haukisalmi, V, Hardman, LM, Hardman, M, Rausch, RL and Henttonen, H (2008) Molecular systematics of the Holarctic Anoplocephaloides variabilis (Douthitt, 1915) complex, with the proposal of Microcephaloides n. g. (Cestoda: Anoplocephalidae). Systematic Parasitology 70, 15–26.Google Scholar
Haukisalmi, V, Hardman, LM, Henttonen, H, Laakkonen, J, Niemimaa, J, Hardman, M and Gubányi, A (2009) Molecular systematics and morphometrics of Anoplocephaloides dentata (Cestoda, Anoplocephalidae) and related species in voles and lemmings. Zoologica Scripta 38, 199–220.Google Scholar
Haukisalmi, V, Hardman, LM, Fedorov, VB, Hoberg, EP and Henttonen, H (2016) Molecular systematics and Holarctic phylogeography of cestodes of the genus Anoplocephaloides Baer, 1923 s. s. (Cyclophyllidea, Anoplocephalidae) in lemmings (Lemmus, Synaptomys). Zoologica Scripta 45, 88–102.Google Scholar
Haukisalmi, V, Ribas, A, Junker, K, Spickett, A, Matthee, S, Henttonen, H, Jrijer, J, Halajian, A, Anders, JL and Nakao, M (2018) Molecular systematics and evolutionary history of catenotaeniid cestodes (Cyclophyllidea). Zoologica Scripta 47, 221–230.Google Scholar
Hulbert, IAR and Boag, B (2001) The potential role of habitat on intestinal helminths of mountain hares, Lepus timidus. Journal of Helminthology 75, 345–349.Google Scholar
Ikeh, Z, Anosike, J and Okon, E (1992) Acanthocephalan infection in man in northern Nigeria. Journal of Helminthology 66, 241–242.Google Scholar
Inglis, WG, Harris, EA and Lewis, JW (1990) A new species of the nematode genus Aspiculuris Schulz, 1924 from Aethomys namaquensis (Mammalia: Rodentia) in the Kruger National Park, South Africa. Systematic Parasitology 17, 231–236.Google Scholar
Julius, RS, Schwan, EV and Chimimba, CT (2017) Helminth composition and prevalence of indigenous and invasive synanthropic murid rodents in urban areas of Gauteng Province, South Africa. Journal of Helminthology 92, 445–454.Google Scholar
Kinsella, LM (1991) Comparison of helminths of three species of mice, Podomys floridanus, Peromyscus gossypinus, and Peromyscus polionotus, from southern Florida. Canadian Journal of Zoology 69, 3079–3083.Google Scholar
Krasnov, BR, Shenbrot, GI, Khokhlova, IS and Degen, AA (2004) Relationship between host diversity and parasite diversity: flea assemblages on small mammals. Journal of Biogeography 31, 1857–1866.Google Scholar
Krasnov, BR, Korallo-Vinarskaya, NP, Vinarski, MV, Shenbrot, GI, Mouillot, D and Poulin, R (2008) Searching for general patterns in parasite ecology: host identity versus environmental influence on gamasid mite assemblages in small mammals. Parasitology 135, 229–242.Google Scholar
Lewis, JW (1987) Helminth parasites of British rodents and insectivores. Mammal Review 17, 81–93.Google Scholar
Lichtenfels, JR and Quigley, D (1968) Pseudabbreviata nudamphida gen. et sp. n. (Nematoda: Physalopteridae) from an African ‘lizard’. Journal of Parasitology 54, 1092–1094.Google Scholar
Littlewood, DT, Curini-Galletti, M and Herniou, EA (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution 16, 449–466.Google Scholar
Lockyer, AE, Olson, PD and Littlewood, DTJ (2003) Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biological Journal of the Linnean Society 78, 155–171.Google Scholar
Lutermann, H, Medger, K and Junker, K (2014) Endoparasites of the spiny mouse (Acomys spinosissimus) from South Africa. Journal of Parasitology 100, 144–146.Google Scholar
Lutermann, H, Medger, K and Junker, K (2015) Endoparasites of the eastern rock sengi (Elephantulus myurus) from South Africa. Journal of Parasitology 101, 677–681.Google Scholar
Macnish, MG, Ryan, UM, Behnke, JM and Thompson, RCA (2003) Detection of the rodent tapeworm Rodentolepis (=Hymenolepis) microstoma in humans. A new zoonosis? International Journal for Parasitology 33, 1079–1085.Google Scholar
Mas-Coma, S, Valero, MA and Bargues, MD (2008) Effects of climate change on animal and zoonotic helminthiases. Scientific and Technical Review of the Office International des Epizooties 27, 443–452.Google Scholar
Milazzo, C, Casanova, JC, Aloise, G, Ribas, A and Cagnin, M (2002) The helminth community of Talpa romana (Thomas, 1902) (Insectivora, Talpidae) in southern Italy. Parasitology Research 88, 979–983.Google Scholar
Milazzo, C, Aloise, G, Cagnin, M, Di Bella, C, Geraci, F, Feliu, C and Casanova, JC (2005) Helminths of Apodemus sylvaticus (Muridae) distributed on the southern European Border (Italian Peninsula). Vie et Milieu 55, 45–51.Google Scholar
Milazzo, C, Cagnin, M, Di Bella, C, Geraci, F and Ribas, A (2010) Helminth fauna of commensal rodents, Mus musculus (Linnaeus, 1758) and Rattus rattus (Linnaeus, 1758) (Rodentia, Muridae) in Sicily (Italy). Revista Ibero-latinoamericana de Parasitologia 69, 197–198.Google Scholar
Nielsen, MK, Kaplan, RM, Thamsborg, SM, Monrad, J and Olsen, SN (2007) Climatic influences on development and survival of free–living stages of equine strongyles: implications for worm control strategies and managing anthelmintic resistance. The Veterinary Journal 174, 23–32.Google Scholar
Ortlepp, RJ (1939) South African helminths, Part VI. Some helminths, chiefly from rodents. Onderstepoort Journal of Veterinary Science and Animal Industry 12, 75–101.Google Scholar
Ortlepp, RJ (1940) South African helminths, Part VII. Miscellaneous helminths, chiefly cestodes. Onderstepoort Journal of Veterinary Science and Animal Industry 14, 97–110.Google Scholar
Ortlepp, RJ (1962) On two new Catenotaenia tapeworms from a South African rat with remarks on the species of the genus. Onderstepoort Journal of Veterinary Science and Animal Industry 29, 11–19.Google Scholar
Pakdeenarong, N, Siribat, P, Chaisiri, K, Douangboupha, B, Ribas, A, Chaval, Y, Herbreteau, V and Morand, S (2014) Helminth communities in murid rodents from southern and northern localities in Lao PDR: the role of habitat and season. Journal of Helminthology 88, 302–309.Google Scholar
Portolés, E, Granel, P, Esteban, GJ and Caberet, J (2004) Helminth associations in white–toothed shrews Crocidura russula (Insectivora: Soricidae) from the Albufera Natural Park, Spain. Journal of Parasitology 90, 572–578.Google Scholar
Poulin, R (2007) Evolutionary ecology of parasites. p. 360. Princeton, Princeton University Press.Google Scholar
Poulin, R, Krasnov, BR, Mouillot, D and Thieltges, DW (2011) The comparative ecology and biogeography of parasites. Philosophical Transactions of the Royal Society B 366, 2379–2390.Google Scholar
Price, PW (1990) Host populations as resources defining parasite community organisation. pp. 21–40 in Esch, GW, Bush, AO and Aho, JM (Eds) Parasite communities: patterns and processes. London, Chapman & Hall.Google Scholar
Price, PW and Clancy, KM (1983) Patterns in number of helminth parasite species in fresh water fishes. Journal of Parasitology 69, 449–454.Google Scholar
Procheş, Ş and Cowling, R (2007) Do insect distributions fit our biomes? South African Journal of Science 103, 258–261.Google Scholar
QGIS Development Team (2016) QGIS geographic information system. Open Source Geospatial Foundation. Available at http://qgis.osgeo.org (accessed 20 June 2017).Google Scholar
Quentin, JC (1964) Nématodes parasites de rongeurs du Congo. Parc National de l'Upemba. – Mission G.F. de Witte en collaboration avec W. Adam, L. van Meel et R. Verheyen (1946–1949) 69, 73–91.Google Scholar
R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org/.Google Scholar
Rambau, RV, Robinson, TJ and Stanyon, R (2003) Molecular genetics of Rhabdomys pumilio subspecies boundaries: mtDNA phylogeography and karyotypic analysis by fluorescence in situ hybridization. Molecular Phylogenetics and Evolution 28, 564–575.Google Scholar
Ribas, A and Casanova, JC (2006) Acanthocephalans. pp. 81–90 in Morand, S, Krasnov, BR and Poulin, R (Eds) Micromammals and macroparasites: from evolutionary ecology to management. Tokyo, Springer.Google Scholar
Sands, AF, Matthee, S, Mfune, JKE and Matthee, CA (2015) The influence of life history and climate driven diversification on the mtDNA phylogenetic structures of two southern African Mastomys species (Rodentia: Muridae: Murinae). Biological Journal of the Linnean Society 114, 58–68.Google Scholar
Salehabadi, A, Mowlavi, G and Sadjjadi, SM (2008) Human infection with Moniliformis moniliformis (Bremser, 1811) (Travassos, 1915) in Iran: another case report after three decades. Vector–Borne and Zoonotic Diseases 8, 101–103.Google Scholar
Schmidt, GD (1971) Acanthocephalan infections of man, with two new records. Journal of Parasitology 57, 582–584.Google Scholar
Shimalov, VV (2001) Helminth fauna of the common shrew (Sorex aureus Linnaeus, 1785) in ecosystems of Belorussian Polesie transformed by reclamation. Parasitological Research 87, 792–793.Google Scholar
Shostak, AW (2014) Hymenolepis diminuta infections in tenebrionid beetles as a model system for ecological interactions between helminth parasites and terrestrial intermediate hosts: a review and meta–analysis. Journal of Parasitology 100, 46–58.Google Scholar
Skinner, JD and Chimimba, CT (2005) The mammals of the southern African subregion. p. 814. Cape Town, Cambridge University Press.Google Scholar
Smales, LR and Spratt, DM (2004) Helminth community structure in Rattus leucopus (Gray) (Muridae) from Australia, Papua New Guinea and Papua. Australian Journal of Zoology 52, 283–291.Google Scholar
Sousa, WP and Grosholz, D (1991) The influence of habitat structure on the transmission of parasites. pp. 300–324 in Bell, SS, McCoy, ED and Mushinsky, HR (Eds) Habitat structure: the physical arrangement of objects in space. London, Chapman & Hall.Google Scholar
Spickett, A, Junker, K, Krasnov, BR, Haukisalmi, V and Matthee, S (2017) Helminth parasitism in two closely related South African rodents: abundance, prevalence, species richness and impinging factors. Parasitology Research 116, 1395–1409.Google Scholar
Stuart, C and Stuart, T (2007) Field guide to mammals of southern Africa. p. 307. Cape Town, Struik Nature.Google Scholar
Taffs, LF (1976) Pinworm infections in laboratory rodents: a review. Laboratory Animals 10, 1–13.Google Scholar
Turner, WC and Getz, WM (2010) Seasonal and demographic factors influencing gastrointestinal parasitism in ungulates of Etosha National Park. Journal of Wildlife Diseases 46, 1108–1119.Google Scholar
Verster, A (1960) Trichuris species from South African rodents and a hyracoid. Onderstepoort Journal of Veterinary Research 28, 465–471.Google Scholar
von Nickisch-Rosenegk, M, Brown, WM and Boore, JL (2001) Complete sequence of the mitochondrial genome of the tapeworm Hymenolepis diminuta: gene arrangements indicate that platyhelminths are eutrochozoans. Molecular Biology and Evolution 18, 721–730.Google Scholar
Waugh, CA, Lindo, JF, Foronda, P, Ángeles-Santana, M, Lorenzo-Morales, J and Robinson, RD (2006) Population distribution and zoonotic potential of gastrointestinal helminths of wild rats Rattus rattus and R. norvegicus from Jamaica. Journal of Parasitology 92, 1014–1018.Google Scholar
Wilamowski, A, Moran, S and Greenburg, Z (2002) Commensal rodents and their parasites in Israel. pp. 103–112 in Proceedings of the 4th International Conference on Urban Pests, 7-10/07/2002, Charleston, SC.Google Scholar
Wilson, DE and Reeder, DAM (2005) Mammal species of the world. A taxonomic and geographic reference. Available at http://www.press.jhu.edu (accessed 12 July 2017).Google Scholar
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