Landscape characteristics influence helminth infestations in a peri-domestic rodent - implications for possible zoonotic disease

Particle and Fibre Toxicology

Sonja Matthee¹  Götz Froeschke¹ 

[1] Department of Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Stellenbosch 7602, South Africa

关键词: South Africa;    Small mammal;    Helminth;    Zoonotic disease;    Landuse;   

Others  :  1181843
DOI  :  10.1186/1756-3305-7-393

 received in 2014-02-18, accepted in 2014-08-18,  发布年份 2014

【 摘 要 】

Background

Anthropogenic habitat change often results in altered landscapes that can provide new environments where hosts, parasites and pathogens can interact. The latter can have implications for human and animal health when in close proximity to developed areas. We recorded the helminth species richness and level of infestation in the peri-domestic rodent, Rhabdomys pumilio, in three different human linked landscapes. The aim was, to investigate the potential of R. pumilio to act as a reservoir host for zoonotic helminths and to compare the effect of anthropogenic habitat change on its parasite infestation patterns.

Methods

Rodents (n = 518) were trapped in natural areas (nature reserves) and in three human linked landscapes (crop, livestock and urban fragments). Gastrointestinal parasite burdens were recovered and helminths identified from each animal. Generalized linear models were applied to investigate the effect of different landscape types on helminth infestation.

Results

Rhabdomys pumilio was the most abundant rodent species within each landscape type. Eight helminths species were recovered and overall helminth prevalence was 86.68%. Mean helminth species richness, prevalence and abundance were significantly higher in crop fragments compared to natural landscapes and overall lower for nematodes in livestock and urban areas. Cestode prevalence showed a tendency to be elevated at anthropogenic linked landscape types.

Conclusions

Host parameters and parasite infestations were strongly influenced by landscape characteristics. Resource-rich landscapes (crop fragments) provide favorable conditions for helminth infestations, while landscapes that are more closely associated with humans (livestock and urban landscapes) pose a larger risk by zoonotic species.

【 授权许可】

   
2014 Froeschke and Matthee; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Price PW: Evolutionary Biology of Parasites. Princeton, New Jersey: Princeton University Press; 1980.
• [2]Brooks DR, Hoberg EP: Systematics and emerging infectious diseases: from management to solution. J Parasitol 2006, 92:426-429.
• [3]Taylor LH, Latham SM, Woolhouse ME: Risk factors for human disease emergence. Philos T Roy Soc B 2001, 356:983-989.
• [4]Weil ZM, Martin LB II, Nelson RJ: Interactions Among Immune, Endocrine, and Behavioural Response to Infection. In Micromammals and Macroparasites. Edited by Morand S, Krasnov BR, Poulin R. Tokyo: Springer; 2006:443-473.
• [5]Stear MH, Bairden K, Duncan JL, Holmes PH, McKellar QA, Park M, Stain S, Murray M, Bishop SC, Gettinby G: How hosts control worms. Nature 1997, 389:27.
• [6]Mas-Coma S, Valero MA, Bargues MD: Effects of climate change on animal and zoonotic helminthiases. Rev Sci Tech 2008, 27:443-452.
• [7]WHO: Parasitic Zoonoses. Report of a WHO Expert Committee with Participation of FAO. Geneva, Switzerland; 1979. Technical report series 637
• [8]Albon SD, Stien A, Irvine RJ, Langvatn R, Ropstad E, Halvorsen O: The role of parasites in the dynamics of a reindeer population. Proc R Soc Lond B Biol Sci 2002, 269:1625-1632.
• [9]Mouritsen KN, Poulin R: Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 2002, 2002(124):S101-S117.
• [10]Dobson AP, Carper ER: Infectious diseases and human population history. Biosci 1996, 46:115-126.
• [11]Jackson LE, Hilborn ED, Thomas JC: Towards landscape design guidelines for reducing Lyme disease risk. Int J Epidemiol 2006, 35:315-322.
• [12]McGinnis S, Kerans BL: Land use and host community characteristics as predictors of disease risk. Landscape Ecol 2013, 28:29-44.
• [13]Hulbert IAR, Boag B: The potential role of habitat on intestinal helminths of mountain hares, Lepus timidus. J Helminth 2001, 75:345-349.
• [14]Brouat C, Kane M, Diouf BK, Sall-Dramé R, Duplalntier JM: Host ecology and variation in helminth community structure in Mastomys rodents from Senegal. Parasitology 2007, 134:437-450.
• [15]Ollerenshaw CB, Smith LP: Meterological factors and forecasts of helminthic disease. Adv Parasitol 1969, 7:283-323.
• [16]Froeschke G, Harf R, Sommer S, Matthee S: 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 2010, 119:1029-1039.
• [17]Graham AJ, Danson FM, Giraudoux P, Craig PS: Ecological epidemiology: landscape metrics and human alveolar echinococossis. Acta Trop 2004, 91:267-278.
• [18]Karesh WB, Dobson A, Lloyd-Smith JO, Lubroth J, Dixon MA, Bennett M, Aldrich S, Harrington T, Formenty P, Loh EH, Machalaba CC, Thomas MJ, Heymann DL: Ecology of zoonoses: natural and unnatural histories. Lancet 2012, 380:1936-1945.
• [19]Murray KA, Daszak P: Human ecology in pathogenic landscapes: two hypotheses on how land use change drives viral emergence. Curr Opin Virol 2013, 3:79-83.
• [20]Reperant LA, Hegglin D, Tanner I, Fischer C, Deplazes P: Rodents as shared indicators for zoonotic parasites of carnivores in urban environments. Parasitology 2009, 136:329-337.
• [21]Reisen WK: Landscape epidemiology of vector-borne diseases. Annu Rev Entomol 2010, 55:461-483.
• [22]Wilson DE, Reeder DM: Mammal Species of the World. Baltimore, MD: Johns Hopkins University Press; 2005.
• [23]Jittapalapong S, Herbreteau V, Hugot J-P, Aresrisom P, Karnchananabanthoeng A, Rerkamnuaychoke W, Morand S: Relationship of parasites and pathogens diversity to rodents in Thailand. Kasetsart J (Nat Sci) 2009, 43:106-117.
• [24]Luis AD, Hayman DTS, O’Shea TJ, Cryan PM, Gilbert AT, Pulliam JRC, Mills JN, Timonin ME, Willis CKR, Cunningham AA, Fooks AR, Rupprecht CE, Wood JLN, Webb CT: A comparison of bats and rodents as reservoir of zoonotic viruses: are bats special? Proc R Soc B 2013, 280:20122753.
• [25]Klimpel S, Förster M, Schmahl G: Parasite fauna of the bank vole (Clethrionomys glareolus) in an urban region of Germany: reservoir host of zoonotic metazoan parasites? Parasitol Res 2007, 102:69-75.
• [26]McKinney ML: Urbanization, biodiversity, and conservation. Biosci 2002, 52:883-890.
• [27]van der Mescht L, Le Roux PC, Matthee S: Remnant fragments within an agricultural matrix enhance conditions for a rodent host and its fleas. Parasitology 2013, 1:1-10.
• [28]Froeschke G, van der Mescht L, McGeoch M, Matthee S: Life history strategy influences parasite responses to habitat fragmentation. Int J Parasitol 2013, 43:1109-1118.
• [29]Wilcox BA, Gubler DJ: Disease ecology and the global emergence of zoonotic pathogens. Environ Health Prev Med 2005, 10:263-272.
• [30]Chaisiri K, Chaeychomsri W, Siruntawineti J, Bordes F, Herbreteau V, Morand S: Human-dominated habitats and helminth parasitism in Southeast Asian murids. Parasitol Res 2010, 107:931-937.
• [31]McFarlane R, Sleigh A, McMichael T: Synanthropy of wild mammals as a determinant of emerging infectious diseases in the Asian-Australasian region. Ecohealth 2012, 9:24-35.
• [32]Bordes F, Herbreteau V, Dupuy S, Chaval Y, Tran A, Morand S: The diversity of microparasites of rodents: a comparative analysis that helps in identifying rodent-borne rich habitats in Southeast Asia. IEE 2013, 3:20178. http://dx.doi.org/10.3402/iee.v3i0.20178 webcite
• [33]Gillespie TR, Chapman CA, Greiner EC: Effects of logging on gastrointestinal parasite infections and infection risk in African primates. J Appl Ecol 2005, 42:699-707.
• [34]Bull JC, Jepson PD, Ssuna RK, Deaville R, Allchin CR, Law RJ, Fenton A: The relationship between polychlorinated biphenyls in blubber and levels of nematode infestations in harbour porpoises, Phocoena phocoena. Parasitology 2006, 132:565-573.
• [35]Wells K, Smales LR, Kalko EKV, Pfeiffer M: Impact of rain-forest logging on helminth assemblages in small mammals (Muridae, Tupaiidae) from Borneo. J Trop Ecol 2007, 23:35-43.
• [36]Gillespie TR, Chapman CA: Forest fragmentation, the decline of an endangered primate, and changes in host–parasite interactions relative to an unfragmented forest. Am J Primatol 2008, 70:222-230.
• [37]Rohr JR, Schotthoefer AM, Raffel TR, Carrick HJ, Halstead N, Hoverman JT, Johnson CM, Johnson LB, Lieske C, Piwoni MD, Schoff PK, Beasley VR: Agrochemicals increase trematode infections in a declining amphibian species. Nature 2008, 455:1235-1239.
• [38]Püttker T, Meyer-Lucht Y, Sommer S: Effects of fragmentation on parasite burden (nematodes) of generalist and specialist small mammal species in secondary forest fragments of the coastal Atlantic Forest, Brazil. Ecol Res 2008, 23:207-215.
• [39]Raharivololona BM, Ganzhorn JU: Gastrointestinal parasite infection of the gray mouse lemur (Microcebus murinus) in the littoral forest of Mandena, Madagascar: effects of forest fragmentation and degradation. Madag Conserv Dev 2009, 4:103-112.
• [40]Bradley AB, Altizer S: Urbanization and the ecology of wildlife diseases. Trends Ecol Evol 2007, 22:95-102.
• [41]Farrell MJ, Berrang-Ford L, Davies TJ: The study of parasite sharing for surveillance of zoonotic diseases. Environ Res Lett 2013, 8:015036.
• [42]Cowling RM, Pressey RL, Rouget M, Lombard AT: A conservation plan for a global biodiversity hotspot – the Cape Floristic Region, South Africa. Biol Conserv 2003, 112:191-216.
• [43]Rebelo AG: Preservation of biotic diversity. In The Ecology of Fynbos. Nutrients, Fire and Diversity. Edited by Cowling RM. Cape Town: Oxford University Press; 1992:309-344.
• [44]Skinner JD, Chimimba CT: The Mammals of the Southern African Subregion. South Africa: Cambridge University Press; 2005.
• [45]Tipton VJ: The genus Laelaps. With review of the Laelaptinae and a new subfamily Alphalaelaptinae (Acarina: Laelaptinae). Univ Calif Publ Entomol 1960, 16:233-356.
• [46]De Meillon B, Davis D, Hardy F: Plaque in Southern Africa - The Siphonaptera (Excluding Ischnopsyllidae), Volume 1. Government Printer: South Africa, Pretoria; 1961.
• [47]Zumpt F: The Arthropod Parasites of Vertebrates in Africa South of the Sahara. Volume 1 (Chelicerata). South Africa, Johannesburg: Publications of the South African Institute for Medical Research. South African Institute for Medical Research; 1961.
• [48]Till WM: Ethiopian mites of the genus Androlaelaps Berlese s. lat. (Acari: Mesostigmata). Bull Nat Hist Mus Zool 1963, 10:1-104.
• [49]Ledger JA: The Arthropod Parasites of Vertebrates in Africa South of the Sahara. Volume IV. Phthiraptera (Insecta). South Africa, Johannesburg: South African Institute for Medical Research; 1980.
• [50]De Graaff G: The Rodents of Southern Africa. South Africa, Durban: Butterworths; 1981.
• [51]Horak IG, Sheppey K, Knight MM, Beuthin CL: Parasites of domestic and wild animals in South Africa. XXI. Arthropod parasites of vaal ribbok, bontebok and scrub hares in the Western Cape Province. Onderstepoort J Vet Res 1986, 53:187-197.
• [52]Horak IG, Boomker J: Parasites of domestic and wild animals in South Africa, XXXV. Ixodid ticks and bot fly larvae in the Bontebok National Park. Onderstepoort J Vet Res 1998, 65:205-211.
• [53]Howell DJ, Petney TN, Horak IG: The host status of the striped mouse, Rhabdomys pumilio, in relation to the tick vectors of heartwater in South Africa. Onderstepoort J Vet Res 1989, 56:289-291.
• [54]Segerman J: Siphonaptera of Southern Africa. Handbook for the Identification of Fleas. South Africa, Johannesburg: Publications of The South African Institute for Medical Research No. 57; 1995.
• [55]Petney TN, Horak IG, Howell DJ, Meyer S: Striped mice, Rhabdomys pumilio, and other murid rodents as hosts for immature ixodid ticks as in the Eastern Cape Province. Onderstepoort J Vet Res 2004, 71:313-318.
• [56]Matthee S, Horak IG, Beaucournu J-C, Durden LA, Ueckermann EA, McGeoch MA: Epifaunistic arthropod parasites of the four-striped mouse, Rhabdomys pumilio, in the Western Cape Province, South Africa. J Parasitol 2007, 93:47-59.
• [57]Matthee S, Horak IG, van der Mescht L, Ueckermann EA, Radloff FGT: Ectoparasite diversity on rodents at De hoop nature reserve, western cape province. Afr Zool 2010, 45:213-224.
• [58]Shepherd AJ, Leman PA: Plaque in South African rodents. Trans R Soc Trop Med H 1983, 77:208-211.
• [59]Walker JB: A review of the ixodid ticks (Acari, Ixodidae) occurring in Southern Africa. Onderstepoort J Vet Res 1991, 58:81-105.
• [60]Drexler JF, Corman VM, Müller MA, Maganga GD, Vallo P, Binger T, Gloza-Rausch F, Rasche A, Yordanov S, Seebens A, Oppong S, Sarkodie YA, Pongombo C, Lukashev AN, Schmidt-Chanasit J, Stöcker A, Carneiro AJB, Erbar S, Maisner A, Fronhoffs F, Buettner R, Kalko EDV, Kruppa T, Franke CR, Kallies R, Yandoko ERN, Herrler G, Reusken C, Hassanin A, Krüger DH, et al.: Bats host major mammalian paramyxoviruses. Nat Commun 2012, 3:796.
• [61]Drexler JF, Corman VM, Müller MA, Lukashev AN, Gmyl A, Coutard B, Adam A, Ritz D, Leijten LM, van Riel D, Kallies R, Klose SM, Gloza-Rausch F, Binger T, Annan A, Adu-Sarkodie Y, Oppong S, Bourgarel M, Rupp D, Hoffmann B, Schlegel M, Kümmerer BM, Krüger DH, Schmidt-Chanasit J, Setien AA, Cottontail VM, Hemachudha T, Wacharapluesadee S, Osterrieder K, Bartenschlager R, et al.: Evidence for novel Hepaciviruses in rodents. Plos Pathog 2013, 9:e1003428.
• [62]Aremu AO, Finnie JF, Van Staden J: Potential of South African medicinal plants used as anthelmintics – their efficacy, safety concerns and reappraisal of current screening methods. S Afr J Bot 2012, 82:134-150.
• [63]Adams VJ, Markus MB, Adams FA, Jordaan E, Curtis B, Dhansay MA, Obihara CC, Fincham JE: Paradoxical helminthiasis and giardiasis in Cape Town, South Africa: epidemiology and control. Afr Health Sci 2005, 5:131-136.
• [64]Gómez M, Nunn CL, Verdú M: Centrality in primate-parasite networks reveals the potential for the transmission of emerging infectious diseases to humans. Proc Natl Acad Sci U S A 2013, 110:7738-7741.
• [65]Apps PE: Smither’s Mammals of Southern Africa – A Field Guide. South Africa, Johannesburg: Southern Book Publishers; 2000.
• [66]Rangel TF, Diniz-Filho JAF, Bini LM: SAM: a comprehensive application for spatial analysis in macroecology. Ecography 2010, 33:46-50.
• [67]Meyer-Lucht Y, Otten C, Puttker T, Pardini R, Metzger JP, Sommer S: Variety matters: adaptive genetic diversity and parasite load in two mouse opossumsfrom the Brazilian Atlantic forest. Conserv Genet 2010, 11:2001-2013.
• [68]Crawley MJ: The R Book. 1st edition. Oxford: Wiley Publishing; 2007.
• [69]Zuur A, Leno EN, Walker N, Saveliev AA, Smith GM: Mixed Effects Models and Extensions in Ecology With R. New York: Springer; 2009.
• [70]Venables WN, Ripley BD: Modern Applied Statistics with S. 4th edition. New York: Springer; 2002.
• [71]Atkinson J-AM, Gray DJ, Clements ACA, Barnes TS, McManus DP, Yang YR: Environmental changes impacting Echinococcus transmission: research to support predictive surveillance and control. Glob Change Biol 2013, 19:677-688.
• [72]Ostfeld RS, Lidicker WZ Jr, Heske EJ: The relationship between habitat heterogeneity, space use, and demography in a population of California voles. Oikos 1985, 1985(45):433-442.
• [73]Dickman CR, Doncaster CP: The ecology of small mammals in urban habitats. I. Populations in a patchy environment. J Anim Ecol 1987, 56:629-640.
• [74]Eccard JA, Walther RB, Milton SJ: How livestock grazing affects vegetation structures and small mammal distribution in the semi-arid Karoo. J Arid Environ 2000, 46:103-106.
• [75]Ernest SKM, Brown JH, Parmenter RR: Rodents, plants, and precipitation: spatial and temporal dynamics of consumers and resources. Oikos 2000, 88:470-482.
• [76]Jensen SP, Gray SJ, Hurst JL: How does habitat structure affect activity and use of space among house mice? Anim Behav 2003, 66:239-250.
• [77]Baker PJ, Ansell RJ, Dodds PAA, Webber CE, Harris S: Factors affecting the distribution of small mammals in an urban area. Mammal Rev 2003, 33:95-100.
• [78]Durette-Desset M-C: Phylogeny of Trichostrongyloidea nematodes as seen through some of their vertebrate hosts. Parasitologia 1992, 34:1-16.
• [79]Crofton HD: The ecology of immature phases of Trichostrongyle nematodes: I. The vertical distribution of infective larvae of Trichostrongylus retortaeformis in relation to their habitat. Parasitology 1948, 39:17-25.
• [80]Crofton HD: The ecology of immature phases of Trichostrongyle nematodes: II. The vertical distribution of infective larvae of Trichostrongylus retortaeformis in relation to their habitat. Parasitology 1948, 39:26-38.
• [81]Jones HG: Plants and Microclimate: A Quantitative Approach to Environmental Plant Physiology. Cambridge: Cambridge University Press; 1983.
• [82]Broekhuizen S, Kemmers R: The stomach worm, Graphidium Strigosum (Dujardin) Railliet and Henry, in the European Hare, Lepus Europaeus Pallus. In The Ecology and Management of European Hare Populations. Edited by Pielowski Z, Pucek Z. Warsaw: Polish Hunting Association; 1976:157-170.
• [83]Anderson RC: Nematode Parasites of Vertebrates: Their Development and Transmission. 2nd edition. Wallingford: CAB International; 2000.
• [84]Anderson RM, May RM: Regulation and stability of host-parasite population interactions I. Regulatory processes. J Anim Ecol 1978, 47:219-247.
• [85]Sorci G, Møller AP, Boulinier T: Genetics of host-parasite interactions. TREE 1997, 12:196-200.
• [86]Arneberg P, Skorping A, Read AF: Parasite abundance, body size, life histories, and the energetic equivalence rule. Am Nat 1998, 151:497-513.
• [87]Connell JH: Diversity in tropical rain forests and coral reefs. Science 1978, 199:1302-1310.
• [88]Shea K, Roxburgh SH, Rauschert ESJ: Moving from pattern to process: coexistence mechanisms under intermediate disturbance regimes. Ecol Lett 2004, 7:491-508.
• [89]Gallet R, Alizon S, Comte P-A, Gutierrez A, Depaulis F, van Baalen M, Michel E, Müller-Graf CDM: Predation and disturbance interact to shape prey species diversity. Am Nat 2007, 170:143-154.
• [90]Morand S, Bouamer S, Hugot J-P: Nematodes. In Micromammals and Macroparasites. Edited by Morand S, Krasnov BR, Poulin R. Berlin: Springer; 2006:63-80.
• [91]Friggens MM, Beier P: Anthropogenic disturbance and the risk of flea-borne disease transmission. Oecologica 2010, 164:809-820.
• [92]Schmidt NM, Olsen H, Bildsøe M, Sluydts V, Leirs H: Effects of grazing intensity on small mammal population ecology in wet meadows. Basic Appl Ecol 2005, 6:57-66.
• [93]Keesing F: Impacts of ungulates on the demography and diversity of small mammals in central Kenya. Oecologia 1998, 116:381-389.
• [94]Caro TM: Factors affecting the small mammal community inside and outside Katavi National Park, Tanzania. Biol Conserv 2002, 34:310-318.
• [95]Bock CE, Bock JH, Kenney WR, Hawthorne VM: Responses of birds, rodents, and vegetation to livestock exclosure in a semidesert grassland site. J Range Manage 1984, 37:239-242.
• [96]Edge WD, Wolff JO, Carey RL: Density-dependent responses of gray-tailed voles to mowing. J Wildl Manage 1995, 59:245-251.
• [97]Peles JD, Barrett GW: Effects of vegetation cover on the population dynamics of meadow voles. J Mammal 1996, 77:857-869.
• [98]Chaisiri K, Chaeychomsri W, Siruntawineti J, Ribas A, Herbreteau V, Morand S: Diversity of gastrointestinal helminths among murid rodents from northern and northeastern Thailand. Southeast Asian J Trop Med Public Health 2012, 43:21-28.
• [99]Lloyd-Smith JO, Cross PC, Briggs CJ, Daugherty M, Getz WM, Latto J, Sanchez MS, Smith AB, Swei A: Should we expect population thresholds for wildlife disease? Trends Ecol Evol 2005, 20:511-519.
• [100]Winternitz JC, Yabsley MJ, Altizer SM: Parasite infection and host dynamics in a naturally fluctuating rodent population. Can J Zool 2012, 90:1149-1160.
• [101]Grice RL, Prociv P: In vitro embryonation of Syphacia obvelata eggs. Int J Parasitol 1993, 23:257-260.
• [102]Pisanu B, Chapuis J-L, Durette-Desset M-C, Morand S: Epizootiology of Syphacia obvelata from a domestic mouse population on the Subantarctic Kerguelen Archipelago. J Parasitol 2002, 88:645-649.
• [103]Reckardt K, Kerth G: Does the mode of transmission between hosts affect the host choice strategies of parasites? Implications from a field study on bat fly and wing mite infestation of Bechstein’s bats. Oikos 2009, 118:183-190.
• [104]Foronda P, López-González M, Hernández M, Haukisalmi V, Feliu C: Distribution and genetic variation of hymenolepidid cestodes in murid rodents on the Canary Islands (Spain). Parasit Vectors 2011, 4:185. BioMed Central Full Text
• [105]Baldwin R, Fasulo TR: Confused Flour Beetle, Tribolium Confusum Jacquelin du Val (Insecta: Coleoptera: Tenebrionidae) and Red Flour Beetle, Tribolium Castaneum (Herbst) (Insecta: Coleoptera: Tenebrionidae). Florida, USA: University of Florida IFAS Extension; 2003.
• [106]Durett-Desset MC, Digiani MC: The systematic position of some Ethiopian Nippostrongylinae (Nematoda, Trichostrongylina, Heligmosomoidea) from the National Collection of Animal Helminths, Onderstepoort, South Africa. Onderstepoort J Vet Res 2005, 72:55-65.
• [107]Adamson ML: Evolutionary biology of the Oxyourida (Nematoda): biofacies of a haplodiploid taxon. Adv Parasitol 1989, 28:175-228.
• [108]Morrisey JK: Parasites of ferrets, rabbits and rodents. Semin Avian Exot Pet Med 1996, 5:106-114.
• [109]Michels C, Goyal P, Nieuwenhuizen N, Brombacher F: Infection with Syphacia obvelata (pinworm) induces protective Th2 immune responses and influences ovalbumin-induced allergic reactions. Infect Immun 2006, 74:5926-5932.
• [110]Eslami A, Changizy E, Moghadam M: Prevalence of helminth infections in the cape hare (Lepus capensis) in Iran. Vet Res Comm 2000, 24:455-458.
• [111]Goldsmid JM: The African hookworm problem: an overview. In Parasitic Helminths and Zoonoses in Africa. Edited by MacPherson CNL, Craig PS. London: Unwin Hyman; 1991:01-37.
• [112]Marcus LC: Oesophagostomiasis. In CRC Handbook Series in Zoonoses. Edited by Steele JH. Florida: CRC Press; 1982:221-223.
• [113]Tongson MS, Eduardo SL: Trichostrongylidiosis. In CRC Handbook Series in Zoonoses. Edited by Steele JH. Florida: CRC Press; 1982:331-337.
• [114]Feliu C, Spakulova M, Casanova JC, Renaud F, Morand S, Hugot JP, Santalla F, Durand P: Genetic and morphological heterogeneity in small rodent whipworms in southwestern Europe: Characterization of Trichuris muris and description of Trichuris arvicolae n. sp (Nematoda: Trichuridae). J Parasitol 2000, 86:442-449.
• [115]Macpherson CNL, Craig PS: Zoonotic Helminthes of wild and domestic animals in Africa. In Parasitic Helminthes and Zoonoses in Africa. London: Unwin Hyman; 1991:260-272.
• [116]Harkness JE, Wagner JE: Specific Diseases and Conditions. In Harkness and Wagner’s Biology and Medicine of Rabbits and Rodents. 5th edition. Ames: Wiley Blackwell; 2010:235-236.
• [117]Jenkins DJ, Andrew PL: Intestinal parasites in dogs from an Aboriginal community in New South Wales. Aust Vet J 1993, 70:115-116.
• [118]Thompson RCA, Meloni BP, Hopkins RM, Deplazes P, Reynoldson JA: Observations on the endo- and ectoparasites affecting dogs and cats in Aboriginal communities in the north-west of Western Australia. Aust Vet J 1993, 70:268-269.
• [119]Zain SNM, Behnke JM, Lewis JW: Helminth communities from two urban rat populations in Kuala Lumpur Malaysia. Parasit Vectors 2012, 5:47. BioMed Central Full Text
• [120]Hopkins CA, Goodall RI, Zajac A: The longevity of Hymenolepis microstoma in mice, and its immunological cross reaction with Hymenolepis diminuta. Parasitology 1977, 74:175-183.
• [121]Smyth JD, McManus DP: The Physiology and Biochemistry of Cestodes. UK, Cambridge: Cambridge University Press; 1989.
• [122]Macnish MG, Ryan UM, Behnke JM, Thompson RCA: Detection of the rodent tapeworm Rodentolepis (=Hymenolepis) microstoma in humans. A new zoonosis? Int J Parasitol 2003, 33:1079-1085.
• [123]Goodall RI: The growth of Hymenolepis microstoma in the laboratory rat. Parasitology 1972, 65:137-142.
• [124]Feliu C, Renaud F, Catzeflis F, Hugot J-P, Durande P, Morand S: A comparative analysis of parasite species richness of Iberian rodents. Parasitology 1997, 115:453-466.