Skip to main content

Cryptosporidium and Giardia in feral water buffalo (Bubalus bubalis) in the South East Arnhem Land Indigenous Protected Area, Australia

Parasitology Research volume 119, pages 2149–2157 (2020)Cite this article

Abstract

Global investigations have implicated water buffalo (Bubalus bubalis) as a potential source of zoonotic Cryptosporidium and Giardia parasites which may pose a threat to human health. In Australia, buffalo are a feral pest that have colonised the floodplains, wetlands and woodlands of Indigenous owned and managed Arnhem Land, in tropical monsoonal Northern Australia. Indigenous people from the remote community Ngukurr have raised concerns about the potential threat to their health from shared use of surface waters inhabited by buffalo, in the South East Arnhem Land Indigenous Protected Area (SEAL IPA), Northern Australia. Surface waters are valued by local Indigenous people for spiritual and customary reasons, bush foods, medicines and drinking water. Here, we used molecular methods to characterise Cryptosporidium spp. and Giardia duodenalis assemblages from feral water buffalo living in the SEAL IPA to determine potential zoonotic risks to health of Indigenous people through co-use of surface water billabongs. Buffalo faecal DNA was screened for Cryptosporidium and Giardia using the 18S rRNA gene. Giardia were also screened using Glutamate hydrogenase (gdh) and βeta-giardin (β-giardin) genes. DNA sequencing identified C. ryanae in 9.9% (31/313) and G. duodenalis assemblage E 1.9% (6/313) in buffalo. Cryptosporidium ryanae is not considered zoonotic and G. duodenalis assemblage E is a livestock assemblage that has been reported in humans. Carriage of G. duodenalis assemblage E in buffalo may present a disease risk for Indigenous people utilising billabongs, according to customary practice.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Notes

  1. In Aboriginal English, “‘Country’ refers to more than just a geographical area: it is shorthand for all of the values, places, resources, stories and cultural obligations associated with that geographical area” (Smyth 1994).

  2. A billabong is an Australian term for an oxbow lake and a commonly used term by Indigenous people in Ngukurr.

References

  • Abdel-Moein KA, Saeed H (2016) The zoonotic potential of Giardia intestinalis assemblage E in rural settings. Parasitol Res 115(8):3197–3202

    Article  PubMed  Google Scholar 

  • Abeywardena H, Jex AR, von Samson-Himmelstjerna G, Haydon SR, Stevens MA, Gasser RB (2013) First molecular characterisation of Cryptosporidium and Giardia from Bubalus bubalis (water buffalo) in Victoria, Australia. Infect Genet Evol:2096–2102

  • Abeywardena H, Jex AR, Gasser RB (2015) A perspective on Cryptosporidium and Giardia, with an emphasis on bovines and recent epidemiological findings. Adv Parasitol:88243–88301

  • Albrecht G, McMahon C, Bowman DMJS, Bradshaw C (2009) Convergence of culture, ecology, and ethics: management of feral swamp buffalo in northern Australia. J Agric Environ Ethics 22(4):361–378

    Article  Google Scholar 

  • Amer S, Zidan S, Feng Y, Adamu H, Li N, Xiao L (2013) Identity and public health potential of Cryptosporidium spp. in water buffalo calves in Egypt. Vet Parasitol 191(1–2):123–127

    Article  PubMed  Google Scholar 

  • Aquino MCC, Widmer G, Zucatto AS, Viol MA, Inácio SV, Nakamura AA, Coelho WMD, Perri SHV, Meireles MV, Bresciani KDS (2015) First molecular characterization of Cryptosporidium spp. infecting buffalo calves in Brazil. J Eukaryot Microbiol 62(5):657–661

    Article  PubMed  CAS  Google Scholar 

  • Asher AJ, Holt DC, Andrews M, Power ML (2014) Distribution of Giardia duodenalis assemblages A and B amongst children living in a remote indigenous community of the Northern Territory. PLoS One 9(11):e112058

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Baldursson S, Karanis P (2011) Waterborne transmission of protozoan parasites: review of worldwide outbreaks–an update 2004–2010. Water Res 45(20):6603–6614

    Article  PubMed  CAS  Google Scholar 

  • Betancourt WQ, Rose JB (2004) Drinking water treatment processes for removal of Cryptosporidium and Giardia. Vet Parasitol 126(1–2):219–234

    Article  PubMed  CAS  Google Scholar 

  • Black EK, Finch GR, Taghi-Kilani R, Belosevic M (1996) Comparison of assays for Cryptosporidium parvum oocysts viability after chemical disinfection. FEMS Microbiol Lett 135(2–3):187–189

    Article  PubMed  CAS  Google Scholar 

  • Caccio SM, Rinaldi L, Cringoli G, Condoleo R, Pozio E (2007) Molecular identification of Cryptosporidium parvum and Giardia duodenalis in the Italian water buffalo (Bubalus bubalis). Vet Parasitol 150(1–2):146–149

    Article  PubMed  CAS  Google Scholar 

  • Ens EJ, Daniels C, Nelson E, Roy J, Dixon P (2016) Creating multi-functional landscapes: using exclusion fences to frame feral ungulate management preferences in remote Aboriginal-owned northern Australia. Biol Conserv 197:235–246

    Article  Google Scholar 

  • Fantinatti M, Bello AR, Fernandes O, Da-Cruz AM (2016) Identification of Giardia lamblia assemblage E in humans points to a new anthropozoonotic cycle. J Infect Dis 214(8):1256–1259

    Article  PubMed  Google Scholar 

  • Feng Y, Xiao L (2011) Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev 24(1):110–140

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Feng Y, Karna SR, Dearen TK, Singh DK, Adhikari LN, Shrestha A, Xiao L (2012) Common occurrence of a unique Cryptosporidium ryanae variant in zebu cattle and water buffaloes in the buffer zone of the Chitwan National Park, Nepal. Vet Parasitol 185(2–4):309–314

    Article  PubMed  Google Scholar 

  • Fong TT, Lipp EK (2005) Enteric viruses of humans and animals in aquatic environments: health risks, detection, and potential water quality assessment tools. Microbiol Mol Biol Rev 69(2):357–371

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fordham D, Georges A, Corey B, Brook BW (2006) Feral pig predation threatens the Indigenous harvest and local persistence of snake-necked turtles in northern Australia. Biol Conserv 133(3):379–388

    Article  Google Scholar 

  • Foronda P, Bargues MD, Abreu-Acosta N, Periago MV, Valero MA, Valladares B, Mas-Coma S (2008) Identification of genotypes of Giardia intestinalis of human isolates in Egypt. Parasitol Res 103(5):1177–1181

    Article  PubMed  CAS  Google Scholar 

  • Gomez-Couso H, Amar CF, McLauchlin J, Ares-Mazas E (2005) Characterisation of a Cryptosporidium isolate from water buffalo (Bubalus bubalis) by sequencing of a fragment of the Cryptosporidium oocyst wall protein gene (COWP). Vet Parasitol 131(1–2):139–144

    Article  PubMed  CAS  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59(3):307–321

    Article  PubMed  CAS  Google Scholar 

  • Helmy YA, Krücken J, Nöckler K, Von Samson-Himmelstjerna G, Zessin K-H (2013) Molecular epidemiology of Cryptosporidium in livestock animals and humans in the Ismailia province of Egypt. Vet Parasitol 193(1–3):15–24

    Article  PubMed  Google Scholar 

  • Helmy YA, Klotz C, Wilking H, Krücken J, Nöckler K, Von Samson-Himmelstjerna G, Zessin K-H, Aebischer T (2014) Epidemiology of Giardia duodenalis infection in ruminant livestock and children in the Ismailia province of Egypt: insights by genetic characterization. Parasit Vectors 7(1):321

    Article  PubMed  PubMed Central  Google Scholar 

  • Hopkins RM, Meloni BP, Groth DM, Wetherall JD, Reynoldson JA, Thompson RCA (1997) Ribosomal RNA sequencing reveals differences between the genotypes of Giardia isolates recovered from humans and dogs living in the same locality. J Parasitol 83(1):44–51

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755

    Article  CAS  PubMed  Google Scholar 

  • Hunter PR, Thompson RC (2005) The zoonotic transmission of Giardia and Cryptosporidium. Int J Parasitol 35(11–12):1181–1190

    Article  PubMed  Google Scholar 

  • Inpankaew T, Jiyipong T, Wongpanit K, Pinyopanuwat N, Chimnoi W, Kengradomkij C, Xuan X, Igarashi I, Xiao L, Jittapalapong S (2014) Molecular detection of Cryptosporidium spp. infections in water buffaloes from northeast Thailand. Trop Anim Health Prod 46(2):487–490

    Article  PubMed  Google Scholar 

  • Khaldi S, Ratajczak M, Gargala G, Fournier M, Berthe T, Favennec L, Dupont JP (2011) Intensive exploitation of a karst aquifer leads to Cryptosporidium water supply contamination. Water Res 45(9):2906–2914

    Article  PubMed  CAS  Google Scholar 

  • Kretzschmar AL, Verma A, Harwood T, Hoppenrath M, Murray S (2017) Characterization of Gambierdiscus lapillus sp. nov. (Gonyaulacales, Dinophyceae): a new toxic dinoflagellate from the Great Barrier Reef (Australia). J Phycol 53(2):283–297

    Article  PubMed  CAS  Google Scholar 

  • Lal A, Cornish LM, Fearnley E, Glass K, Kirk M (2015) Cryptosporidiosis: a disease of tropical and remote areas in Australia. PLoS Negl Trop Dis 9(9):e0004078

    Article  PubMed  PubMed Central  Google Scholar 

  • Lalle M, Pozio E, Capelli G, Bruschi F, Crotti D, Caccio SM (2005) Genetic heterogeneity at the beta-giardin locus among human and animal isolates of Giardia duodenalis and identification of potentially zoonotic subgenotypes. Int J Parasitol 35(2):207–213

    Article  PubMed  CAS  Google Scholar 

  • Letts GA (1964) Feral animals in the Northern Territory. Aust Vet J 40(3):84–88

    Article  Google Scholar 

  • Ma J, Li P, Zhao X, Xu H, Wu W, Wang Y, Guo Y, Wang L, Feng Y, Xiao L (2015) Occurrence and molecular characterization of Cryptosporidium spp. and Enterocytozoon bieneusi in dairy cattle, beef cattle and water buffaloes in China. Vet Parasitol 207(3–4):220–227

    Article  PubMed  Google Scholar 

  • Martins TA, Seixas M, Brito DRB, Martins FDC, Cardim ST, Melo P, da Paixão Guterres SF, Patrício EG, Garcia JL (2018) First identification of Cryptosporidium parvum subtype IIaA20G1R1 in water buffalos (Bubalus bubalis). Res Vet Sci:118181–118183

  • Matsubayashi M, Kimata I, Abe N. (2005) Identification of genotypes of Giardia intestinalis isolates from a human and calf in Japan

  • Monally Conceição Costa de A, Tatiani Vitor H, Valéria IS, Walter Bertequini N, Elis Domingos F, Miranda OBC, Rego AG, Giovanni W, Vasconcelos MM, Saraiva BKD (2019) First description of Giardia duodenalis in buffalo calves (Bubalus bubalis) in southwest region of São Paulo State, Brazil. Food Waterborne Parasitol 16

  • Ng-Hublin JSY, Combs B, Reid S, Ryan U (2017) Differences in the occurrence and epidemiology of cryptosporidiosis in Aboriginal and non-Aboriginal people in Western Australia (2002-2012). Infect Genet Evol 53:100–106

    Article  PubMed  Google Scholar 

  • Plutzer J, Ongerth J, Karanis P (2010) Giardia taxonomy, phylogeny and epidemiology: facts and open questions. Int J Hyg Environ Health 213(5):321–333

    Article  PubMed  Google Scholar 

  • Read CM, Monis PT, Thompson RC (2004) Discrimination of all genotypes of Giardia duodenalis at the glutamate dehydrogenase locus using PCR-RFLP. Infect Genet Evol 4(2):125–130

    Article  PubMed  CAS  Google Scholar 

  • Ryan U, Caccio SM (2013) Zoonotic potential of Giardia. Int J Parasitol 43(12–13):943–956

    Article  PubMed  CAS  Google Scholar 

  • Saalfeld K (2014) Feral buffalo (Bubalus bubalis): distribution and abundance in Arnhem Land, Northern Territory. Northern Territory Government

  • Smyth D (1994) Understanding Country: the importance of land and sea in Aboriginal and Torres Strait Islander societies. Key Issue Paper No.1

  • Triggs B (1996) Tracks, scats and other traces : a field guide to Australian mammals / Barbara Triggs. New ed. edition. Oxford University Press, Melbourne, Melbourne

    Google Scholar 

  • Xiao L (2010) Molecular epidemiology of cryptosporidiosis: an update. Exp Parasitol 124(1):80–89

    Article  PubMed  CAS  Google Scholar 

  • Xiao L, Singh A, Limor J, Graczyk TK, Gradus S, Lal A (2001) Molecular characterization of Cryptosporidium oocysts in samples of raw surface water and wastewater. Appl Environ Microbiol 67(3):1097–1101

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zahedi A, Phasey J, Boland T, Ryan U (2016) First report of Cryptosporidium species in farmed and wild buffalo from the Northern Territory, Australia. Parasitol Res 115(3):1349–1353

    Article  PubMed  Google Scholar 

  • Zahedi A, Field D, Ryan U (2017) Molecular typing of Giardia duodenalis in humans in Queensland-first report of assemblage E. Parasitology 144(9):1154–1161

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank the Traditional Owners of the SEAL IPA for supporting our research on their Country. Thanks also goes to the Macquarie University Department of Biological Sciences for the use of the laboratory facilities.

Funding

Funding for this research was received from Macquarie University’s Department of Environmental Science (Higher Degree Research grant) and The Nature Conservancy who supported the engagement of the Ngukurr Yangbala Rangers.

Author information

Authors and Affiliations

  1. Department of Environmental Sciences, Macquarie University, University Avenue, North Ryde, NSW, 2109, Australia

    Shaina Russell & Emilie Ens

  2. Department of Biological Sciences, Macquarie University, University Avenue, North Ryde, NSW, 2109, Australia

    Michelle Power

Authors
  1. Shaina Russell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michelle Power
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Emilie Ens
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shaina Russell.

Additional information

Section Editor: Lihua Xiao

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 14.9 kb)

ESM 2

(DOCX 15.9 kb)

ESM 3

(DOCX 17.6 kb)

ESM 4

(DOCX 18.4 kb)

ESM 5

(DOCX 17.0 kb)

ESM 6

(DOCX 17.5 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Russell, S., Power, M. & Ens, E. Cryptosporidium and Giardia in feral water buffalo (Bubalus bubalis) in the South East Arnhem Land Indigenous Protected Area, Australia. Parasitol Res 119, 2149–2157 (2020). https://doi.org/10.1007/s00436-020-06703-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-020-06703-6

Keywords

  • Giardia duodenalis assemblage E
  • Cryptosporidium ryanae
  • Feral water buffalo
  • Wetland
  • Northern Australia
  • Indigenous land