Skip to main content

Advertisement

Log in

Attempted Detection of Toxoplasma gondii Oocysts in Environmental Waters Using a Simple Approach to Evaluate the Potential for Waterborne Transmission in the Galápagos Islands, Ecuador

  • Short Communication
  • Published:
EcoHealth Aims and scope Submit manuscript

Abstract

Toxoplasmosis is a health concern for wildlife and humans, particularly in island ecosystems. In the Galápagos Islands, exposure to Toxoplasma gondii has been found in marine avifauna on islands with and without domestic cats. To evaluate potential waterborne transmission of T. gondii, we attempted to use filtration and epifluorescent microscopy to detect autofluorescent T. gondii oocysts in fresh and estuarine surface water samples. T. gondii oocyst-like structures were microscopically visualized but were not confirmed by polymerase chain reaction and sequence analyses. Further research is needed to refine environmental pathogen screening techniques and to evaluate disease risk of waterborne zoonoses such as T. gondii for wildlife and humans, particularly in the Galápagos and other naive island ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

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

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4

References

  • Afonso E, Thulliez P, Pontier D, and Gilot-Fromont E (2007). Toxoplamsosis in prey species and consequences for prevalence in feral cats: not all prey species are equal. Parsitology 134:1963-1971.

    Article  CAS  PubMed  Google Scholar 

  • Bahia-Oliveira LM, Jones JL, Azevedo-Silva J, Alves CC, Orefice F, and Addiss DG (2003). Highly endemic, waterborne toxoplasmosis in north Rio de Janeiro state, Brazil. Emerg Infect Dis 9:55-62.

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bowie WR, King AS, Werker DH, Isaac-Renton JL, Bell A, Eng SB, et al. (1997). Outbreak of toxoplasmosis associated with municipal drinking water. The BC Toxoplasma Investigation Team. Lancet 350:173-177.

    Article  CAS  PubMed  Google Scholar 

  • Carlson-Bremer D, Johnson CK, Miller RH, Gulland FMD, Conrad PA, Wasmuth JD, et al. (2011). Identification of two novel coccidian species shed by California sea lions (Zalophus californianus). Journal of Parasitology 98:347-354.

    Article  PubMed  Google Scholar 

  • Colegrove KM, Grigg ME, Carlson-Bremer D, Miller RH, Gulland FMD, Ferguson DJP, et al. (2011). Discovery of three novel coccidian parasites infecting California sea lions (Zalophus californianus), with evidence of sexual replication and interspecies pathogenicity. Journal of Parasitology 97:868-877.

    Article  PubMed  Google Scholar 

  • Conrad PA, Miller MA, Kreuder C, James ER, Mazet J, Dabritz H, et al. (2005). Transmission of Toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. International Journal for Parasitology 35:1155-1168.

    Article  CAS  PubMed  Google Scholar 

  • d’Ozouville N (2007) Fresh water in the Galapagos: the reality of a critic resource. CDF, SPNG, INGALA, Puerto Ayora, Santa Cruz, Galapagos, Ecuador.

  • d’Ozouville N, Deffontaines B, Benveniste J, Wegmuller U, Violette S, and Marsily Gd (2008). DEM generation using ASAR (ENVISAT) for addressing the lack of freshwater ecosystems management, Santa Cruz Island, Galapagos Remote Sensing of Environment 112:4131-4147.

    Article  Google Scholar 

  • Davies A, and Stewart B (2000). Autofluorescence in the oocysts of marine and freshwater fish coccidia. Folia Parasitologica 47:157-158.

    Article  CAS  PubMed  Google Scholar 

  • Deem S, Merkel J, Ballweber L, Vargas FH, Cruz M, and Parker P (2010). Exposure to Toxoplasma gondii in Galapagos Penguins (Spheniscus mendiculus) and flightless cormorants (Phalacrocorax harrisi) in the Galapagos Islands, Ecuador. Journal of Wildlife Disease 46:1005-1011.

    Article  Google Scholar 

  • Dubey J (1995). Duration of immunity to shedding of Toxoplasma gondii oocysts by cats. Journal of Parasitology 81:410-415.

    Article  CAS  PubMed  Google Scholar 

  • Dubey J (2002). A review of toxoplasmosis in wild birds. Veterinary Parasitology 106:121-153.

    Article  CAS  PubMed  Google Scholar 

  • Dubey J, and Frenkel J (1972). Cyst-Induced Toxoplasmosis in Cats*. Journal of Eukaryotic Microbiology 19:155-177.

    CAS  Google Scholar 

  • Duffie CV, Glenn TC, Vargas FH, and Parker PG (2009). Genetic structure within and between island populations of the flightless cormorant (Phalacrocorax harrisi). Molecular Ecology 18:2103-2111.

    Article  PubMed  Google Scholar 

  • Dumètre A, and Dardé ML (2005). Immunomagnetic separation of Toxoplasma gondii oocysts using a monoclonal antibody directed against the oocyst wall. Journal of Microbiological Methods 61:209-217.

    Article  PubMed  Google Scholar 

  • Gallas-Lindemann C, Sotiriadou I, Mahmoodi MR, and Karanis P (2013). Detection of Toxoplasma gondii oocysts in different water resources by Loop Mediated Isothermal Amplification (LAMP). Acta Tropica 125:231-236.

    Article  CAS  PubMed  Google Scholar 

  • Glynn PW (1988). El Nino Southern Oscillation 1982-1983 - Nearshore population, community, and ecosystem responses. Annual Review of Ecology and Systematics 19:309-345.

    Google Scholar 

  • González J, Montes C, Rodríguez J, and Tapia W (2008). Rethinking the Galapagos Islands as a complex social-ecological system: implications for conservation and management. Ecology and Society 13:13.

    Google Scholar 

  • Gottdenker NL, Walsh T, Vargas H, Merkel J, Jiménez GU, Miller RE, et al. (2005). Assessing the risks of introduced chickens and their pathogens to native birds in the Galápagos Archipelago. Biological Conservation 126:429-439.

    Article  Google Scholar 

  • Grigg ME, and Boothroyd JC (2001). Rapid identification of virulent Type I strains of the protozoan pathogen Toxoplasma gondii by PCR-restriction fragment length polymorphism analysis at the B1 gene. Journal of Clinical Microbiology 39:398-400.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Homan WL, Vercammen M, De Braekeleer J, and Verschueren H (2000). Identification of a 200- to 300-fold repetitive 529 bp DNA fragment in Toxoplasma gondii, and its use for diagnostic and quantitative PCR. International Journal for Parasitology 30:69-75.

    Article  CAS  PubMed  Google Scholar 

  • J Craig Venter Institute (2008) Global ocean sampling expedition. www.jvci.org. Accessed on June 5, 2011.

  • Jiménez-Uzcátegui G, Vargas F (2008) Censo del pingüino de Galápagos y Cormorán no volador. Estación Científica Charles Darwin, Puerto Ayora, Santa Cruz, Galapagos, Ecuador.

  • Jones JL, and Dubey JP (2010). Waterborne toxoplasmosis–recent developments. Experimental Parasitology 124:10-25.

    Article  CAS  PubMed  Google Scholar 

  • Kaiser J (2001). Galápagos takes aim at alien invaders. Science 293:590-592.

    Article  CAS  PubMed  Google Scholar 

  • Karanis P, Aldeyarbi H, Mirhashemi M, and Khalil K (2013). The impact of the waterborne transmission of Toxoplasma gondii and analysis efforts for water detection: an overview and update. Environmental Science and Pollution Research 20:86-99.

    Article  PubMed  Google Scholar 

  • Konecny MJ (1987). Food habits and energetics of feral house cats in the Galapagos Islands. Oikos 50:24-32.

    Article  Google Scholar 

  • Kourenti C, and Karanis P (2006). Evaluation and applicability of a purification method coupled with nested PCR for the detection of Toxoplasma oocysts in water. Letters of Applied Microbiology 43:475-481.

    Article  CAS  Google Scholar 

  • Kreuder C, Miller MA, Jessup DA, Lowenstine LJ, Harris MD, Ames JA, et al. (2003). Patterns of mortality in southern sea otters (Enhydra lutris nereis) from 1998-2001. Journal of Wildlife Disease 39:495-509.

    Article  CAS  Google Scholar 

  • Levy JK, Crawford PC, Lappin MR, Dubovi EJ, Levy MG, Alleman R, et al. (2008). Infectious diseases of dogs and cats on Isabela Island, Galapagos. Journal of Veterinary Internal Medicine 22:60-65.

    Article  CAS  PubMed  Google Scholar 

  • Lindquist HD, Bennett JW, Hester JD, Ware MW, Dubey JP, and Everson WV (2003). Autofluorescence of Toxoplasma gondii and related coccidian oocysts. Journal of Parasitology 89:865-867.

    Article  PubMed  Google Scholar 

  • Lindsay D, and Dubey J (2009). Long-term survival of Toxoplasma gondii sporulated oocysts in seawater. Journal of Parasitology 95:1019-1020.

    Article  PubMed  Google Scholar 

  • Liu J, d’Ozouville N (2013) Water contamination in Puerto Ayora: applied interdisciplinary research using Escherichia coli as an indicator bacteria. GNPS, GCREG, CDF, and GC, Puerto Ayora, Santa Cruz, Galapagos, Ecuador.

  • Mason RW, Hartley WJ, and Dubey JP (1991). Lethal toxoplasmosis in a Little penguin (Eudyptula minor) from Tasmania. Journal of Parasitology 77:328.

    Article  CAS  PubMed  Google Scholar 

  • Massie GN, Ware MW, Villegas EN, and Black MW (2010). Uptake and transmission of Toxoplasma gondii oocysts by migratory, filter-feeding fish. Veterinary Parasitology 169:296-303.

    Article  CAS  PubMed  Google Scholar 

  • Miller MA, Gardner IA, Kreuder C, Paradies DM, Worcester KR, Jessup DA, et al. (2002). Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection of southern sea otters (Enhydra lutris nereis). International Journal for Parasitology 32:997-1006.

    Article  CAS  PubMed  Google Scholar 

  • Miller MA, Miller WA, Conrad PA, James ER, Melli AC, Leutenegger CM, et al. (2008). Type X Toxoplasma gondii in a wild mussel and terrestrial carnivores from coastal California: new linkages between terrestrial mammals, runoff and toxoplasmosis of sea otters. International Journal for Parasitology 38:1319-1328.

    Article  CAS  PubMed  Google Scholar 

  • Moulin L, Richard F, Stefania S, Goulet M, Gosselin S, Gonçalves A, et al. (2010). Contribution of treated wastewater to the microbiological quality of Seine River in Paris. Water Research 44:5222-5231.

    Article  CAS  PubMed  Google Scholar 

  • Nims BD, Vargas FH, Merkel J, and Parker PG (2008). Low genetic diversity and lack of population structure in the endangered Galapagos penguin (Spheniscus mendiculus). Conservation Genetics 9:1413-1420.

    Article  Google Scholar 

  • Nogales M, MartÍN A, Tershy BR, Donlan CJ, Veitch D, Puerta N, et al. (2004). A Review of Feral Cat Eradication on Islands. Conservation Biology 18:310-319.

    Article  Google Scholar 

  • Pryet A, d’Ozouville N, Violette S, Deffontaines B, and Auken E (2012). Hydrological settings of a volcanic island (San Cristobal, Galapagos) from joint interpretation of airborne electromagnetics and geomorphological observations. Hydrology and Earth System Science 16:4571-4579.

    Article  Google Scholar 

  • Reid A, Lymbery A, Ng J, Tweedle S, and Ryan U (2010). Identification of novel and zoonotic Cryptosporidium species in marine fish. Veterinary Parasitology 168:190-195.

    Article  CAS  PubMed  Google Scholar 

  • Rejmanek D, VanWormer E, Miller M, Mazet J, Nichelason A, Melli AC, et al. (2009). Prevalence and risk factors associated with Sarcocystis neurona infections in opossums (Didelphis virginiana) from central California. Veterinary Parasitology 3:8-14.

    Article  Google Scholar 

  • Rengifo-Herrera C, Ortega-Mora LM, Gómez-Bautista M, García-Peña FJ, García-Párraga D, and Pedraza-Díaz S (2013). Detection of a novel genotype of Cryptosporidium in Antarctic pinnipeds. Veterinary Parasitology 191:112-118.

    Article  CAS  PubMed  Google Scholar 

  • Shapiro K, Largier J, Mazet JA, Bernt W, Ell JR, Melli AC, et al. (2009). Surface properties of Toxoplasma gondii oocysts and surrogate microspheres. Applied Environmental Microbiology 75:1185-1191.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shapiro K, Mazet JA, Schriewer A, Wuertz S, Fritz H, Miller WA, et al. (2010). Detection of Toxoplasma gondii oocysts and surrogate microspheres in water using ultrafiltration and capsule filtration. Water Research 44:893-903.

    Article  CAS  PubMed  Google Scholar 

  • Snell H, Tye A, Causton C, Bensted-Smith R (2002) Current status of and threats to the terrestrial biodiversity of Galapagos. In: A biodiversity vision for the Galapagos Islands. Charles Darwin Foundation and World Wildlife Fund, Puerto Ayora, Santa Cruz, Galapagos, Ecuador, pp 30–47.

  • Sotiriadou I, and Karanis P (2008). Evaluation of loop-mediated isothermal amplification for detection of Toxoplasma gondii in water samples and comparative findings by polymerase chain reaction and immunofluorescence test (IFT). Diagnostic Microbiology and Infectious Disease 62:357-365.

    Article  CAS  PubMed  Google Scholar 

  • Trueman M, and d’Ozouville N (2010). Characterizing the Galapagos terrestrial climate in the face of global climate change. Galapagos Research 67:26-37.

    Google Scholar 

  • VanWormer E, Conrad PA, Miller MA, Melli AC, Carpenter TE, Mazet J (2013) Toxoplasma gondii, source to sea: higher contribution of domestic felids to terrestrial parastie loading despite lower infection prevalence. EcoHealth. doi:10.1007/s10393-013-0859-x

    Google Scholar 

  • Vargas F, Harrison S, Rea S, and Macdonald D (2006). Biological effects of El Niño on the Galápagos penguin. Biological Conservation 127:107-114.

    Article  Google Scholar 

  • Vargas F, and Wiedenfeld D (2004). Summary report: 2004 penguin and cormorant survey. Oxford University and Charles Darwin Foundation, Oxford, UK.

    Google Scholar 

  • Violette S, d’Ozouville N, Deffontaines B, Pryet A, Fortin J, Adelinet M (2013). Hydrogeology of the Galapagos Archipelago: an integrated and comparative approach between islands. In: Galapagos Islands: a natural laboratory for Earth Sciences. AGU Chapman Monograph Series

  • Wallace GD, Marshall L, and Marshall M (1972). Cats, rats, and toxoplasmosis on a small Pacific island. American Journal of Epidemiology 95:475-482.

    CAS  PubMed  Google Scholar 

  • Watkins G, Cruz F (2007) Galapagos at risk: a socioeconomic analysis of the situation in the archipelago. Charles Darwin Foundation, Puerto Ayora, Santa Cruz, Galapagos, Ecuador

  • Work TM, Massey JG, Lindsay D, and Dubey JP (2002). Toxoplasmosis in three species of native and introduced Hawaiian birds. Journal of Parasitology 88:1040-1042.

    Article  PubMed  Google Scholar 

  • Work TM, Massey JG, Rideout BA, Gardiner CH, Ledig DB, Kwok OC, et al. (2000). Fatal toxoplasmosis in free-ranging endangered ‘Alala from Hawaii. Journal of Wildlife Disease 36:205-212.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Thank you to the Saint Louis Zoo WildCare Center for Avian Health in the Galápagos Islands and the Charles Darwin Foundation for sponsorship of this project. Laboratory space, permit arrangements, and field assistance were provided by the Charles Darwin Foundation and the Galápagos National Park Directorate. This study was supported by the Morris Animal Foundation and the St. Louis Zoo’s Field Research for Conservation program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michelle L. Verant.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Verant, M.L., d’Ozouville, N., Parker, P.G. et al. Attempted Detection of Toxoplasma gondii Oocysts in Environmental Waters Using a Simple Approach to Evaluate the Potential for Waterborne Transmission in the Galápagos Islands, Ecuador. EcoHealth 11, 207–214 (2014). https://doi.org/10.1007/s10393-013-0888-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-013-0888-5

Keywords

Navigation