The effects of Toxoplasma gondii on New Zealand wildlife: implications for conservation and management
Jim O. Roberts
A D , Hannah F. E. Jones B and Wendi D. Roe C
+ Author Affiliations
- Author Affiliations
A Anemone, Wellington, New Zealand.
B Waikato Regional Council, Hamilton, New Zealand.
C School of Veterinary Science, Massey University, Palmerston North, New Zealand.
D Corresponding author. Email: jimoroberts@gmail.com
Pacific Conservation Biology - https://doi.org/10.1071/PC20051
Submitted: 4 June 2020 Accepted: 26 October 2020 Published online: 1 December 2020
Abstract
Toxoplasma gondii is a globally widespread protozoan parasite that can infect all bird and mammal species. Cat species (Felidae) are the only known definitive host for T. gondii and this parasite should have been absent from New Zealand prior to the introduction of the domestic cat (Felis catus) in the 18th Century. Clinical toxoplasmosis has recently been reported in multiple wild-living New Zealand native species, including: Hector’s and Māui dolphins (Cephalorhynchus hectori hectori and Cephalorhynchus hectori maui, respectively), kākā (Nestor meridionalis), red-crowned kākāriki (Cyanoramphus novaezelandiae), kererū (Hemiphaga novaeseelandiae) and several kiwi species (Apteryx spp.). However, the prevalence of T. gondii infection and associated disease are unknown for most New Zealand native species, and the wider conservation risks of T. gondii remain poorly understood. The preliminary evidence suggests that fatal toxoplasmosis may be more frequent in Hector’s and Māui dolphins relative to other native cetaceans and avifauna that have been assessed for infection. This review summarises the research on the effects of T. gondii on New Zealand wildlife, identifies potential options for managing conservation risks, and outlines critical knowledge gaps.
Keywords: cat management, feral cats, freshwater management, oocyst, stray cats, Toxoplasma gondii, toxoplasmosis.
References
Afonso, E., Thulliez, P., and Gilot-Fromont, E. (2006). Transmission of Toxoplasma gondii in an urban population of domestic cats (Felis catus). International Journal for Parasitology 36, 1373–1382.| Transmission of Toxoplasma gondii in an urban population of domestic cats (Felis catus).Crossref | GoogleScholarGoogle Scholar | 16989836PubMed |
Afonso, E., Thulliez, P., Pontier, D., and Gilot-Fromont, E. (2007). Toxoplasmosis in prey species and consequences for prevalence in feral cats: not all prey species are equal. Parasitology 134, 1963–1971.
| Toxoplasmosis in prey species and consequences for prevalence in feral cats: not all prey species are equal.Crossref | GoogleScholarGoogle Scholar | 17672925PubMed |
Aghaeepour, N., Ganio, E. A., Mcilwain, D., Tsai, A. S., Tingle, M., Van gassen, S., Gaudilliere, D. K., Baca, Q., McNeil, L., Okada, R., Ghaemi, M. S., Furman, D., Wong, R. J., Winn, V. D., Druzin, M. L., El-Sayed, Y. Y., Quaintance, C., Gibbs, R., Darmstadt, G. L., Shaw, G. M., Stevenson, D. K., Tibshirani, R., Nolan, G. P., Lewis, D. B., Angst, M. S., and Gaudilliere, B. (2017). An immune clock of human pregnancy. Science Immunology 2, eaan2946.
| An immune clock of human pregnancy.Crossref | GoogleScholarGoogle Scholar | 28864494PubMed |
Aguilar, G. D., and Farnworth, M. J. (2012). Stray cats in Auckland, New Zealand: discovering geographic information for exploratory spatial analysis. Applied Geography 34, 230–238.
| Stray cats in Auckland, New Zealand: discovering geographic information for exploratory spatial analysis.Crossref | GoogleScholarGoogle Scholar |
Aguilar, G. D., Farnworth, M. J., and Winder, L. (2015). Mapping the stray domestic cat (Felis catus) population in New Zealand: species distribution modelling with a climate change scenario and implications for protected areas. Applied Geography 63, 146–154.
| Mapping the stray domestic cat (Felis catus) population in New Zealand: species distribution modelling with a climate change scenario and implications for protected areas.Crossref | GoogleScholarGoogle Scholar |
Aguirre, A. A., Longcore, T., Barbieri, M., Dabritz, H., Hill, D., Klein, P. N., Lepczyk, C., Lilly, E. L., McLeod, R., Milcarsky, J., Murphy, C. E., Su, C., VanWormer, E., Yolken, R., and Sizemore, G. C. (2019). The One Health approach to toxoplasmosis: epidemiology, control, and prevention strategies. EcoHealth 16, 378–390.
| The One Health approach to toxoplasmosis: epidemiology, control, and prevention strategies.Crossref | GoogleScholarGoogle Scholar | 30945159PubMed |
Arkush, K. D., Miller, M. A., Leutenegger, C. M., Gardner, I. A., Packham, A. E., Heckeroth, A. R., Tenter, A. M., Barr, B. C., and Conrad, P. A. (2003). Molecular and bioassay-based detection of Toxoplasma gondii oocyst uptake by mussels (Mytilus galloprovincialis). International Journal for Parasitology 33, 1087–1097.
| Molecular and bioassay-based detection of Toxoplasma gondii oocyst uptake by mussels (Mytilus galloprovincialis).Crossref | GoogleScholarGoogle Scholar | 13129531PubMed |
Bahia-Oliveira, L., Gomez-Marin, J., and Shapiro, K. (2017). Toxoplasma gondii. In ‘Global Water Pathogen Project’. (Eds J. B. Rose and B. Jimenez-Cisneros.) Part 3 Protists. (UNESCO: Michigan State University.) Available at http://www.waterpathogens.org/book/toxoplasma-gondii [Accessed 3 November 2020].
Baker, C. S., Boren, L., Childerhouse, S., van Helden, A., Lundquist, D., Rayment, W., and Rolfe, J. R. (2019). Conservation status of New Zealand marine mammals, 2019. New Zealand Threat Classification Series No. 29. Department of Conservation, Wellington.
Baldock, F., Alexander, L., and More, S. (2003). Estimated and predicted changes in the cat population of Australian households from 1979 to 2005. Australian Veterinary Journal 81, 289–292.
| Estimated and predicted changes in the cat population of Australian households from 1979 to 2005.Crossref | GoogleScholarGoogle Scholar | 15084040PubMed |
Bobić, B., Sibalić, D., and Djurković-Djaković, O. (1991). High levels of IgM antibodies specific for Toxoplasma gondii in pregnancy 12 years after primary toxoplasma infection. Case report. Gynecologic and Obstetric Investigation 31, 182–184.
| High levels of IgM antibodies specific for Toxoplasma gondii in pregnancy 12 years after primary toxoplasma infection. Case report.Crossref | GoogleScholarGoogle Scholar | 2071060PubMed |
Bowie, W. R., King, A. S., Werker, D. H., Isaac-Renton, J. L., Bell, A., Eng, S. B., and Marion, S. A. (1997). Outbreak of toxoplasmosis associated with municipal drinking water. The BC Toxoplasma Investigation Team. Lancet 350, 173–177.
| Outbreak of toxoplasmosis associated with municipal drinking water. The BC Toxoplasma Investigation Team.Crossref | GoogleScholarGoogle Scholar | 9250185PubMed |
Bräger, S. H.-J. (1998). Behavioural ecology and population structure of Hector’s dolphin (Cephalorhynchus hectori). Ph.D. Thesis, University of Otago, Dunedin. Available at https://ourarchive.otago.ac.nz/handle/10523/3507 [Accessed 19 February 2020].
Carlson-Bremer, D., Colegrove, K. M., Gulland, F. M. D., Conrad, P. A., Mazet, J. A. K., and Johnson, C. K. (2015). Epidemiology and pathology of Toxoplasma gondii in free-ranging California sea lions (Zalophus californianus). Journal of Wildlife Diseases 51, 362–373.
| Epidemiology and pathology of Toxoplasma gondii in free-ranging California sea lions (Zalophus californianus).Crossref | GoogleScholarGoogle Scholar | 25588007PubMed |
Carme, B., Demar, M., Ajzenberg, D., and Dardé, M. L. (2009). Severe acquired toxoplasmosis caused by wild cycle of Toxoplasma gondii, French Guiana. Emerging Infectious Diseases 15, 656–658.
| Severe acquired toxoplasmosis caused by wild cycle of Toxoplasma gondii, French Guiana.Crossref | GoogleScholarGoogle Scholar | 19331765PubMed |
Castillo-Morales, V. J., Acosta viana, K. Y., Guzmán-Marín, E. S., Jiménez-Coello, M., Segura-Correa, J. C., Aguilar-Caballero, A. J., and Ortega-Pacheco, A. (2012). Prevalence and risk factors of Toxoplasma gondii infection in domestic cats from the tropics of Mexico using serological and molecular tests. Interdisciplinary Perspectives on Infectious Diseases 2012, 529108.
| Prevalence and risk factors of Toxoplasma gondii infection in domestic cats from the tropics of Mexico using serological and molecular tests.Crossref | GoogleScholarGoogle Scholar | 22997512PubMed |
CDC (2019 ). Parasites – Toxoplasmosis (Toxoplasma infection). Available at https://www.cdc.gov/parasites/toxoplasmosis/index.html [Accessed 15 December 2019].
Charleston, W. A. G. (1994). Toxoplasma and other protozoan infections of economic importance in New Zealand. New Zealand Journal of Zoology 21, 67–81.
| Toxoplasma and other protozoan infections of economic importance in New Zealand.Crossref | GoogleScholarGoogle Scholar |
Chiang, T.-Y., Kuo, M.-C., Chen, C.-H., Yang, J.-Y., Kao, C.-F., Ji, D.-D., and Fang, C.-T. (2014). Risk factors for acute Toxoplasma gondii diseases in Taiwan: a population-based case-control study. PloS One 9, e90880.
| Risk factors for acute Toxoplasma gondii diseases in Taiwan: a population-based case-control study.Crossref | GoogleScholarGoogle Scholar | 24609112PubMed |
Conrad, P. A., Miller, M. A., Kreuder, C., James, E. R., Mazet, J., Dabritz, H., Jessup, D. A., Gulland, F., and Grigg, M. E. (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.
| Transmission of Toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment.Crossref | GoogleScholarGoogle Scholar | 16157341PubMed |
Coupe, A., Howe, L., Burrows, E., Sine, A., Pita, A., Velathanthiri, N., Vallée, E., Hayman, D., Shapiro, K., and Roe, W. D. (2018). First report of Toxoplasma gondii sporulated oocysts and Giardia duodenalis in commercial green-lipped mussels (Perna canaliculus) in New Zealand. Parasitology Research 117, 1453–1463.
| First report of Toxoplasma gondii sporulated oocysts and Giardia duodenalis in commercial green-lipped mussels (Perna canaliculus) in New Zealand.Crossref | GoogleScholarGoogle Scholar | 29550995PubMed |
Dabritz, H. A., and Conrad, P. A. (2010). Cats and Toxoplasma: implications for public health. Zoonoses and Public Health 57, 34–52.
| Cats and Toxoplasma: implications for public health.Crossref | GoogleScholarGoogle Scholar | 19744306PubMed |
Dabritz, H. A., Miller, M. A., Atwill, E. R., Gardner, I. A., Leutenegger, C. M., Melli, A. C., and Conrad, P. A. (2007). Detection of Toxoplasma gondii-like oocysts in cat feces and estimates of the environmental oocyst burden. Journal of the American Veterinary Medical Association 231, 1676–1684.
| Detection of Toxoplasma gondii-like oocysts in cat feces and estimates of the environmental oocyst burden.Crossref | GoogleScholarGoogle Scholar | 18052801PubMed |
DeFeo, M. L., Dubey, J. P., Mather, T. N., and Rhodes III, R. C. (2002). Epidemiologic investigation of seroprevalence of antibodies to Toxoplasma gondii in cats and rodents. American Journal of Veterinary Research 63, 1714–1717.
| Epidemiologic investigation of seroprevalence of antibodies to Toxoplasma gondii in cats and rodents.Crossref | GoogleScholarGoogle Scholar | 12492287PubMed |
Department of Conservation (2020). Threat management plan for Hector’s and Māui dolphin. Available at https://www.doc.govt.nz/our-work/protecting-species/protecting-marine-species/our-work-with-maui-dolphin/hectors-and-maui-dolphin-threat-management-plan/ [Accessed 26 August 2020].
Dietrich, D., Uhl, B., Sailer, V., Holmes, E. E., Jung, M., Meller, S., and Kristiansen, G. (2013). Improved PCR performance using template DNA from formalin-fixed and paraffin-embedded tissues by overcoming PCR inhibition. PloS One 8, e77771.
Dubey, J. P. (1995). Duration of immunity to shedding of Toxoplasma gondii oocysts by cats. The Journal of Parasitology 81, 410–415.
| 7776126PubMed |
Dubey, J. P. (1976). Reshedding of Toxoplasma oocysts by chronically infected cats. Nature 262, 213–214.
| Reshedding of Toxoplasma oocysts by chronically infected cats.Crossref | GoogleScholarGoogle Scholar | 934336PubMed |
Dubey, J. P. (2004). Toxoplasmosis – a waterborne zoonosis. Veterinary Parasitology 126, 57–72.
| Toxoplasmosis – a waterborne zoonosis.Crossref | GoogleScholarGoogle Scholar | 15567579PubMed |
Dubey, J. P., Lindsay, D. S., and Speer, C. A. (1998). Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clinical Microbiology Reviews 11, 267–299.
| Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts.Crossref | GoogleScholarGoogle Scholar | 9564564PubMed |
Dumètre, A., and Dardé, M. L. (2003). How to detect Toxoplasma gondii oocysts in environmental samples? FEMS Microbiology Reviews 27, 651–661.
| How to detect Toxoplasma gondii oocysts in environmental samples?Crossref | GoogleScholarGoogle Scholar | 14638417PubMed |
Dumètre, A., Le Bras, C., Baffet, M., Meneceur, P., Dubey, J. P., Derouin, F., Duguet, J.-P., Joyeux, M., and Moulin, L. (2008). Effects of ozone and ultraviolet radiation treatments on the infectivity of Toxoplasma gondii oocysts. Veterinary Parasitology 153, 209–213.
| Effects of ozone and ultraviolet radiation treatments on the infectivity of Toxoplasma gondii oocysts.Crossref | GoogleScholarGoogle Scholar | 18355965PubMed |
Elmore, S. A., Huyvaert, K. P., Bailey, L. L., Milhous, J., Alisauskas, R. T., Gajadhar, A. A., and Jenkins, E. J. (2014). Toxoplasma gondii exposure in arctic-nesting geese: a multi-state occupancy framework and comparison of serological assays. International Journal for Parasitology: Parasites and Wildlife 3, 147–153.
| Toxoplasma gondii exposure in arctic-nesting geese: a multi-state occupancy framework and comparison of serological assays.Crossref | GoogleScholarGoogle Scholar | 25161913PubMed |
Elmore, S. A., Samelius, G., Fernando, C., Alisauskas, R. T., and Jenkins, E. J. (2015). Evidence for Toxoplasma gondii in migratory vs. nonmigratory herbivores in a terrestrial arctic ecosystem. Canadian Journal of Zoology 93, 671–675.
| Evidence for Toxoplasma gondii in migratory vs. nonmigratory herbivores in a terrestrial arctic ecosystem.Crossref | GoogleScholarGoogle Scholar |
Fancourt, B. A., and Jackson, R. B. (2014). Regional seroprevalence of Toxoplasma gondii antibodies in feral and stray cats (Felis catus) from Tasmania. Australian Journal of Zoology 62, 272–283.
| Regional seroprevalence of Toxoplasma gondii antibodies in feral and stray cats (Felis catus) from Tasmania.Crossref | GoogleScholarGoogle Scholar |
Fancourt, B. A., Nicol, S. C., Hawkins, C. E., Jones, M. E., and Johnson, C. N. (2014). Beyond the disease: is Toxoplasma gondii infection causing population declines in the eastern quoll (Dasyurus viverrinus)? International Journal for Parasitology: Parasites and Wildlife 3, 102–112.
| Beyond the disease: is Toxoplasma gondii infection causing population declines in the eastern quoll (Dasyurus viverrinus)?Crossref | GoogleScholarGoogle Scholar | 25161908PubMed |
Farnworth, M. J., Campbell, J., and Adams, N. J. (2011). What’s in a name? Perceptions of stray and feral cat welfare and control in Aotearoa, New Zealand. Journal of Applied Animal Welfare Science 14, 59–74.
| What’s in a name? Perceptions of stray and feral cat welfare and control in Aotearoa, New Zealand.Crossref | GoogleScholarGoogle Scholar | 21191848PubMed |
Farnworth, M., Campbell, J., and Adams, N. (2010). Public awareness in New Zealand of animal welfare legislation relating to cats. New Zealand Veterinary Journal 58, 213–217.
| Public awareness in New Zealand of animal welfare legislation relating to cats.Crossref | GoogleScholarGoogle Scholar | 20676160PubMed |
Fitzgerald, A. M., and Karl, B. J. (1979). Foods of feral house cats (Felis catus L.) in forest of the Orongorongo Valley, Wellington. New Zealand Journal of Zoology 6, 107–126.
| Foods of feral house cats (Felis catus L.) in forest of the Orongorongo Valley, Wellington.Crossref | GoogleScholarGoogle Scholar |
Ferrer, I., Armstrong, J., Capellari, S., Parchi, P., Arzberger, T., Bell, J., et al. (2007). Effects of formalin fixation, paraffin embedding, and time of storage on DNA preservation in brain tissue: a BrainNet Europe study. Brain Pathology 17, 297–303.
Frenkel, J. K., Pfefferkorn, E. R., Smith, D. D., and Fishback, J. L. (1991). Prospective vaccine prepared from a new mutant of Toxoplasma gondii for use in cats. American Journal of Veterinary Research 52, 759–763.
| 1854103PubMed |
Galloway, T., and Handy, R. (2003). Immunotoxicity of organophosphorous pesticides. Ecotoxicology 12, 345–363.
| Immunotoxicity of organophosphorous pesticides.Crossref | GoogleScholarGoogle Scholar | 12739880PubMed |
Gartrell, B., Agnew, D., Alley, M., Carpenter, T., Ha, H. J., Howe, L., Hunter, S., McInnes, K., Munday, R., Roe, W., and Young, M. (2017). Investigation of a mortality cluster in wild adult yellow-eyed penguins (Megadyptes antipodes) at Otago Peninsula, New Zealand. Avian Pathology 46, 278–288.
| Investigation of a mortality cluster in wild adult yellow-eyed penguins (Megadyptes antipodes) at Otago Peninsula, New Zealand.Crossref | GoogleScholarGoogle Scholar | 27919180PubMed |
Gillies, C., and Fitzgerald, B. M. (2005). Feral cat. In ‘The Handbook of New Zealand Mammals’. (Ed. C. M. King.) pp. 308–327. (Oxford University Press: Auckland, New Zealand.)
Hall, C. M., Adams, N. A., Bradley, J. S., Bryant, K. A., Davis, A. A., Dickman, C. R., Fujita, T., Kobayashi, S., Lepczyk, C. A., McBride, E. A., Pollock, K. H., Styles, I. M., van Heezik, Y., Wang, F., and Calver, M. C. (2016). Community attitudes and practices of urban residents regarding predation by pet cats on wildlife: an international comparison. PLoS One 11, .
| Community attitudes and practices of urban residents regarding predation by pet cats on wildlife: an international comparison.Crossref | GoogleScholarGoogle Scholar | 27050447PubMed |
Hanley, P., and Bollard, C. (2014). Controlling cytomegalovirus: helping the immune system take the lead. Viruses 6, 2242–2258.
| Controlling cytomegalovirus: helping the immune system take the lead.Crossref | GoogleScholarGoogle Scholar | 24872114PubMed |
Harper, G. (2010). Diet of feral cats on subantarctic Auckland Island. New Zealand Journal of Ecology 34, 259–261.
Hartley, W. J., and Boyes, B. W. (1964). Incidence of ovine perinatal mortality in New Zealand with particular reference to intrauterine infections. New Zealand Veterinary Journal 12, 33–36.
| Incidence of ovine perinatal mortality in New Zealand with particular reference to intrauterine infections.Crossref | GoogleScholarGoogle Scholar |
Hartley, W. J., and Marshall, S. C. (1957). Toxoplasmosis as a cause of ovine perinatal mortality. New Zealand Veterinary Journal 5, 119–124.
| Toxoplasmosis as a cause of ovine perinatal mortality.Crossref | GoogleScholarGoogle Scholar |
Hill, D. E., and Dubey, J. P. (2014). Toxoplasmosis. US Geological Survey Circular 1389. Reston, VA
Hillman, A. E., Lymbery, A. J., and Thompson, R. C. A. (2016). Is Toxoplasma gondii a threat to the conservation of free-ranging Australian marsupial populations? International Journal for Parasitology: Parasites and Wildlife 5, 17–27.
| Is Toxoplasma gondii a threat to the conservation of free-ranging Australian marsupial populations?Crossref | GoogleScholarGoogle Scholar | 27141439PubMed |
Hogan, J. N., Daniels, M. E., Watson, F. G., Oates, S. C., Miller, M. A., Conrad, P. A., Shapiro, K., Hardin, D., Dominik, C., Melli, A., Jessup, D. A., and Miller, W. A. (2013). Hydrologic and vegetative removal of Cryptosporidium parvum, Giardia lamblia, and Toxoplasma gondii surrogate microspheres in coastal wetlands. Applied and Environmental Microbiology 79, 1859–1865.
| Hydrologic and vegetative removal of Cryptosporidium parvum, Giardia lamblia, and Toxoplasma gondii surrogate microspheres in coastal wetlands.Crossref | GoogleScholarGoogle Scholar | 23315738PubMed |
Howe, L., Hunter, S., Burrows, E., and Roe, W. (2014). Four cases of fatal toxoplasmosis in three species of endemic New Zealand birds. Avian Diseases 58, 171–175.
| Four cases of fatal toxoplasmosis in three species of endemic New Zealand birds.Crossref | GoogleScholarGoogle Scholar | 24758132PubMed |
Hunter, R. (1986). Project Report HR 005 – To determine the prevalence of toxoplasma titres in a Waikato goat population. Surveillance 13, 11.
Hunter, S., and Alley, M. (2014). Toxoplasmosis in wild birds in New Zealand. Kokako 21, 58–59.
Jensen, S. K., Aars, J., Lydersen, C., Kovacs, K. M., and Åsbakk, K. (2010). The prevalence of Toxoplasma gondii in polar bears and their marine mammal prey: evidence for a marine transmission pathway? Polar Biology 33, 599–606.
| The prevalence of Toxoplasma gondii in polar bears and their marine mammal prey: evidence for a marine transmission pathway?Crossref | GoogleScholarGoogle Scholar |
Jones, J. L., Dargelas, V., Roberts, J., Press, C., Remington, J. S., and Montoya, J. G. (2009). Risk factors for Toxoplasma gondii infection in the United States. Clinical Infectious Diseases 49, 878–84.
| Risk factors for Toxoplasma gondii infection in the United States.Crossref | GoogleScholarGoogle Scholar | 19663709PubMed |
Jones, J. L., and Dubey, J. P. (2010). Waterborne toxoplasmosis – recent developments. Experimental Parasitology 124, 10–25.
| Waterborne toxoplasmosis – recent developments.Crossref | GoogleScholarGoogle Scholar | 19324041PubMed |
Jones, J. L., Kruszon-Moran, D., Rivera, H., Price, C., and Wilkins, P. (2014). Toxoplasma gondii seroprevalence in the United States 2009–2010 and comparison with the past two decades American Journal of Tropical Medicine and Hygiene 90, 1135–1139.
| 24710615PubMed |
Kang, Y.-H., Cong, W., Qin, S.-Y., Shan, X.-F., Gao, Y.-H., Wang, C.-F., and Qian, A.-D. (2016). First report of Toxoplasma gondii, Dirofilaria immitis, and Chlamydia felis infection in stray and companion cats in northeastern and eastern China. Vector-Borne and Zoonotic Diseases 16, 654–658.
| First report of Toxoplasma gondii, Dirofilaria immitis, and Chlamydia felis infection in stray and companion cats in northeastern and eastern China.Crossref | GoogleScholarGoogle Scholar | 27463689PubMed |
Karanis, P., Aldeyarbi, H. M., Mirhashemi, M. E., and Khalil, K. M. (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 International 20, 86–99.
| The impact of the waterborne transmission of Toxoplasma gondii and analysis efforts for water detection: an overview and update.Crossref | GoogleScholarGoogle Scholar | 22990578PubMed |
Kikillus, K. H., Chambers, G. K., Farnworth, M. J., and Hare, K. M. (2017). Research challenges and conservation implications for urban cat management in New Zealand. Pacific Conservation Biology 23, 15–24.
| Research challenges and conservation implications for urban cat management in New Zealand.Crossref | GoogleScholarGoogle Scholar |
Klasing, K. C. (1998). Nutritional modulation of resistance to infectious diseases. Poultry Science 77, 1119–1125.
| Nutritional modulation of resistance to infectious diseases.Crossref | GoogleScholarGoogle Scholar | 9706075PubMed |
Lindsay, D. S., Collins, M. V., Mitchell, S. M., Cole, R. A., Flick, G. J., Wetch, C. N., Lindquist, A., and Dubey, J. P. (2003). Sporulation and survival of Toxoplasma gondii oocysts in seawater. The Journal of Eukaryotic Microbiology 50 Suppl, 687–688.
| Sporulation and survival of Toxoplasma gondii oocysts in seawater.Crossref | GoogleScholarGoogle Scholar | 14736220PubMed |
Lindsay, D. S., Collins, M. V., Mitchell, S. M., Wetch, C. N., Rosypal, A. C., Flick, G. J., Zajac, A. M., Lindquist, A., and Dubey, J. P. (2004). Survival of Toxoplasma gondii oocysts eastern oysters (Crassostrea virginica). Journal of Parasitology 90, 1054–1057.
| Survival of Toxoplasma gondii oocysts eastern oysters (Crassostrea virginica).Crossref | GoogleScholarGoogle Scholar | 15562605PubMed |
Lindsay, D. S., and Dubey, J. P. (2009). Long-term survival of Toxoplasma gondii sporulated oocysts in seawater. Journal of Parasitology 95, 1019–1020.
| Long-term survival of Toxoplasma gondii sporulated oocysts in seawater.Crossref | GoogleScholarGoogle Scholar | 20050010PubMed |
Linklater, W. L., Farnworth, M. J., Heezik, Y., Stafford, K. J., and MacDonald, E. A. (2019). Prioritising cat-owner behaviours for a campaign to reduce wildlife depredation. Conservation Science and Practice 1, e29.
| Prioritising cat-owner behaviours for a campaign to reduce wildlife depredation.Crossref | GoogleScholarGoogle Scholar |
Lynch, M., Nielsen, O., Duignan, P.J., Kirkwood, R., Hoskins, A., and Arnould, J. P. (2011). Serologic survey for potential pathogens and assessment of disease risk in Australian fur seals. Journal of Wildlife Diseases 47, 555–565.
Mahlow, J. C., and Slater, M. R. (1996). Current issues in the control of stray and feral cats. Journal of the American Veterinary Medical Association 209, 2016–2020.
| 8960173PubMed |
Massie, G. N., Ware, M. W., Villegas, E. N., and Black, M. W. (2010). Uptake and transmission of Toxoplasma gondii oocysts by migratory, filter-feeding fish. Veterinary Parasitology 169, 296–303.
| Uptake and transmission of Toxoplasma gondii oocysts by migratory, filter-feeding fish.Crossref | GoogleScholarGoogle Scholar | 20097009PubMed |
Mazzillo, F. F. M., Shapiro, K., and Silver, M. W. (2013). A new pathogen transmission mechanism in the ocean: the case of sea otter exposure to the land-parasite Toxoplasma gondii. PloS One 8, e82477.
| A new pathogen transmission mechanism in the ocean: the case of sea otter exposure to the land-parasite Toxoplasma gondii.Crossref | GoogleScholarGoogle Scholar |
McKenna, P. B. (1978). Coccidia (Protozoa: Sporozoasida) of cats and dogs. M.Phil. Thesis, Massey University Palmerston North, New Zealand.
McKenna, P. B. (1998). Special issue: Parasites of birds in New Zealand – checklist of helminth and protozoan parasites – Part II: Parasite list by parasite. Surveillance 25, 26–31.
McKenna, P. B., and Charleston, W. A. G. (1980). Coccidia (Protozoa: Sporozoasida) of cats and dogs. I. Identity and prevalence in cats. New Zealand Veterinary Journal 28, 86–88.
| Coccidia (Protozoa: Sporozoasida) of cats and dogs. I. Identity and prevalence in cats.Crossref | GoogleScholarGoogle Scholar | 6776453PubMed |
McLeod, L., Driver, A., Bengsen, A. J., and Hine, D. W. (2017). Refining online communication strategies for domestic cat management. Available at https://rune.une.edu.au/web/handle/1959.11/22292 [Accessed 13 February 2020]
Michael, S., Howe, L., Chilvers, B., Morel, P., and Roe, W. (2016). Seroprevalence of Toxoplasma gondii in mainland and sub-Antarctic New Zealand sea lion (Phocarctos hookeri) populations. New Zealand Veterinary Journal 64, 293–297.
| Seroprevalence of Toxoplasma gondii in mainland and sub-Antarctic New Zealand sea lion (Phocarctos hookeri) populations.Crossref | GoogleScholarGoogle Scholar | 27211206PubMed |
Ming, J. E., Stiehm, E. R., and Graham, Jr., J. M. (2003). Syndromic immunodeficiencies: genetic syndromes associated with immune abnormalities. Critical Reviews in Clinical Laboratory Sciences 40, 587–642.
| Syndromic immunodeficiencies: genetic syndromes associated with immune abnormalities.Crossref | GoogleScholarGoogle Scholar | 14708957PubMed |
Mirza, V., Burrows, E. B., Gils, S., Hunter, S., Gartrell, B. D., and Howe, L. (2017). A retrospective survey into the presence of Plasmodium spp. and Toxoplasma gondii in archived tissue samples from New Zealand raptors: New Zealand falcons (Falco novaeseelandiae), Australasian harriers (Circus approximans) and moreporks (Ninox novaeseelandiae). Parasitology Research 116, 2283–2289.
| A retrospective survey into the presence of Plasmodium spp. and Toxoplasma gondii in archived tissue samples from New Zealand raptors: New Zealand falcons (Falco novaeseelandiae), Australasian harriers (Circus approximans) and moreporks (Ninox novaeseelandiae).Crossref | GoogleScholarGoogle Scholar | 28660290PubMed |
Montoya, J., and Liesenfeld, O. (2004). Toxoplasmosis. The Lancet 363, 1965–1976.
| Toxoplasmosis.Crossref | GoogleScholarGoogle Scholar |
Moor, C., Stone, P., Purdie, G., and Weinstein, P. (2000). An investigation into the incidence of toxoplasmosis in pregnancy in New Zealand. The New Zealand Medical Journal 113, 29–32.
| 11482326PubMed |
de Moura, L., Bahia-Oliveira, L. M. G., Wada, M. Y., Jones, J. L., Tuboi, S. H., Carmo, E. H., Ramalho, W. M., Camargo, N. J., Trevisan, R., Graça, R. M. T., da Silva, A. J., Moura, I., Dubey, J. P., and Garrett, D. O. (2006). Waterborne toxoplasmosis, Brazil, from field to gene. Emerging Infectious Diseases 12, 326–329.
| Waterborne toxoplasmosis, Brazil, from field to gene.Crossref | GoogleScholarGoogle Scholar | 16494765PubMed |
MPI (2015). Risk profile update: Toxoplasma gondii in red meat and meat products. Ministry for Primary Industries Technical Paper No. 2015/08. Wellington, New Zealand. Available at https://www.mpi.govt.nz/dmsdocument/7266/send
Murphy, E. C., Keedwell, R. J., Brown, K. P., and Westbrooke, I. (2004). Diet of mammalian predators in braided river beds in the central South Island, New Zealand. Wildlife Research 31, 631–638.
| Diet of mammalian predators in braided river beds in the central South Island, New Zealand.Crossref | GoogleScholarGoogle Scholar |
Murray, J. K., Browne, W. J., Roberts, M. A., Whitmarsh, A., and Gruffydd-Jones, T. J. (2010). Number and ownership profiles of cats and dogs in the UK. The Veterinary Record 166, 163–168.
| Number and ownership profiles of cats and dogs in the UK.Crossref | GoogleScholarGoogle Scholar | 20139379PubMed |
Ngô, H. M., Zhou, Y., Lorenzi, H., Wang, K., Kim, T.-K., Zhou, Y., El Bissati, K., Mui, E., Fraczek, L., Rajagopala, S. V., Roberts, C. W., Henriquez, F. L., Montpetit, A., Blackwell, J. M., Jamieson, S. E., Wheeler, K., Begeman, I. J., Naranjo-Galvis, C., Alliey-Rodriguez, N., Davis, R. G., Soroceanu, L., Cobbs, C., Steindler, D. A., Boyer, K., Noble, A. G., Swisher, C. N., Heydemann, P. T., Rabiah, P., Withers, S., Soteropoulos, P., Hood, L., and McLeod, R. (2017). Toxoplasma modulates signature pathways of human epilepsy, neurodegeneration and cancer. Scientific Reports 7, 11496.
| Toxoplasma modulates signature pathways of human epilepsy, neurodegeneration and cancer.Crossref | GoogleScholarGoogle Scholar | 28904337PubMed |
NZCAC (2016). Companion animals in New Zealand 2016. New Zealand Companion Animal Council, Auckland. Available at https://www.nzvna.org.nz/site/nzvna/files/Documents/Companion%20Animals_in_New_Zealand_2016_Report_web.pdf
NZCMS (2017). New Zealand national cat management strategy discussion paper. New Zealand Cat Management Strategy Group. Available at http://www.nzcac.org.nz/images/downloads/nz-national-cat-management-strategy-discussion-paper.pdf
NZFSA (2010). Toxoplasma gondii. New Zealand Food Safety Authority. Available at https://www.mpi.govt.nz/dmsdocument/11054-toxoplasma-gondii-microbial-pathogen-data-sheet [Accessed 3 February 2020]
NZVA (2013). A systematic review of the impacts of feral, stray and companion domestic cats (Felis catus) on wildlife in New Zealand and options for their management. New Zealand Veterinary Association. Available at https://www.epi-interactive.com/sites/default/files/documents/NZVA%20Report%20Cat%20Predation.pdf [Accessed 3 November 2020]
Opsteegh, M., Haveman, R., Swart, A. N., Mensink-Beerepoot, M. E., Hofhuis, A., Langelaar, M. F. M., and van der Giessen, J. W. B. (2012). Seroprevalence and risk factors for Toxoplasma gondii infection in domestic cats in The Netherlands. Preventive Veterinary Medicine 104, 317–326.
| Seroprevalence and risk factors for Toxoplasma gondii infection in domestic cats in The Netherlands.Crossref | GoogleScholarGoogle Scholar | 22305876PubMed |
Osterhaus, A. D. M. E., and Vedder, E. J. (1988). Identification of virus causing recent seal deaths. Nature 335, 20–20.
| Identification of virus causing recent seal deaths.Crossref | GoogleScholarGoogle Scholar |
Orr, M., and Black, A. (1996). Animal health laboratory network. Review of diagnostic cases – October to December 1995. Surveillance 23, 3–5.
Patel, K. K., Burrows, E., Heuer, C., Asher, G. W., Wilson, P. R., and Howe, L. (2019). Investigation of Toxoplasma gondii and association with early pregnancy and abortion rates in New Zealand farmed red deer (Cervus elaphus). Parasitology Research 118, 2065–2077.
| Investigation of Toxoplasma gondii and association with early pregnancy and abortion rates in New Zealand farmed red deer (Cervus elaphus).Crossref | GoogleScholarGoogle Scholar | 31187222PubMed |
Peterson, M. N., Hartis, B., Rodriguez, S., Green, M., and Lepczyk, C. A. (2012). Opinions from the front lines of cat colony management conflict. PLOS One 7, e44616.
| Opinions from the front lines of cat colony management conflict.Crossref | GoogleScholarGoogle Scholar | 22970269PubMed |
Prestrud, K. W., Åsbakk, K., Fuglei, E., Mørk, T., Stien, A., Ropstad, E., Tryland, M., Gabrielsen, G. W., Lydersen, C., Kovacs, K. M., Loonen, M. J. J. E., Sagerup, K., and Oksanen, A. (2007). Serosurvey for Toxoplasma gondii in Arctic foxes and possible sources of infection in the high Arctic of Svalbard. Veterinary Parasitology 150, 6–12.
| Serosurvey for Toxoplasma gondii in Arctic foxes and possible sources of infection in the high Arctic of Svalbard.Crossref | GoogleScholarGoogle Scholar | 17950534PubMed |
Prusa, A.-R., Kasper, D. C., Sawers, L., Walter, E., Hayde, M., and Stillwaggon, E. (2017). Congenital toxoplasmosis in Austria: prenatal screening for prevention is cost-saving. Plos Neglected Tropical Diseases 11, e0005648.
| Congenital toxoplasmosis in Austria: prenatal screening for prevention is cost-saving.Crossref | GoogleScholarGoogle Scholar | 28692640PubMed |
Ramakrishnan, C., Maier, S., Walker, R. A., Rehrauer, H., Joekel, D. E., Winiger, R. R., Basso, W. U., Grigg, M. E., Hehl, A. B., Deplazes, P., and Smith, N. C. (2019). An experimental genetically attenuated live vaccine to prevent transmission of Toxoplasma gondii by cats. Scientific Reports 9, 1474.
| An experimental genetically attenuated live vaccine to prevent transmission of Toxoplasma gondii by cats.Crossref | GoogleScholarGoogle Scholar | 30728393PubMed |
Reichel, M. P., Timbs, D., Ross, G. P., and Penrose, M. E. (1999). Seroprevalence of Leptospira and Toxoplasma in New Zealand farmed deer. Surveillance 26, 5–6.
Rengifo-Herrera, C., Ortega-Mora, L. M., Álvarez-García, G., Gómez-Bautista, M., García-Párraga, D., García-Peña, F. J., and Pedraza-Díaz, S. (2012). Detection of Toxoplasma gondii antibodies in Antarctic pinnipeds. Veterinary Parasitology 190, 259–262.
| Detection of Toxoplasma gondii antibodies in Antarctic pinnipeds.Crossref | GoogleScholarGoogle Scholar | 22726387PubMed |
Roberts, J. O., Webber, D. N., Roe, W. D., Edwards, C. T. T., and Doonan, I. J. (2019). Spatial risk assessment of threats to Hector’s and Māui dolphins (Cephalorhynchus hectori). New Zealand Aquatic Environment and Biodiversity Report No. 214. Available at https://www.fisheries.govt.nz/dmsdocument/35007/direct [Accessed 3 November 2020]
Roe, W. D., Howe, L., Baker, E. J., Burrows, L., and Hunter, S. A. (2013). An atypical genotype of Toxoplasma gondii as a cause of mortality in Hector’s dolphins (Cephalorhynchus hectori). Veterinary Parasitology 192, 67–74.
| An atypical genotype of Toxoplasma gondii as a cause of mortality in Hector’s dolphins (Cephalorhynchus hectori).Crossref | GoogleScholarGoogle Scholar | 23207018PubMed |
Roe, W., Michael, S., Fyfe, J., Burrows, E., Hunter, S., and Howe, L. (2017). First report of systemic toxoplasmosis in a New Zealand sea lion (Phocarctos hookeri). New Zealand Veterinary Journal 65, 46–50.
| First report of systemic toxoplasmosis in a New Zealand sea lion (Phocarctos hookeri).Crossref | GoogleScholarGoogle Scholar | 27588458PubMed |
Ross, P., DeSwart, R., Addison, R., VanLoveren, H., Vos, J., and Osterhaus, A. (1996). Contaminant-induced immunotoxicity in harbour seals: Wildlife at risk? Toxicology 112, 157–169.
| Contaminant-induced immunotoxicity in harbour seals: Wildlife at risk?Crossref | GoogleScholarGoogle Scholar | 8814345PubMed |
Salmond, A. (1991). ‘Two Worlds: First Meetings between Māori and Europeans, 1642-1772.’ (Penguin Books: New Zealand.) Available at https://natlib.govt.nz/records/22111350 [Accessed 20 December 2019]
Shapiro, K., Bahia-Oliveira, L., Dixon, B., Dumètre, A., de Wit, L. A., VanWormer, E., and Villena, I. (2019). Environmental transmission of Toxoplasma gondii: oocysts in water, soil and food. Food and Waterborne Parasitology 15, e00049.
| Environmental transmission of Toxoplasma gondii: oocysts in water, soil and food.Crossref | GoogleScholarGoogle Scholar | 32095620PubMed |
Shapiro, K., Conrad, P. A., Mazet, J. A. K., Wallender, W. W., Miller, W. A., and Largier, J. L. (2010). Effect of estuarine wetland degradation on transport of Toxoplasma gondii surrogates from land to sea. Applied and Environmental Microbiology 76, 6821–6828.
| Effect of estuarine wetland degradation on transport of Toxoplasma gondii surrogates from land to sea.Crossref | GoogleScholarGoogle Scholar | 20802072PubMed |
Slater, M. R., Di Nardo, A., Pediconi, O., Villa, P. D., Candeloro, L., Alessandrini, B., and Del Papa, S. (2008). Cat and dog ownership and management patterns in central Italy. Preventive Veterinary Medicine 85, 267–294.
| Cat and dog ownership and management patterns in central Italy.Crossref | GoogleScholarGoogle Scholar | 18374434PubMed |
Stockin, K. A., Law, R. J., Roe, W. D., Meynier, L., Martinez, E., Duignan, P. J., Bridgen, P., and Jones, B. (2010). PCBs and organochlorine pesticides in Hector’s (Cephalorhynchus hectori hectori) and Maui’s (Cephalorhynchus hectori maui) dolphins. Marine Pollution Bulletin 60, 834–842.
| PCBs and organochlorine pesticides in Hector’s (Cephalorhynchus hectori hectori) and Maui’s (Cephalorhynchus hectori maui) dolphins.Crossref | GoogleScholarGoogle Scholar | 20226477PubMed |
Suijkerbuijk, A. W. M., van Gils, P. F., Bonačić Marinović, A. A., Feenstra, T. L., Kortbeek, L. M., Mangen, M.-J. J., Opsteegh, M., de Wit, G. A., and van der Giessen, J. W. B. (2018). The design of a social cost–benefit analysis of preventive interventions for toxoplasmosis: an example of the One Health approach. Zoonoses and Public Health 65, 185–194.
| The design of a social cost–benefit analysis of preventive interventions for toxoplasmosis: an example of the One Health approach.Crossref | GoogleScholarGoogle Scholar |
Tenter, A. M., Heckeroth, A. R., and Weiss, L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 1217–1258.
| Toxoplasma gondii: from animals to humans.Crossref | GoogleScholarGoogle Scholar | 11113252PubMed |
Tenter, A. M., Vietmeyer, C., Johnson, A. M., Janitschke, K., Rommel, M., and Lehmacher, W. (1994). ELISAs based on recombinant antigens for seroepidemiological studies on Toxoplasma gondii infections in cats. Parasitology 109, 29–36.
| ELISAs based on recombinant antigens for seroepidemiological studies on Toxoplasma gondii infections in cats.Crossref | GoogleScholarGoogle Scholar | 8058366PubMed |
Tompkins, D. M. (2014). Potential of feral cat control to reduce the incidence of toxoplasmosis on sheep farms. Report Addendum. Landcare Research. Available at https://www.pfhb.nz/assets/Image-Gallery/Tompkins-2014-Potential-of-feral-cat-control-to-reduce-the-incidence-of-toxoplasmosis.pdf [Accessed 3 November 2020]
Toukhsati, S. R., Young, E., Bennett, P. C., and Coleman, G. J. (2012). Wandering cats: attitudes and behaviors towards cat containment in Australia. Anthrozoos 25, 61–74.
| Wandering cats: attitudes and behaviors towards cat containment in Australia.Crossref | GoogleScholarGoogle Scholar |
VanWormer, E., Carpenter, T. E., Singh, P., Shapiro, K., Wallender, W. W., Conrad, P. A., Largier, J. L., Maneta, M. P., and Mazet, J. A. K. (2016). Coastal development and precipitation drive pathogen flow from land to sea: evidence from a Toxoplasma gondii and felid host system. Scientific Reports 6, 29252.
| Coastal development and precipitation drive pathogen flow from land to sea: evidence from a Toxoplasma gondii and felid host system.Crossref | GoogleScholarGoogle Scholar | 27456911PubMed |
VanWormer, E., Conrad, P. A., Miller, M. A., Melli, A. C., Carpenter, T. E., and Mazet, J. A. K. (2013). Toxoplasma gondii, source to sea: higher contribution of domestic felids to terrestrial parasite loading despite lower infection prevalence. Ecohealth 10, 277–289.
| Toxoplasma gondii, source to sea: higher contribution of domestic felids to terrestrial parasite loading despite lower infection prevalence.Crossref | GoogleScholarGoogle Scholar | 24048652PubMed |
Verant, M. L., d’Ozouville, N., Parker, P. G., Shapiro, K., VanWormer, E., and Deem, S. L. (2014). 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.
| 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.Crossref | GoogleScholarGoogle Scholar | 24306552PubMed |
Wainwright, K. E., Lagunas-Solar, M., Miller, M. A., Barr, B. C., Gardner, I. A., Pina, C., Melli, A. C., Packham, A. E., Zeng, N., Truong, T., and Conrad, P. A. (2007a). Physical inactivation of Toxoplasma gondii oocysts in water. Applied and Environmental Microbiology 73, 5663–5666.
| Physical inactivation of Toxoplasma gondii oocysts in water.Crossref | GoogleScholarGoogle Scholar | 17616618PubMed |
Wainwright, K. E., Miller, M. A., Barr, B. C., Gardner, I. A., Melli, A. C., Essert, T., Packham, A. E., Truong, T., Lagunas-Solar, M., and Conrad, P. A. (2007b). Chemical inactivation of Toxoplasma gondii oocysts in water. The Journal of Parasitology 93, 925–931.
| Chemical inactivation of Toxoplasma gondii oocysts in water.Crossref | GoogleScholarGoogle Scholar | 17918377PubMed |
Weiskopf, D., Weinberger, B., and Grubeck-Loebenstein, B. (2009). The aging of the immune system. Transplant International: Official Journal of the European Society for Organ Transplantation 22, 1041–1050.
| The aging of the immune system.Crossref | GoogleScholarGoogle Scholar |
Wilkins, M., and O’Connell, E. (1992). Vaccination of sheep against Toxoplasma abortion. Surveillance 19, 20–23.
Wu, H., Zhang, J., Ngo, H. H., Guo, W., Hu, Z., Liang, S., Fan, J., and Liu, H. (2015). A review on the sustainability of constructed wetlands for wastewater treatment: design and operation. Bioresource Technology 175, 594–601.
| A review on the sustainability of constructed wetlands for wastewater treatment: design and operation.Crossref | GoogleScholarGoogle Scholar | 25453440PubMed |
Zarkovic, A., MacMurray, C., Deva, N., Ghosh, S., Whitley, D., and Guest, S. (2007). Seropositivity rates for Bartonella henselae, Toxocara canis and Toxoplasma gondii in New Zealand blood donors. Clinical & Experimental Ophthalmology 35, 131–134.
| Seropositivity rates for Bartonella henselae, Toxocara canis and Toxoplasma gondii in New Zealand blood donors.Crossref | GoogleScholarGoogle Scholar |
Zedler, J. B., and Kercher, S. (2005). Wetland resources: status, trends, ecosystem services, and restorability. Annual Review of Environment and Resources 30, 39–74.
| Wetland resources: status, trends, ecosystem services, and restorability.Crossref | GoogleScholarGoogle Scholar |
