The effects of Toxoplasma gondii on New Zealand wildlife: implications for conservation and management

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.

[1]  C. Heuer,et al.  Investigation of Toxoplasma gondii and association with early pregnancy and abortion rates in New Zealand farmed red deer (Cervus elaphus) , 2019, Parasitology Research.

[2]  K. Stafford,et al.  Prioritizing cat‐owner behaviors for a campaign to reduce wildlife depredation , 2019, Conservation Science and Practice.

[3]  Christopher A. Lepczyk,et al.  The One Health Approach to Toxoplasmosis: Epidemiology, Control, and Prevention Strategies , 2019, EcoHealth.

[4]  I. Villena,et al.  Environmental transmission of Toxoplasma gondii: Oocysts in water, soil and food , 2019, Food and waterborne parasitology.

[5]  A. Hehl,et al.  An experimental genetically attenuated live vaccine to prevent transmission of Toxoplasma gondii by cats , 2019, Scientific Reports.

[6]  A. Pita,et al.  First report of Toxoplasma gondii sporulated oocysts and Giardia duodenalis in commercial green-lipped mussels (Perna canaliculus) in New Zealand , 2018, Parasitology Research.

[7]  M. Mangen,et al.  The design of a Social Cost‐Benefit Analysis of preventive interventions for toxoplasmosis: An example of the One Health approach , 2018, Zoonoses and public health.

[8]  L. Hood,et al.  Toxoplasma Modulates Signature Pathways of Human Epilepsy, Neurodegeneration & Cancer , 2017, Scientific Reports.

[9]  R. Tibshirani,et al.  An immune clock of human pregnancy , 2017, Science Immunology.

[10]  B. Gartrell,et al.  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) , 2017, Parasitology Research.

[11]  K. Hare,et al.  Research challenges and conservation implications for urban cat management in New Zealand. , 2017 .

[12]  T. Carpenter,et al.  Investigation of a mortality cluster in wild adult yellow-eyed penguins (Megadyptes antipodes) at Otago Peninsula, New Zealand , 2017, Avian pathology : journal of the W.V.P.A.

[13]  J. Fyfe,et al.  First report of systemic toxoplasmosis in a New Zealand sea lion (Phocarctos hookeri) , 2017, New Zealand veterinary journal.

[14]  A. Prusa,et al.  Congenital toxoplasmosis in Austria: Prenatal screening for prevention is cost-saving , 2016, PLoS neglected tropical diseases.

[15]  CongWei,et al.  First Report of Toxoplasma gondii, Dirofilaria immitis, and Chlamydia felis Infection in Stray and Companion Cats in Northeastern and Eastern China , 2016 .

[16]  T. Carpenter,et al.  Coastal development and precipitation drive pathogen flow from land to sea: evidence from a Toxoplasma gondii and felid host system , 2016, Scientific Reports.

[17]  B. Chilvers,et al.  Seroprevalence of Toxoplasma gondii in mainland and sub-Antarctic New Zealand sea lion (Phocarctos hookeri) populations , 2016, New Zealand veterinary journal.

[18]  Kenneth H. Pollock,et al.  Community Attitudes and Practices of Urban Residents Regarding Predation by Pet Cats on Wildlife: An International Comparison , 2016, PloS one.

[19]  A. Lymbery,et al.  Is Toxoplasma gondii a threat to the conservation of free-ranging Australian marsupial populations? , 2015, International journal for parasitology. Parasites and wildlife.

[20]  Glenn D. Aguilar,et al.  Mapping the stray domestic cat (Felis catus) population in New Zealand: Species distribution modelling with a climate change scenario and implications for protected areas , 2015 .

[21]  Stacey A Elmore,et al.  Evidence for Toxoplasma gondii in migratory vs. nonmigratory herbivores in a terrestrial arctic ecosystem , 2015 .

[22]  Christine K. Johnson,et al.  EPIDEMIOLOGY AND PATHOLOGY OF TOXOPLASMA GONDII IN FREE-RANGING CALIFORNIA SEA LIONS (ZALOPHUS CALIFORNIANUS) , 2015, Journal of wildlife diseases.

[23]  B. Fancourt,et al.  Regional seroprevalence of Toxoplasma gondii antibodies in feral and stray cats (Felis catus) from Tasmania , 2014, Australian Journal of Zoology.

[24]  L. L. Bailey,et al.  Toxoplasma gondii exposure in arctic-nesting geese: A multi-state occupancy framework and comparison of serological assays , 2014, International journal for parasitology. Parasites and wildlife.

[25]  P. Wilkins,et al.  Toxoplasma gondii seroprevalence in the United States 2009-2010 and comparison with the past two decades. , 2014, The American journal of tropical medicine and hygiene.

[26]  Menna E. Jones,et al.  Beyond the disease: Is Toxoplasma gondii infection causing population declines in the eastern quoll (Dasyurus viverrinus)? , 2014, International journal for parasitology. Parasites and wildlife.

[27]  P. Hanley,et al.  Controlling Cytomegalovirus: Helping the Immune System Take the Lead , 2014, Viruses.

[28]  J. Yang,et al.  Risk Factors for Acute Toxoplasma gondii Diseases in Taiwan: A Population-Based Case-Control Study , 2014, PloS one.

[29]  W. Roe,et al.  Four Cases of Fatal Toxoplasmosis in Three Species of Endemic New Zealand Birds , 2014, Avian diseases.

[30]  M. Silver,et al.  A New Pathogen Transmission Mechanism in the Ocean: The Case of Sea Otter Exposure to the Land-Parasite Toxoplasma gondii , 2013, PloS one.

[31]  T. Carpenter,et al.  Toxoplasma gondii, Source to Sea: Higher Contribution of Domestic Felids to Terrestrial Parasite Loading Despite Lower Infection Prevalence , 2013, EcoHealth.

[32]  W. Roe,et al.  An atypical genotype of Toxoplasma gondii as a cause of mortality in Hector's dolphins (Cephalorhynchus hectori). , 2013, Veterinary parasitology.

[33]  Melissa A. Miller,et al.  Hydrologic and Vegetative Removal of Cryptosporidium parvum, Giardia lamblia, and Toxoplasma gondii Surrogate Microspheres in Coastal Wetlands , 2013, Applied and Environmental Microbiology.

[34]  S. Pedraza-Díaz,et al.  Detection of Toxoplasma gondii antibodies in Antarctic pinnipeds. , 2012, Veterinary parasitology.

[35]  E. Guzmán-Marín,et al.  Prevalence and Risk Factors of Toxoplasma gondii Infection in Domestic Cats from the Tropics of Mexico Using Serological and Molecular Tests , 2012, Interdisciplinary perspectives on infectious diseases.

[36]  Christopher A. Lepczyk,et al.  Opinions from the Front Lines of Cat Colony Management Conflict , 2012, PloS one.

[37]  Glenn D. Aguilar,et al.  Stray cats in Auckland, New Zealand: Discovering geographic information for exploratory spatial analysis , 2012 .

[38]  A. Swart,et al.  Seroprevalence and risk factors for Toxoplasma gondii infection in domestic cats in The Netherlands. , 2012, Preventive veterinary medicine.

[39]  P. Bennett,et al.  Wandering Cats: Attitudes and Behaviors towards Cat Containment in Australia , 2012 .

[40]  N. Adams,et al.  What's in a Name? Perceptions of Stray and Feral Cat Welfare and Control in Aotearoa, New Zealand , 2011, Journal of applied animal welfare science : JAAWS.

[41]  W. Wallender,et al.  Effect of Estuarine Wetland Degradation on Transport of Toxoplasma gondii Surrogates from Land to Sea , 2010, Applied and Environmental Microbiology.

[42]  M. Farnworth,et al.  Public awareness in New Zealand of animal welfare legislation relating to cats , 2010, New Zealand veterinary journal.

[43]  K. Stockin,et al.  PCBs and organochlorine pesticides in Hector's (Cephalorhynchus hectori hectori) and Maui's (Cephalorhynchus hectori maui) dolphins. , 2010, Marine pollution bulletin.

[44]  M. W. Ware,et al.  Uptake and transmission of Toxoplasma gondii oocysts by migratory, filter-feeding fish. , 2010, Veterinary parasitology.

[45]  J. Aars,et al.  The prevalence of Toxoplasma gondii in polar bears and their marine mammal prey: evidence for a marine transmission pathway? , 2010, Polar Biology.

[46]  W. Browne,et al.  Number and ownership profiles of cats and dogs in the UK , 2010, Veterinary Record.

[47]  P. Conrad,et al.  Cats and Toxoplasma: Implications for Public Health , 2010, Zoonoses and public health.

[48]  D. Weiskopf,et al.  The aging of the immune system , 2009, Transplant international : official journal of the European Society for Organ Transplantation.

[49]  J. Montoya,et al.  Risk factors for Toxoplasma gondii infection in the United States. , 2009, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[50]  D. Lindsay,et al.  Long-Term Survival of Toxoplasma gondii Sporulated Oocysts in Seawater , 2009, The Journal of parasitology.

[51]  M. Demar,et al.  Severe Acquired Toxoplasmosis Caused by Wild Cycle of Toxoplasma gondii, French Guiana , 2009, Emerging infectious diseases.

[52]  A. Di Nardo,et al.  Cat and dog ownership and management patterns in central Italy. , 2008, Preventive veterinary medicine.

[53]  F. Derouin,et al.  Effects of ozone and ultraviolet radiation treatments on the infectivity of Toxoplasma gondii oocysts. , 2008, Veterinary parasitology.

[54]  Melissa A. Miller,et al.  Detection of Toxoplasma gondii-like oocysts in cat feces and estimates of the environmental oocyst burden. , 2007, Journal of the American Veterinary Medical Association.

[55]  G. Gabrielsen,et al.  Serosurvey for Toxoplasma gondii in arctic foxes and possible sources of infection in the high Arctic of Svalbard. , 2007, Veterinary parasitology.

[56]  D. Pontier,et al.  Toxoplasmosis in prey species and consequences for prevalence in feral cats: not all prey species are equal , 2007, Parasitology.

[57]  Melissa A. Miller,et al.  CHEMICAL INACTIVATION OF TOXOPLASMA GONDII OOCYSTS IN WATER , 2007, The Journal of parasitology.

[58]  Melissa A. Miller,et al.  Physical Inactivation of Toxoplasma gondii Oocysts in Water , 2007, Applied and Environmental Microbiology.

[59]  S. Ghosh,et al.  Seropositivity rates for Bartonella henselae, Toxocara canis and Toxoplasma gondii in New Zealand blood donors , 2007, Clinical & experimental ophthalmology.

[60]  E. Afonso,et al.  Transmission of Toxoplasma gondii in an urban population of domestic cats (Felis catus). , 2006, International journal for parasitology.

[61]  W. Ramalho,et al.  Waterborne Toxoplasmosis, Brazil, from Field to Gene , 2006, Emerging infectious diseases.

[62]  J. Zedler,et al.  Wetland resources : Status, trends, ecosystem services, and restorability , 2005 .

[63]  M. Miller,et al.  Transmission of Toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. , 2005, International journal for parasitology.

[64]  J. Dubey Toxoplasmosis - a waterborne zoonosis. , 2004, Veterinary parasitology.

[65]  G. Flick,et al.  SURVIVAL OF TOXOPLASMA GONDII OOCYSTS IN EASTERN OYSTERS (CRASSOSTREA VIRGINICA) , 2004, The Journal of parasitology.

[66]  M. Dardé,et al.  How to detect Toxoplasma gondii oocysts in environmental samples? , 2003, FEMS microbiology reviews.

[67]  Melissa A. Miller,et al.  Molecular and bioassay-based detection of Toxoplasma gondii oocyst uptake by mussels (Mytilus galloprovincialis). , 2003, International journal for parasitology.

[68]  R. Cole,et al.  Sporulation and Survival of Toxoplasma gondii Oocysts in Seawater , 2003, The Journal of eukaryotic microbiology.

[69]  S. More,et al.  Estimated and predicted changes in the cat population of Australian households from 1979 to 2005. , 2003, Australian veterinary journal.

[70]  E. Stiehm,et al.  Syndromic Immunodeficiencies: Genetic Syndromes Associated with Immune Abnormalities , 2003, Critical reviews in clinical laboratory sciences.

[71]  R. C. Rhodes,et al.  Epidemiologic investigation of seroprevalence of antibodies to Toxoplasma gondii in cats and rodents. , 2002, American journal of veterinary research.

[72]  L. Weiss,et al.  Toxoplasma gondii: from animals to humans. , 2000, International journal for parasitology.

[73]  P. Weinstein,et al.  An investigation into the incidence of toxoplasmosis in pregnancy in New Zealand. , 2000, The New Zealand medical journal.

[74]  K. Klasing Nutritional modulation of resistance to infectious diseases. , 1998, Poultry science.

[75]  D. Lindsay,et al.  Structures of Toxoplasma gondiiTachyzoites, Bradyzoites, and Sporozoites and Biology and Development of Tissue Cysts , 1998, Clinical Microbiology Reviews.

[76]  S. Marion,et al.  Outbreak of toxoplasmosis associated with municipal drinking water , 1997, The Lancet.

[77]  M. Slater,et al.  Current issues in the control of stray and feral cats. , 1996, Journal of the American Veterinary Medical Association.

[78]  H. van Loveren,et al.  Contaminant-induced immunotoxicity in harbour seals: wildlife at risk? , 1996, Toxicology.

[79]  J. Dubey,et al.  Duration of immunity to shedding of Toxoplasma gondii oocysts by cats. , 1995, The Journal of parasitology.

[80]  W. Lehmacher,et al.  ELISAs based on recombinant antigens for sero-epidemiological studies on Toxoplasma gondii infections in cats , 1994, Parasitology.

[81]  J. Fishback,et al.  Prospective vaccine prepared from a new mutant of Toxoplasma gondii for use in cats. , 1991, American journal of veterinary research.

[82]  A. Osterhaus,et al.  Identification of virus causing recent seal deaths , 1988, Nature.

[83]  W. Charleston,et al.  Coccidia (Protozoa:Sporozoasida) of cats and dogs. I. Identity and prevalence in cats. , 1980, New Zealand veterinary journal.

[84]  J. P. Dubey,et al.  Reshedding of Toxoplasma oocysts by chronically infected cats , 1976, Nature.

[85]  B. W. B. B.Sc. Incidence of ovine perinatal mortality in New Zealand with particular reference to intrauterine infections , 1964 .

[86]  W. Hartley,et al.  Toxoplasmosis as a cause of ovine perinatal mortality , 1957 .

[87]  Hai Liu,et al.  A review on the sustainability of constructed wetlands for wastewater treatment: Design and operation. , 2015, Bioresource technology.

[88]  P. Parker,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 , 2013, EcoHealth.

[89]  P. Karanis,et al.  The impact of the waterborne transmission of Toxoplasma gondii and analysis efforts for water detection: an overview and update , 2012, Environmental Science and Pollution Research.

[90]  J. Dubey,et al.  Waterborne toxoplasmosis--recent developments. , 2010, Experimental parasitology.

[91]  G. Harper Diet of feral cats on subantarctic Auckland Island , 2010 .

[92]  E. Murphy,et al.  Diet of mammalian predators in braided river beds in the central South Island, New Zealand , 2004 .

[93]  T. Galloway,et al.  Immunotoxicity of Organophosphorous Pesticides , 2003, Ecotoxicology.

[94]  W. Charleston Toxoplasma and other protozoan infections of economic importance in New Zealand , 1994 .

[95]  O. Djurković-Djaković,et al.  High levels of IgM antibodies specific for Toxoplasma gondii in pregnancy 12 years after primary toxoplasma infection. Case report. , 1991, Gynecologic and obstetric investigation.

[96]  B. Karl,et al.  Foods of feral house cats (Felis catus L.) in forest of the Orongorongo Valley, Wellington , 1979 .