HUMAN INFECTIOUS DISEASE​

Protozoan pathogens, including Cryptosporidium spp., Giardia duodenalis, and Toxoplasma gondii

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CONSERVATION PROBLEM

Marine mammal declines (potentially caused by T. gondii)

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INTERVENTION

Management/treatment of fecal-contaminated water: (1) reduce or eliminate human and animal manure and resulting runoff from agriculture; (2) disinfect aquatic discharge (e.g. UV-treatment), or (3) construct, conserve, or restore wetlands between agricultural lands or urban communities and waterways to reduce protozoan loads in runoff (also see this case study).

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TARGET

Protozoan-contaminated aquatic discharge to the marine environment

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MECHANISM

Reducing protozoans in effluent will both decrease exposure for humans during ocean recreation and/or shellfish consumption and decrease exposure for marine mammals.

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HUMAN INFECTIOUS DISEASE EVIDENCE

DIVERSE EVIDENCE: Secondary wastewater treatment does not remove protozoans, whereas tertiary treatment removes most protozoans. OBSERVATIONAL: Many waterborne protozoan outbreaks have been reported and seasonal peaks in disease are hypothetically linked to aquatic recreation. Transmission through eating shellfish has been reported, but likely underestimated. Natural/constructed wetlands can remove some, but probably not all, protozoans from effluent, depending on design/structure (also see this case study).

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CONSERVATION EVIDENCE

OBSERVATIONAL/MODEL: Densely populated areas (more humans and cats) have been associated with increased T. gondii oocyst delivery to the ocean and infection in otters. T. gondii antibodies in Antarctic pinnipeds suggests potential long-distance dispersal of oocysts. However, one study found that otters near densely populated areas have lower T. gondii prevalence. ANECDOTE: Acanthocephalans (trophically-transmitted via sand crabs) may be true driver of otter declines.

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LOCATION AND SPATIAL SCALE

Human health risk is global, from marine to freshwater systems. Otter deaths attributed to protozoan infection are predominantly from the Pacific coast of North America, but this may be detection bias. Dolphin infections have been reported worldwide, including cases of congenital Toxoplasmosis acquired through transplacental transmission.

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TEMPORAL SCALE

Cysts/oocysts are environmentally resilient for up to a year; marine mammal populations have declined over decades for various reasons, with disease as a possible driver.

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HEALTH SUCCESS METRICS

Hypothetically, reduced gastrointestinal illness and T. gondii-associated pregnancy complications in humans

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CONSERVATION SUCCESS METRICS

Hypothetically, population rebounds in marine mammals

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HUMAN CO-BENEFITS

People enjoy observing marine mammals, which can benefit coastal economies (e.g. tourism and whale-watching).

 

CONSERVATION CO-BENEFITS

Potentially decreased pollution from other pathogens and non-infectious contaminants and improved kelp forest and/or wetland functioning.

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COLLATERAL HUMAN IMPACTS

Sludge treatment for protozoans reduces nutrient value when using sludge for farming.

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COLLATERAL CONSERVATION IMPACTS

None known

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SOCIAL ACCEPTABILITY

Likely socially acceptable, but wetland restoration/construction may face opposition by developers.

 

EQUITY CONSIDERATIONS

None known

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PRACTICALITY/CHALLENGES

Wastewater treatment requires land, infrastructure, and public funding. Feral cat colonies on coastlines serve as an untreated source of T. gondii input.

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STATUS

Wastewater treatment is commonly used to protect human health in developed nations, but tertiary treatment plants that can remove protozoans are less widespread.

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RESEARCH NEEDS

To determine whether this is a “win” for conservation, research must identify the sources of protozoans responsible for marine mammal infections (i.e., domestic vs. wildlife sources). We also need intervention studies linking wastewater management and human health outcomes.

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REFERENCES

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EXPERIMENTS

K. Shapiro, P. A. Conrad, J. A. K. Mazet, W. W. Wallender, W. A. Miller, J. L. Largier, Effect of estuarine wetland degradation on transport of Toxoplasma gondii surrogates from land to sea. Appl. Environ. Microb. 76, 6821-6828 (2010).

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OBSERVATIONAL STUDIES

W. Q. Betancourt, D. C. Duarte, R. C. Vásquez, P. L. Gurian, Cryptosporidium and Giardia in tropical recreational marine waters contaminated with domestic sewage: estimation of bathing-associated disease risks. Mar. Pollut. Bull. 85, 268-273 (2014). 

 

N. J. Hogan, M. E. Daniels, F. G. Watson, P. A. Conrad, S. C. Oates, M. A. Miller, D. Hardin, B. A. Byrne, C. Dominik, A. Melli, D. A. Jessup, W. A. Miller, Longitudinal poisson regression to evaluate the epidemiology of Cryptosporidium, Giardia and fecal indicator bacteria in coastal California wetlands. Appl. Environ. Microb. 78, 3606-3613 (2012).

 

J. Ma, Y. Feng, Y. Hu, E. N. Villegas, L. Xiao, Human infective potential of Cryptosporidum spp., Giardia duodenalis and Enterocytozoon bieneusi in urban wastewater treatment plant effluents. J. Water Health 14, 411-423 (2016).

 

M. A. Miller, L. A. Gardner, C. Kreuder, D. Paradies, K. Worcester, D. Jessup, E. Dodd, M. Harris, J. Ames, A. Packham, P. A. Conrad, Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection of southern sea otters (Enhydra lutris nereis). Int. J. Parasitol. 32, 997-1006 (2002).

 

C. Rengifo-Herrera, L. M. Ortega-Mora, G. Álvarez-García, M. Gómez-Bautista, D. García-Párraga, F. J. García-Peña, S. Pedraza-Díaz, Detection of Toxoplasma gondii antibodies in Antarctic pinnipeds, Vet. Parasitol. 190, 259-262 (2012).

 

M. T. Tinker Ed. “Sea otter population biology at Big Sur and Monterey California: investigating the consequences of resource abundance and anthropogenic stressors for sea otter recovery.” University of California, Santa Cruz, CA. Draft Final Report to California Coastal Conservancy and U.S. Fish and Wildlife Service (2013).

http://www.fws.gov/ventura/docs/species/sso/Big%20Sur%20Monterey%20Sea%20Otter%20Study%20Draft%20Report.pdf

 

E. VanWormer, P. A. Conrad, M. A. Miller, A. C. Melli, T. E. Carpenter, J. A. K. Mazet, Toxoplasma gondii, source to sea: higher contribution of domestic felids to terrestrial parasite loading despite lower infection prevalence. EcoHealth 10, 227-289 (2013).

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MODELING STUDIES

E. VanWormer, T. E. Carpenter, P. Singh, K. Shapiro, W. W. Wallender, P. A. Conrad, J. L. Largier, M. P. Maneta, J. A. K. Mazet, Coastal development and precipitation drive pathogen flow from land to sea: evidence from a Toxoplasma gondii and felid host system. Sci. Rep. 6, 29252 (2016).

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REVIEWS

S. M. Fletcher, D. Stark, J. Harkness, J. Ellis, Enteric protozoa in the developed world: a public health perspective. Clin. Microbiol. Rev. 25, 420-449 (2012).

 

A. M. Nasser, Removal of Cryptosporidium by wastewater treatment processes: a review. J. Water Health 14, 1-13 (2016).

 

L. J. Robertson, The potential for marine bivalve shellfish to act as transmission vehicles for outbreaks of protozoan infections in humans: a review. Int. J. Food Microbiol. 120, 201-216 (2007).

M. E. Verbyla, M. R. Cairns, P. A. Gonzalez, L. M. Whiteford, J. R. Mihelcic, Emerging challenges for pathogen control and resource recovery in natural wastewater treatment systems. WIREs Water 2, 701-704 (2015).

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OTHER SUPPORTING INFORMATION

A. D. Adell, G. McBride, S. Wuertz, P. A. Conrad, W. A. Smith, Comparison of human and southern sea otter (Enhydra lutris nereis) health risks for infection with protozoa in nearshore waters. Water Res. 104, 220–230 (2016).

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J. L. Baily, G. Méric, S. Bayliss, G. Foster, S. E. Moss, E. Watson, B. Pascoe, J. Mikhail, R. Pizzi, R. J. Goldstone, D. G. E. Smith, K. Willoughby, A. J. Hall, S. K. Sheppard, M. P. Dagleish, Evidence of land-sea transfer of the zoonotic pathogen Campylobacter to a wildlife marine sentinel species. Mol Ecol. 24, 208–221 (2015).

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G. D. Bossart, Marine mammals as sentinel species for oceans and human health. Vet Pathol. 48, 676–690 (2011).

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P. A. Conrad, M. A. Miller, C. Krueder, E. R. James, J. Mazet, H. Dabritz, D. A. Jessup, F. Gulland, M. E. Grigg, Transmission of Toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. Int. J. Parasitol. 35, 1155-1168 (2005).

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M. C. F. Davidson, T. Berardi, B. Aguilar, B. A. Byrne, K. Shapiro, Effects of transparent exopolymer particles and suspended particles on the survival of Salmonella enterica serovar Typhimurium in seawater. FEMS Microbiol Ecol. 91 (2015), doi:10.1093/femsec/fiv005.

 

R. Fayer, J. P. Dubey, D. S. Lindsay, Zoonotic protozoa: from land to sea. Trends Parasitol. 20, 531-536 (2004).

 

K. D. Lafferty, L. R. Gerber, Good medicine for conservation biology: the intersection of epidemiology and conservation theory. Conserv. Biol. 16, 593-604 (2002).

 

K. D. Lafferty, Sea otter health: challenging a pet hypothesis. Int. J. Parasitol.- Par. 4, 291-294 (2015). 

 

D. S. Lindsay, J. P. Dubey, “Toxoplasmosis in wild and domestic animals” in Toxoplasma gondii. The Model Apicomplexan: Perspectives and Methods, L. M. Weiss, K. Kim, Eds. (Academic Press, 2014), pp. 193-215.

 

K. Shapiro, M. Miller, J. Mazet, Temporal association between land-based runoff events and California sea otter (Enhydra lutris nereis) protozoal mortalities. J Wildl Dis. 48, 394–404 (2012).

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A. Simon, A. N. Rousseau, S. Savary, M. Bigras-Poulin, N. H. Ogden, Hydrological modelling of Toxoplasma gondii oocysts transport to investigate contaminated snowmelt runoff as a potential source of infection for marine mammals in the Canadian Arctic. J Environ Manage. 127, 150–161 (2013).

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M. Strathmann, M. Horstkott, C. Koch, U. Gayer, J. Wingender, The River Ruhr - an urban river under particular interest for recreational use and as a raw water source for drinking water: The collaborative research project “Safe Ruhr” - microbiological aspects. Int J Hyg Environ Health. 219, 643–661 (2016).

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Page last updated: 3/14/2021 

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