Abstract
Recent evidence suggests that snail predators may aid efforts to control the human parasitic disease schistosomiasis by eating aquatic snail species that serve as intermediate hosts of the parasite. Here, potential synergies between schistosomiasis control and aquaculture of giant prawns are evaluated using an integrated bioeconomic–epidemiological model. Combinations of stocking density and aquaculture cycle length that maximize cumulative, discounted profit are identified for two prawn species in sub-Saharan Africa: the endemic, non-domesticated Macrobrachium vollenhovenii and the non-native, domesticated Macrobrachium rosenbergii. At profit-maximizing densities, both M. rosenbergii and M. vollenhovenii may substantially reduce intermediate host snail populations and aid schistosomiasis control efforts. Control strategies drawing on both prawn aquaculture to reduce intermediate host snail populations and mass drug administration to treat infected individuals are found to be superior to either strategy alone. Integrated aquaculture-based interventions can be a win–win strategy in terms of health and sustainable development in schistosomiasis endemic regions of the world.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Data availability
All data used to conduct this analysis are freely available at https://github.com/cmhoove14/Prawn_fisheries_Public_health, provided in the Supplementary Code and Data folder and available from the corresponding author on request.
Code availability
All code used to conduct this analysis is freely available at https://github.com/cmhoove14/Prawn_fisheries_Public_health, provided in the Supplementary Code and Data folder and available from the corresponding author on request.
References
Schistosomiasis: Progress Report 2001–2011, Strategic Plan 2012–2020 (WHO, 2013).
Lai, Y.-S. et al. Spatial distribution of schistosomiasis and treatment needs in sub-Saharan Africa: a systematic review and geostatistical analysis. Lancet Infect. Dis. 15, 927–940 (2015).
Steinmann, P., Keiser, J., Bos, R., Tanner, M. & Utzinger, J. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect. Dis. 6, 411–425 (2006).
Colley, D. G. et al. Defining persistent hotspots: areas that fail to decrease meaningfully in prevalence after multiple years of mass drug administration with praziquantel for control of schistosomiasis. Am. J. Trop. Med. Hyg. 97, 1810–1817 (2017).
Stothard, J. R. et al. Towards interruption of schistosomiasis transmission in sub-Saharan Africa: developing an appropriate environmental surveillance framework to guide and to support ‘end game’ interventions. Infect. Dis. Poverty 6, 10 (2017).
Sokolow, S. H. et al. Global assessment of schistosomiasis control over the past century shows targeting the snail intermediate host works best. PLoS Negl. Trop. Dis. 10, e0004794 (2016).
Lo, N. C. et al. Impact and cost-effectiveness of snail control to achieve disease control targets for schistosomiasis. Proc. Natl Acad. Sci. USA 115, E584–E591 (2018).
King, C. H., Sutherland, L. J. & Bertsch, D. Systematic review and meta-analysis of the impact of chemical-based mollusciciding for control of Schistosoma mansoni and S. haematobium transmission. PLoS Negl. Trop. Dis. 9, e0004290 (2015).
Andrews, P., Thyssen, J. & Lorke, D. The biology and toxicology of molluscicides, Bayluscide. Pharmacol. Ther. 19, 245–295 (1982).
Dawson, V. K. Environmental fate and effects of the lampricide Bayluscide: a review. J. Great Lakes Res. 29, 475–492 (2003).
Mkoji, G. M. et al. Impact of the crayfish Procambarus clarkii on Schistosoma haematobium transmission in Kenya. Am. J. Trop. Med. Hyg. 61, 751–759 (1999).
Sokolow, S. H. et al. Reduced transmission of human schistosomiasis after restoration of a native river prawn that preys on the snail intermediate host. Proc. Natl Acad. Sci. USA 112, 9650–9655 (2015).
Sokolow, S. H., Lafferty, K. D. & Kuris, A. M. Regulation of laboratory populations of snails (Biomphalaria and Bulinus spp.) by river prawns, Macrobrachium spp. (Decapoda, Palaemonidae): implications for control of schistosomiasis. Acta Trop. 132, 64–74 (2014).
Roberts, J. K. & Kuris, A. M. Predation and control of laboratory populations of the snail Biomphalaria glabrata by the freshwater prawn Macrobrachium rosenbergii. Ann. Trop. Med. Parasitol. 84, 401–412 (1990).
Islam, M. S. & Wahab, M. A. A review on the present status and management of mangrove wetland habitat resources in Bangladesh with emphasis on mangrove fisheries and aquaculture. Hydrobiologia 542, 165–190 (2005).
Report of the FAO Expert Workshop on the Use of Wild Fish and/or Other Aquatic Species as Feed in Aquaculture and its Implications to Food Security and Poverty Alleviation (Food and Agriculture Organization of the United Nations, 2008).
New, M. B., Valenti, W. C., Tidwell, J. H., D’Abramo, L. R. & Kutty, M. N. Freshwater Prawns: Biology and Farming (Blackwell, 2010).
New, M. B. & Valenti, W. C. Freshwater Prawn Culture: the Farming of Macrobrachium Rosenbergii (Blackwell Science, 2000).
Savaya Alkalay, A. et al. The prawn Macrobrachium vollenhovenii in the Senegal River basin: towards sustainable restocking of all-male populations for biological control of schistosomiasis. PLoS Negl. Trop. Dis. 8, e3060 (2014).
Levy, T. et al. All-female monosex culture in the freshwater prawn Macrobrachium rosenbergii—a comparative large-scale field study. Aquaculture 479, 857–862 (2017).
Hotez, P. J. et al. The Global Burden of Disease Study 2010: interpretation and implications for the neglected tropical diseases. PLoS Negl. Trop. Dis. 8, e2865 (2014).
Balasubramanian, V., Sie, M., Hijmans, R. J. & Otsuka, K. Increasing rice production in sub-Saharan Africa: challenges and opportunities. Adv. Agron. 94, 55–133 (2007).
Ahmed, N. & Garnett, S. T. Sustainability of freshwater prawn farming in rice fields in southwest Bangladesh. J. Sustain. Agric. 34, 659–679 (2010).
Lo, N. C. et al. Assessment of global guidelines for preventive chemotherapy against schistosomiasis and soil-transmitted helminthiasis: a cost-effectiveness modelling study. Lancet Infect. Dis. 16, 1065–1075 (2016).
Beverton, R. J. H. & Holt, S. J. On the Dynamics of Exploited Fish Populations (Springer Netherlands, 1993).
Zwang, J. & Olliaro, P. L. Clinical efficacy and tolerability of praziquantel for intestinal and urinary schistosomiasis—a meta-analysis of comparative and non-comparative clinical trials. PLoS Negl. Trop. Dis. 8, e3286 (2014).
Lo, N. C. et al. Comparison of community-wide, integrated mass drug administration strategies for schistosomiasis and soil-transmitted helminthiasis: a cost-effectiveness modelling study. Lancet Glob. Health 3, e629–e638 (2015).
Ngonghala, C. N. et al. Poverty, disease, and the ecology of complex systems. PLoS Biol. 12, e1001827 (2014).
King, C. H. Parasites and poverty: the case of schistosomiasis. Acta Trop. 113, 95–104 (2010).
Toor, J. et al. Are we on our way to achieving the 2020 goals for schistosomiasis morbidity control using current World Health Organization guidelines? Clin. Infect. Dis. 66, S245–S252 (2018).
Younes, A., El-Sherief, H., Gawish, F. & Mahmoud, M. Biological control of snail hosts transmitting schistosomiasis by the water bug, Sphaerodema urinator. Parasitol. Res. 116, 1257–1264 (2017).
Dasgupta, S. & Tidwell, J. H. A breakeven price analysis of four hypothetical freshwater prawn, Macrobrachium rosenbergii, farms using data from Kentucky. J. Appl. Aquac. 14, 1–22 (2003).
Asche, F. Farming the sea. Mar. Resour. Econ. 23, 527–547 (2008).
Kumar, G. & Engle, C. R. Technological advances that led to growth of shrimp, salmon, and tilapia farming. Rev. Fish. Sci. Aquac. 24, 136–152 (2016).
Karplus, I. & Sagi, A. in Freshwater Prawns: Biology and Farming 316–345 (Wiley-Blackwell, 2009).
Ventura, T. & Sagi, A. The insulin-like androgenic gland hormone in crustaceans: from a single gene silencing to a wide array of sexual manipulation-based biotechnologies. Biotechnol. Adv. 30, 1543–1550 (2012).
Aflalo, E. D. et al. A novel two-step procedure for mass production of all-male populations of the giant freshwater prawn Macrobrachium rosenbergii. Aquaculture 256, 468–478 (2006).
Levy, T. et al. A single injection of hypertrophied androgenic gland cells produces all-female aquaculture. Mar. Biotechnol. 18, 554–563 (2016).
Savaya-Alkalay, A. et al. Exploitation of reproductive barriers between Macrobrachium species for responsible aquaculture and biocontrol of schistosomiasis in West. Afr. Aquac. Environ. Interact. 10, 487–499 (2018).
Lalrinsanga, P. L. et al. Length weight relationship and condition factor of giant freshwater prawn Macrobrachium rosenbergii (De Man, 1879) based on developmental stages, culture stages and sex. Turk. J. Fish. Aquat. Sci. 12, 917–924 (2012).
Nwosu, F. & Wolfi, M. Population dynamics of the Giant African River prawn Macrobrachium vollenhovenii Herklots 1857 (Crustacea, Palaemonidae) in the Cross River Estuary, Nigeria. West African J. Appl. Ecol. 9, 1–14 (2009).
Halstead, N. T., Civitello, D. J. & Rohr, J. R. Comparative toxicities of organophosphate and pyrethroid insecticides to aquatic macroarthropods. Chemosphere 135, 265–271 (2015).
Halstead, N. T. et al. Agrochemicals increase risk of human schistosomiasis by supporting higher densities of intermediate hosts. Nat. Commun. 9, 837 (2018).
Gurarie, D., Lo, N. C., Ndeffo-Mbah, M. L., Durham, D. P. & King, C. H. The human–snail transmission environment shapes long term schistosomiasis control outcomes: implications for improving the accuracy of predictive modeling. PLoS Negl. Trop. Dis. 12, e0006514 (2018).
Ciddio, M. et al. The spatial spread of schistosomiasis: a multidimensional network model applied to Saint-Louis region, Senegal. Adv. Water Resour. 108, 406–415 (2016).
Civitello, D. J., Fatima, H., Johnson, L. R., Nisbet, R. M. & Rohr, J. R. Bioenergetic theory predicts infection dynamics of human schistosomes in intermediate host snails across ecological gradients. Ecol. Lett. 21, 692–701 (2018).
Perez-Saez, J. et al. A theoretical analysis of the geography of schistosomiasis in Burkina Faso highlights the roles of human mobility and water resources development in disease transmission. PLoS Negl. Trop. Dis. 9, e0004127 (2015).
Perez-Saez, J. et al. Hydrology and density feedbacks control the ecology of intermediate hosts of schistosomiasis across habitats in seasonal climates. Proc. Natl Acad. Sci. USA 113, 6427–6432 (2016).
Sturrock, R. F. et al. Seasonality in the transmission of schistosomiasis and in populations of its snail intermediate hosts in and around a sugar irrigation scheme at Richard Toll, Senegal. Parasitology 123, 77–89 (2001).
Ranjeet, K. & Kurup, B. M. Heterogeneous individual growth of Macrobrachium rosenbergii male morphotypes. Naga 25, 13–18 (2002).
Von Bertalanffy, L. A quantitative theory of organic growth (inquiries on growth laws II). Hum. Biol. 10, 181–213 (1938).
Sampaio, C. M. & Valenti, W. C. Growth curves for Macrobrachium rosenbergii in semi-intensive culture in Brazil. J. World Aquac. Soc. 27, 353–358 (1996).
Lima, J.d.F., Garcia, J.d.S. & da Silva, T.C. Natural diet and feeding habits of a freshwater prawn (Macrobrachium carcinus: Crustacea, Decapoda) in the estuary of the Amazon River. Acta Amaz. 44, 235–244 (2014).
Lorenzen, K. The relationship between body weight and natural mortality in juvenile and adult fish: a comparison of natural ecosystems and aquaculture. J. Fish Biol. 49, 627–647 (1996).
Discount Rates for Cost-Effectiveness Analysis of Federal Programs (Office of Management and Budget, 2018).
Reed, W. J. Optimal harvesting models in forest management—a survey. Nat. Resour. Model. 1, 55–79 (1986).
Karp, L., Sadeh, A. & Griffin, W. L. Cycles in agricultural production: the case of aquaculture. Am. J. Agric. Econ. 68, 553–561 (1986).
Guttormsen, A. G. Faustmann in the sea: optimal rotation in aquaculture. Mar. Resour. Econ. 23, 401–410 (2008).
Lafferty, K. D. & Kuris, A. M. Parasitic castration: the evolution and ecology of body snatchers. Trends Parasitol. 25, 564–572 (2009).
Mangal, T. D., Paterson, S. & Fenton, A. Effects of snail density on growth, reproduction and survival of Biomphalaria alexandrina exposed to Schistosoma mansoni. J. Parasitol. Res. 2010, 186792 (2010).
Anderson, R. M. & May, R. M. Infectious Diseases of Humans: Dynamics and Control (Oxford Univ. Press, 1991).
May, R. M. Togetherness among schistosomes: its effects on the dynamics of the infection. Math. Biosci. 35, 301–343 (1977).
Chu, K. Y. & Dawood, I. K. Cercarial production from Biomphalaria alexandrina infected with Schistosoma mansoni. Bull. World Health Organ. 42, 569–574 (1970).
Holling, C. S. The components of predation as revealed by a study of small-mammal predation of the European pine sawfly. Can. Entomol. 91, 293–320 (1959).
Soetaert, K., Petzoldt, T. & Setzer, R. W. Solving differential equations in R: package deSolve. J. Stat. Softw. 33, 1–25 (2010).
Acknowledgements
C.M.H., J.V.R., G.A.D.L., I.J.J., A.J.L., S.H.S., G.R. and J.R.R. were supported by National Institutes of Health grant R01TW010286 (to J.R.R. and J.V.R.). C.M.H. and J.V.R. were additionally supported in part by National Science Foundation ‘Water Sustainability and Climate’ grants (1360330 and 1646708 to J.V.R.), National Institutes of Health grant R01AI125842 (to J.V.R.) and the University of California Multicampus Research Programs and Initiatives award MRP-17-446315 (to J.V.R.). G.A.D.L., I.J.J., A.J.L. and S.H.S. were additionally funded by a grant from the Bill and Melinda Gates Foundation (OPP1114050) and a GDP SEED grant from the Freeman Spogli Institute at Stanford University. G.A.D.L., I.J.J., A.J.L., S.H.S. and J.N.S. were also supported by National Science Foundation ‘Dynamics of Coupled Natural and Human Systems’ grant 1414102. G.A.D.L., S.H.S., C.M.H., J.V.R., J.N.S., R.C., L.M. and M.G. were also supported by NIMBioS through the working group on the Optimal Control of Environmentally Transmitted Disease. J.P.-S. and A.R. acknowledge funds provided by the Swiss National Science Foundation via the project ‘Optimal control of intervention strategies for waterborne disease epidemics’ (200021-172578/1). C.L.W. was supported by the Michigan Society of Fellows at the University of Michigan and by a Sloan Research Fellowship from the Alfred P. Sloan Foundation. R.C. and L.M. were also supported by Politecnico di Milano through the Polisocial Award programme (project MASTR-SLS).
Author information
Authors and Affiliations
Contributions
G.A.D.L. and S.H.S. conceived the problem and designed the general modelling framework. C.M.H., S.H.S., J.K., J.V.R. and G.A.D.L. developed the analysis. C.M.H. and J.K. wrote the simulation scripts. G.R. collected field data to parameterize the epidemiological model. S.H.S. provided experimental data to parameterize the predation component of the model. J.N.S. provided guidance on profit estimation of the prawn aquaculture model. A.Savaya, S.C. and A.Sagi. provided guidance on the dynamics of the aquaculture model. C.M.H., J.K., J.N.S., J.V.R. and G.A.D.L. drafted the manuscript. All authors contributed to editing the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Supplementary Information
Supplementary methods, Tables 1–3, Figs. 1–9 and references 1–25
Supplementary Code and Data
A ZIP file containing all R code and the data files necessary to reproduce the analysis. This can also be found on GitHub at https://github.com/cmhoove14/Prawn_fisheries_Public_health
Rights and permissions
About this article
Cite this article
Hoover, C.M., Sokolow, S.H., Kemp, J. et al. Modelled effects of prawn aquaculture on poverty alleviation and schistosomiasis control. Nat Sustain 2, 611–620 (2019). https://doi.org/10.1038/s41893-019-0301-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41893-019-0301-7
This article is cited by
-
A planetary health innovation for disease, food and water challenges in Africa
Nature (2023)
-
Ecohydrology 2.0
Rendiconti Lincei. Scienze Fisiche e Naturali (2022)
-
Emerging human infectious diseases and the links to global food production
Nature Sustainability (2019)