Effect of water temperature and population density on the population dynamics of Schistosoma mansoni intermediate host snails

Particle and Fibre Toxicology

Mark Booth¹  Edridah M Tukahebwa²  Wilber Arineitwe²  Moses Arinaitwe²  Nicky McCreesh¹ 

[1] School of Medicine, Pharmacy and Health, Durham University, Durham DH1 3LE, UK;Vector Control Division, Ministry of Health, Plot 15 Bombo Road, Kampala, Uganda

关键词: Ecology;    Climate change;    Malacology;    Biomphalaria;    Schistosoma mansoni;    Schistosomiasis;   

Others  :  1149402
DOI  :  10.1186/s13071-014-0503-9

 received in 2014-09-24, accepted in 2014-10-26,  发布年份 2014

【 摘 要 】

Background

Mathematical models can be used to identify areas at risk of increased or new schistosomiasis transmission as a result of climate change. The results of these models can be very different when parameterised to different species of host snail, which have varying temperature preferences. Currently, the experimental data needed by these models are available for only a few species of snail. The choice of density-dependent functions can also affect model results, but the effects of increasing densities on Biomphalaria populations have only previously been investigated in artificial aquariums.

Methods

Laboratory experiments were conducted to estimate Biomphalaria sudanica mortality, fecundity and growth rates at ten different constant water temperatures, ranging from 13-32°C. Snail cages were used to determine the effects of snail densities on B. sudanica and B. stanleyi mortality and fecundity rates in semi-natural conditions in Lake Albert.

Results

B. sudanica survival and fecundity were highest at 20°C and 22°C respectively. Growth in shell diameter was estimated to be highest at 23°C in small and medium sized snails, but the relationship between temperature and growth was not clear. The fecundity of both B. sudanica and B. stanleyi decreased by 72-75% with a four-fold increase in population density. Increasing densities four-fold also doubled B. stanleyi mortality rates, but had no effect on the survival of B. sudanica.

Conclusions

The optimum temperature for fecundity was lower for B. sudanica than for previously studied species of Biomphalaria. In contrast to other Biomphalaria species, B. sudanica have a distinct peak temperature for survival, as opposed to a plateau of highly suitable temperatures. For both B. stanleyi and B. sudanica, fecundity decreased with increasing population densities. This means that snail populations may experience large fluctuations in numbers, even in the absence of any external factors such as seasonal temperature changes. Survival also decreased with increasing density for B. stanleyi, in contrast to B. sudanica and other studied Biomphalaria species where only fecundity has been shown to decrease.

【 授权许可】

   
2014 McCreesh et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]McCreesh N, Booth M: The effect of increasing water temperatures on Schistosoma mansoni transmission and Biomphalaria pfeifferi population dynamics: an agent-based modelling study. PLoS One 2014, 9(7):e101462.
• [2]Martens WJM, Jetten TH, Focks DA: Sensitivity of malaria, schistosomiasis and dengue to global warming. Clim Change 1997, 35(2):145-156.
• [3]Martens WJM, Jetten TH, Rotmans J, Niessen LW: Climate change and vector-borne diseases: a global modelling perspective. Glob Environ Chang 1995, 5(3):195-209.
• [4]Mangal TD, Paterson S, Fenton A: Predicting the impact of long-term temperature changes on the epidemiology and control of schistosomiasis: a mechanistic model. PLoS One 2008, 3(1):e1438.
• [5]McCreesh N, Booth M: Challenges in predicting the effects of climate change on Schistosoma mansoni and Schistosoma haematobium transmission potential. Trends Parasitol 2013, 29(11):548-555.
• [6]McCreesh N, Booth M: The effect of simulating different intermediate host snail species on the link between water temperature and schistosomiasis risk. PLoS One 2014, 9(7):e87892.
• [7]Stensgaard A-S, Utzinger J, Vounatsou P, Hürlimann E, Schur N, Saarnak CFL, Simoonga C, Mubita P, Kabatereine NB, Tchuenté L-AT, Rahbek C, Kristensen TK: Large-scale determinants of intestinal schistosomiasis and intermediate host snail distribution across Africa: Does climate matter? Acta Trop 2013, 128(2):378-390.
• [8]Schistosomiasis: Progress Report 2001-2011, Strategic Plan 2012-2020. Potchefstroom, Geneva, Switzerland; 2013.
• [9]Brown D: Freshwater Snails of Africa and their Medical Importance. 2nd edition. Taylor & Francis, London, UK; 1994.
• [10]Rollinson D: Biomphalaria : Natural history, ecology and schistosome transmission. In Biomphalaria Snails and Larval Trematodes. Edited by Toledo R, Fried B. New York: Springer; 2011:57¿79.
• [11]Clements ACA, Deville M-A, Ndayishimiye O, Brooker S, Fenwick A: Spatial co-distribution of neglected tropical diseases in the East African Great Lakes region: revisiting the justification for integrated control. Trop Med Int Health 2010, 15(2):198-207.
• [12]Standley CJ, Wade CM, Stothard JR: A fresh insight into transmission of Schistosomiasis: a misleading tale of Biomphalaria in Lake Victoria. PLoS One 2011, 6(10):e26563.
• [13]Plam M, Jørgensen A, Kristensen TK, Madsen H: Sympatric Biomphalaria species (Gastropoda: Planorbidae) in Lake Albert, Uganda, show homoplasies in shell morphology. Afr Zool 2008, 43(1):34-44.
• [14]Kazibwe F, Makanga B, Rubaire-Akiiki C, Ouma J, Kariuki C, Kabatereine N, Booth M, Vennervald B, Sturrock R, Stothard J: Ecology of Biomphalaria (Gastropoda: Planorbidae) in Lake Albert, Western Uganda: snail distributions, infection with schistosomes and temporal associations with environmental dynamics. Hydrobiologia 2006, 568(1):433-444.
• [15]Thomas JD, Benjamin M: The effects of population density on growth and reproduction of Biomphalaria glabrata (Say) (Gasteropoda: Pulmonata). J Anim Ecol 1974, 43(1):31-50.
• [16]Mangal TD, Paterson S, Fenton A: Effects of snail density on growth, reproduction and survival of Biomphalaria alexandrina exposed to Schistosoma mansoni. J Parasitol Res 2010, 2010:186792.
• [17]Chernin E, Michelson EH: Studies on the biological control of schistosome-bearing snails. III. The effects of population density on growth and fecundity in Australorbis glabratus. Am J Hyg 1957, 65(1):57-70.
• [18]Loreau M, Baluku B: Growth and demography of populations of Biomphalaria pfeifferi (Gastropoda, Planorbidae) in the laboratory. J Molluscan Stud 1987, 53(2):171-177.
• [19]Eveland L, Haseeb M: Laboratory rearing of Biomphalaria glabrata snails and maintenance of larval schistosomes in vivo and in vitro . In Biomphalaria Snails and Larval Trematodes. New York, USA: Springer; 2011:33¿55.
• [20]Woolhouse M: A mark-recapture method for ecological studies of schistosomiasis vector snail populations. Ann Trop Med Parasitol 1988, 82(5):485-497.
• [21]Chlyeh G, Henry P-Y, Jarne P: Spatial and temporal variation of life-history traits documented using capture-mark-recapture methods in the vector snail Bulinus truncatus. Parasitology 2003, 127(03):243-251.
• [22]Kariuki C: Comparative Ecological Studies on Transmission of Schistosoma mansoni and Population Dynamics, Taxonomy and Molluscicide Sensitivity of Biomphalaria pfeifferi, Intermediate Host of S. mansoni, in Two Areas of Machakos District, Kenya. University of Copenhagen; 1994.
• [23]Ravera O: Effects of heavy metals (cadmium, copper, chromium and lead) on a freshwater snail: Biomphalaria glabrata Say (Gastropoda, Prosobranchia). Malacologia 1976, 16(1):231-236.
• [24]Shiff CJ, Garnett B: The influence of temperature on the intrinsic rate of natural increase of the freshwater snail Biomphalaria pfeifferi (Krauss). Arch für Hydrobiologie 1963, 62:429-438.
• [25]Appleton CC: The influence of above-optimal constant temperatures on South African Biomphalaria pfeifferi (Krauss) (Mollusca: Planorbidae). Trans R Soc Trop Med Hyg 1977, 71(2):140-143.
• [26]Foster R: The effect of temperature on the development of Schistosoma mansoni Sambon 1907 in the intermediate host. J Trop Med Hyg 1964, 67:289-292.
• [27]Sturrock RF: The influence of temperature on the biology of Biomphalaria pfeifferi (Krauss), an intermediate host of Schistosoma mansoni. Ann Trop Med Parasitol 1966, 60(1):100-105.
• [28]De Kock KN, Van Eeden JA, Slaknavorsingseenheid PUfCHE, Unit SAMRCSR: Life Table Studies on Freshwater Snails: The Effect of Constant Temperature on the Population Dynamics of Biomphalaria pfeifferi (Krauss). Potchefstroom, South Africa: Potchefstroom University for CHE Publications; 1981.
• [29]El-Hassan AA: Laboratory studies on the direct effect of temperature on Bulinus truncatus and Biomphalaria alexandrina, the snail intermediate hosts of schistosomes in Egypt. Folia Parasitol (Praha) 1974, 21(2):181-187.
• [30]Pfluger W: Experimental epidemiology of schistosomiasis. I. The prepatent period and cercarial production of Schistosoma mansoni in Biomphalaria snails at various constant temperatures. Z Parasitenkd 1980, 63(2):159-169.
• [31]Pimentel-Souza F, Barbosa ND, Resende DF: Effect of temperature on the reproduction of the snail Biomphalaria glabrata. Braz J Med Biol Res 1990, 23(5):441-449.
• [32]Marti H: Field observations on the population dynamics of Bulinus globosus, the Intermediate Host of Schistosoma haematobium in the Ifakara Area, Tanzania. J Parasitol 1986, 72(1):119-124.