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Schistosoma Mansoni Intermediate Host Snails.', Parasites and Vectors., 7 Durham Research Online Deposited in DRO: 08 December 2014 Version of attached le: Published Version Peer-review status of attached le: Peer-reviewed Citation for published item: McCreesh, N. and Booth, M. (2014) 'Eect of water temperature and population density on the population dynamics of Schistosoma mansoni intermediate host snails.', Parasites and vectors., 7 . p. 503. Further information on publisher's website: http://dx.doi.org/10.1186/s13071-014-0503-9 Publisher's copyright statement: c McCreesh et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Additional information: Use policy The full-text may be used and/or reproduced, and given to third parties in any format or medium, without prior permission or charge, for personal research or study, educational, or not-for-prot purposes provided that: • a full bibliographic reference is made to the original source • a link is made to the metadata record in DRO • the full-text is not changed in any way The full-text must not be sold in any format or medium without the formal permission of the copyright holders. Please consult the full DRO policy for further details. Durham University Library, Stockton Road, Durham DH1 3LY, United Kingdom Tel : +44 (0)191 334 3042 | Fax : +44 (0)191 334 2971 https://dro.dur.ac.uk McCreesh et al. Parasites & Vectors 2014, 7:503 http://www.parasitesandvectors.com/content/7/1/503 RESEARCH Open Access Effect of water temperature and population density on the population dynamics of Schistosoma mansoni intermediate host snails Nicky McCreesh1*, Moses Arinaitwe2, Wilber Arineitwe2, Edridah M Tukahebwa2 and Mark Booth1 Abstract 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. Keywords: Schistosomiasis, Schistosoma mansoni, Biomphalaria, Malacology, Climate change, Ecology Background It is crucial, however, to consider the species of intermedi- Mathematical models of water temperature and the life- ate host snail found in an area when parameterising a cycles of schistosomes and their intermediate host snails model, and when using the model to make predictions of can be used to gain valuable insight into the possible ef- the potential effects of environmental change on schisto- fects of environmental changes, including climate change, some transmission [5,6]. To accurately represent a snail on the distribution and intensity of schistosomiasis [1-4]. species in these models, it is necessary to have a wide range of data. This includes data on mortality, egg produc- tion, egg hatching and juvenile development rates at a * Correspondence: [email protected] 1School of Medicine, Pharmacy and Health, Durham University, Durham DH1 range of different temperatures. Experiments determining 3LE, UK the effects of other abiotic factors (e.g. the chemical Full list of author information is available at the end of the article © 2014 McCreesh et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. McCreesh et al. Parasites & Vectors 2014, 7:503 Page 2 of 9 http://www.parasitesandvectors.com/content/7/1/503 composition of the water) on different life stages of the clean the water, and water pumps were used to oxygen- snails will also advance model development. Currently, ate it. Pumps were set to a speed which did not disturb sufficient data are only available to accurately parameterise the snails. Larger particles of waste were removed from models of temperature and snail ecology to three species the base of the aquariums each week using a section of of Biomphalaria: B. pfeifferi, B. alexandrina,andB. glab- hose and suction, and the small volumes of water removed rata [6], and (with the exception B. alexandrina in South were replaced with aged tap water. This procedure, in Sudan) only one of these species can be found in sub- conjunction with the water filters, kept the aquarium Saharan Africa [7], where the majority of schistosomiasis water clean and prevented the need to periodically replace occurs [8]. While B. pfeifferi is generally considered to be large volumes of water. Additional calcium was added to the most important S. mansoni intermediate host in sub- the water in the form of crushed snail shells contained in Saharan Africa due to its widespread distribution [9,10], a fine mesh bag. Two pieces of expanded polystyrene foam other species are also important in maintaining transmis- were placed into each aquarium to provide a surface on sion in many areas. This is particularly the case for lake- which the snails could lay eggs. side areas in eastern Africa, where prevalences and Wild, adult B. sudanica snails were collected from intensities of intestinal schistosomiasis are often very high Lake Albert in western Uganda and transported to a la- [11], and where B. pfeifferi are not commonly found in boratory in Kampala. They were kept in aquariums at large numbers [9,12-14]. ambient temperature (approximately 25°C) for a mini- A critical decision in the design of mathematical mum of a week to acclimatise, before being used in ex- models of snail population dynamics is how to incorpor- periments. Snails that shed cercariae of any species were ate density dependent regulatory factors. In the absence discarded. The shell diameters of the remaining snails of these factors, simulated snail populations can increase were measured at the widest point using digital callipers, exponentially. This is clearly unrealistic, as wild snail and the shells of the snails were individually marked populations are limited in number by constraints such using queen bee markers affixed with nail varnish. It has as food availability. Density-dependent factors can be in- previously been shown that small quantities of nail var- corporated into models in two main ways: by increasing nish applied to the shell is not detrimental to the snails mortality rates and/or by decreasing fecundity as dens- [20,21]. The snails were then placed into the five aquar- ities increase. Laboratory experiments suggest that the iums in equal numbers. The aquariums were kept at am- fecundity of B. pfeifferi, B. alexandrina, and B. glabrata bient temperature for two days to allow the snails to tends to drop in unfavourable conditions, with little acclimatise, after which the water was gradually heated increase in mortality rates [15-18]. It is unclear if this is or cooled to the desired temperature. Snails were fed the case in more natural environments, or for other spe- with dried lettuce and spirulina cyanobacteria, which cies of Biomphalaria. were added to the water as a powder. In this paper, we describe laboratory and field experi- Two sets of experiments were conducted. In the first, ments conducted with two species of Biomphalaria: B. heaters and coolers were set to keep the five aquariums sudanica and B. stanleyi. B. sudanica is found in lakes at constant temperatures of 15°C, 19°C, 23°C, 27°C, and and rivers throughout central and eastern Africa, and is 31°C, and 91 snails were initially added to each aquarium. particularly common in Uganda [7,9]. B. stanleyi has a In the second, the heaters and coolers were set to 13°C, more limited distribution, and has been found in Lake 17°C, 21°C, 25°C, and 29°C, and 99 snails were added.
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