The impact of river flow regulation and manipulation on the invertebrate hosts of malaria, bilharzia and liver fluke disease LM Quayle, CC Appleton & CWS Dickens TT 456/10 The effects of stream flow manipulation on the invertebrate hosts of malaria, bilharzia and liver fluke disease. L M Quayle, C C Appleton and C W S Dickens Report to the Water Research Commission by Institute of Natural Resources WRC Report No. TT 456/10 June 2010 Obtainable from: Water Research Commission Private Bag X03 Gezina, 0031 South Africa [email protected] The publication of this report emanates from a project titled The effects of stream flow manipulation on the intermediate hosts and vector populations of disease and the transmission of the associated parasites (WRC Project No. K5/1589) Disclaimer This report has been reviewed by the Water Research Commission (WRC) and approved for publication. Approval does not signify that the contents necessarily reflect the views and policies of the WRC, nor does mention of trade names or commercial products constitute endorsement or recommendation for use. ISBN 978-1-77005-980-1 Printed in the Republic of South Africa Executive Summary Introduction The regulation of rivers is known to cause a number of changes to the function and form of rivers. According to Davies and Day (1998), the river continuum concept describes the river as a single longitudinal ecosystem with component variables that act as drivers eliciting responses from other variables (response variables). The flow regime in a river is one such ‘driver variable’. Regulation of the flow in a river alters the nature of this important driver, and thus alters the responses elicited in the more reactive variables (for example geomorphic form of the river channel, range of in-stream habitats or biota assemblages). Almost every major river in South Africa has been regulated to a certain degree, largely to meet the growing needs of development (Davies et al., 1993 – as reported in the State of the Environment report 2007). This report aims to assess the current state of knowledge concerning the relationship between river flow regulation and its effects, and the population dynamics of the invertebrate hosts of malaria, schistosomiasis (bilharzia) and fascioliasis (liver fluke disease) in South African rivers. The habitat requirements of these invertebrates will be central to this discussion. Additionally, the concept of using the manipulation of flows to control these invertebrates and thus also the transmission of their associated diseases is addressed. Definition and review of the invertebrate hosts and routes of parasitic transmission in the natural environment. Malaria Four species of malaria parasite occur around the world. Plasmodium falciparum P. ovale P. malariae P. vivax Plasmodium falciparum is the most common in South Africa and is also the most pathogenic. All four of these parasites can be transmitted by 28 of the approximately 200 species of Anopheles mosquitoes found around the world. The most important species for malaria transmission in South Africa are Anopheles funestus and Anopheles arabiensis. The distribution of An. funestus has been reduced significantly by spraying of insecticides, leaving An. arabiensis as the most important malaria vector in South Africa. Anopheles arabiensis is an opportunistic breeder which uses different habitat types in summer and in winter (le Sueur, 1991). During winter they use overflow and seepage irrigation water and the vegetated margins of larger water bodies, where submerged plants protect the larvae from predators. During summer, they use temporary rain-filled, sunlit pools that are typically un-vegetated and can be man-made such as vehicle wheel tracks or cattle hoof prints. I | Page Anopheles funestus breeds in larger, more permanent water bodies with emergent vegetation such as swamp margins and streams. Research in Kenya suggests that they are found breeding mainly in stable stream pools (Mwangangi et al., 2007). Schistosomiasis (bilharzia) Worldwide, 30 species of schistosome (blood flukes) parasitize mammals, and an even larger number parasitize water fowl. Seven of these are known to parasitize people, of which two species commonly infect people in South Africa, Schistosoma haematobium which causes urinary bilharzia, and S. mansoni which causes intestinal or rectal bilharzia. Both of these parasites’ life cycles involve two hosts, a warm blooded vertebrate final host (humans) and an invertebrate intermediate host which is an aquatic snail. Most, if not all of the schistosome parasites of birds are known to penetrate human skin, but they do not develop further and when they die, they cause a rash known as ‘swimmers itch’. In South Africa, S. haematobium has two intermediate snail hosts, Bulinus africanus and the closely related Bulinus globosus. S. mansoni uses Biomphalaria pfeifferi as its snail host. Transmission of these parasites can take place in any water body where these snails occur and with which people have contact. Schistosome eggs are released into the water from the human host through urine (S. haematobium) or through faeces (S. mansoni). The eggs hatch and the motile miracidium seeks out and penetrates its snail intermediate host. Inside the snail, asexual division takes place resulting in the production of cercariae, which leave the snail at the rate of hundreds per day in a diurnal rhythm designed to coincide with the swimming activities of children. The cercariae penetrate the human host through the skin and make their way to the liver where they mature into adult worms. They then pair up and make their way to the vessels draining their final target organs where they begin to produce eggs (S. haematobium – bladder, S. mansoni – lower intestine or rectum). The invertebrate hosts of S. haematobium are generally found in permanent, slow moving water bodies. Bulinus africanus is found over much of the eastern half of the country as far south as the Kromme river in Humansdorp, while B. globosus is limited to the extreme eastern parts of Limpopo and Mpumalanga provinces and to a small area of north-eastern KwaZulu- Natal. Both species are vulnerable to desiccation and their intrinsic rate of increase is considered relatively low (De Kock et al., 2005) but is strongly linked to temperature. Indeed temperature and water body type or flow rate appear to be the major factors determining the distribution of the Bulinus group. Biomphalaria pfeifferi, the intermediate snail host of S. mansoni, is also generally found in still or slow moving permanent water bodies. This species is particularly vulnerable to desiccation and thus is unlikely to be found in temporary rain filled habitats. Its distribution is similar to that of B. africanus, but does not extend further south than Port St Johns. Like the Bulinus species, this snail’s distribution is mostly influenced by water body type and temperature. Fascioliasis (liver fluke disease) Fascioliasis is caused by two species of trematode – Fasciola hepatica and F. gigantica. Very little is known about the epidemiology of fascioliasis in South Africa, though the vast majority of infections are in fact in wild animals and livestock. Infections of humans are extremely rare in South Africa. II | Page Both species use freshwater snails as intermediate hosts. Fasciola hepatica uses Lymnaea truncatula, and F. gigantica uses Lymnaea natalensis. The invader species L. columella may also play a role in the transmission of the parasites, but this is unproven in South Africa. Lymnaea truncatula is an amphibious species, found characteristically on damp mud around temporary habitats such as swamps, bogs, irrigation ditches and drains. Its preference for cooler humid areas means it is most abundant in high lying areas such as Lesotho and northern parts of the Eastern Cape. It can reportedly aestivate up to 12 months (Kendall, 1965). Lymnaea natalensis is widespread across South Africa, and unlike L. truncatula, is completely aquatic. It is thus mostly found in permanent larger bodies of water. Temperature appears to have less of an effect on the distribution of this species, and water body type appears to be the most important determining factor. Important habitats Water body type appears to play an important role in determining suitability of a particular habitat for the invertebrate hosts of the three diseases. This includes the rate of flow. Since mosquito larvae are unable to resist flow, adults particularly seek out still water in which to breed. Snails are also vulnerable to higher flow velocities and Appleton (1978) identified current velocity as the abiotic factor most influential in determining the distribution of host snails in flowing waters, with snails unable to resist flows of greater than approximately 0.3 ms-1. Several other authors have expressed similar views regarding the limiting effect of stronger currents (De Kock et al., 2004; Brown, 1994; O’Keefe, 1985) Temperature also plays a large part in determining habitat suitability. Temperature is documented as being one of the most important factors influencing Anopheles mosquito distribution (Coetzee et al., 2000). Water temperature plays an important role in determining the fecundity of snails, and with the exception of L. natalensis, all species reviewed appear to be temperature sensitive. Temperature also plays a role in the development of the parasites within the snail, a fact which may limit the transmission of the disease in cooler parts of the country during colder months (Moodley