Invasion and Dispersal of Biomphalaria Species: Increased Vigilance Needed to Prevent the Introduction and Spread of Schistosomiasis

Biological invasion is a matter of great concern from both public health and biodiversity perspectives. Some invasive snail species may trigger disease emergence by acting as intermediate hosts. The geographic distribution of Schistosoma mansoni depends on the presence of susceptible species of Biomphalaria freshwater snails that support the parasite's transformation into infective stages. Biomphalaria spp. have shown strong local and global dispersal capacities that may increase due to the global warming phenomenon and increases in the development of agricultural and water projects. Should intermediate hosts become established in new areas then this will create potential transmission foci. Examples of snail invasions that have had an impact on schistosomiasis transmission include the introduction of Biomphalaria tenagophila to Congo and B. glabrata to Egypt. The current spread of B. straminea in China is causing concern and needs to be monitored closely. An understanding of the mode of invasion and distribution of these snails as well as their experimental susceptibility to S. mansoni will predict the potential spread of schistosomiasis. Here we review the invasion patterns of Biomphalaria snails and factors that control their distribution and the impact that invasion may have on intestinal schistosomiasis transmission. In addition, we propose some possible surveillance responses for optimum control strategies and interventions. Whenever possible, swift action should be taken to contain any new occurrence of these intermediate snail hosts.

Biological invasion is a matter of great concern from both public health and biodiversity perspectives. Some invasive snail species may trigger disease emergence by acting as intermediate hosts. The geographic distribution of Schistosoma mansoni depends on the presence of susceptible species of Biomphalaria freshwater snails that support the parasite's transformation into infective stages. Biomphalaria spp. have shown strong local and global dispersal capacities that may increase due to the global warming phenomenon and increases in the development of agricultural and water projects. Should intermediate hosts become established in new areas then this will create potential transmission foci. Examples of snail invasions that have had an impact on schistosomiasis transmission include the introduction of Biomphalaria tenagophila to Congo and B. glabrata to Egypt. The current spread of B. straminea in China is causing concern and needs to be monitored closely. An understanding of the mode of invasion and distribution of these snails as well as their experimental susceptibility to S. mansoni will predict the potential spread of schistosomiasis. Here we review the invasion patterns of Biomphalaria snails and factors that control their distribution and the impact that invasion may have on intestinal schistosomiasis transmission. In addition, we propose some possible surveillance responses for optimum control strategies and interventions. Whenever possible, swift action should be taken to contain any new occurrence of these intermediate snail hosts.
Keywords: Biomphalaria, invasion, Schistosoma mansoni, schistosomiasis, transmission BACKGROUND Aquatic invasion by exogenous species can cause native biodiversity loss and deleterious environmental and economic impacts (1). Biological invasions of gastropod molluscs have been strongly linked to serious problems to human health. They can cause expansion, emergence, or re-emergence of infectious diseases (2). These risks are anticipated to intensify due to ongoing climate change and global warming which continue to create new suitable freshwater environments for snail species serving as disease carriers (3). This review will consider the invasion patterns of Biomphalaria spp. (Class: Gastropoda; Family: Planorbidae) that act as the intermediate hosts for Schistosoma mansoni, a trematode parasite causing intestinal schistosomiasis. Biomphalaria are widely distributed in sub-Saharan Africa, South America, and other subtropical regions. Several species of Biomphalaria have shown strong local or global dispersal capacities. Numerous accidental or deliberate introductions of Biomphalaria spp. have been reported in tropical areas (4). Biomphalaria dispersal is of prime interest because it is often associated with the creation of new transmission foci for schistosomiasis. B. glabrata, B. straminea, B. tenagophila, and B. pfeifferi are the most common invasive species that have been introduced into new areas outside their native habitats and acted as potential intermediate hosts for schistosomiasis transmission (5). Therefore, an extensive knowledge of the geographic distribution of susceptible species of Biomphalaria is of considerable importance for the control of schistosomiasis and its epidemiologic surveillance as well as for future delineation of potential risk areas.

GEOGRAPHIC DISTRIBUTION OF SUSCEPTIBLE SPECIES OF BIOMPHALARIA
The global distribution map of S. mansoni is largely defined by the occurrence of Biomphalaria species that are able to transmit the parasite. According to DeJong et al. (6), there are 34 species of Biomphalaria distributed worldwide. Looking back at the long evolutionary history of Biomphalaria spp. it is clear that invasions into new geographical areas have been a regular feature. Molecular evidence suggests that a B. glabrata like taxon, South American in origin, dispersed across the Atlantic to Africa and gave rise to the African species possible quite recently in the Plio-Pleistocene (1.8-3.6 Myr ago). This West to East transoceanic dispersal could have occurred in the feathers of aquatic birds or on vegetation rafted across the ocean followed by successful colonization (7  (34). In addition to the geographic areas mentioned above for naturally infected snails, Biomphalaria spp. are widely distributed in many other wetland areas throughout the Americas and Africa (Figure 1 and Table 1).

ECOLOGICAL FACTORS CONTROLLING BIOMPHALARIA ABUNDANCE AND DISTRIBUTION
Many ecological or environmental factors regulate the distribution and abundance of Biomphalaria spp. The high fecundity of Biomphalaria and their ability to self-reproduce are important traits that support their successful invasion. Adult snails can produce 10,000 eggs per year. The egg-to-egg period requires approximately 11 weeks (127). With a life span of up to one year and a half, Biomphalaria can undergo several generations over a year (128). Following embryonic hatching from egg capsules, Biomphalaria undergo a series of developmental steps leading to maturation and reproduction. The snail has a great capacity to live and reproduce under different environmental conditions (129,130). B. glabrata and B. straminea, for example, were found in 10 of 11 different types of aquatic habitats in Brazil (131).
In natural habitats, Biomphalaria are under the influence of several ecological factors that control the population density of snails although temperature is a key determinant. Detailed review of environmental factors conditioning the habitat of Biomphalaria can be found in Malek (132), Brown (15), and Rollinson (133). In summary, these ecological factors can be divided into biotic and abiotic factors.

Biotic Factors
Biotic factors such as plants and food supply have a particular influence on the local abundance and distribution of snails. Predator and competitor species such as other species of snails, fish and insects also control snail populations. Data from field studies in Africa and Brazil indicate that Tilapia fish and some Dipteran insect's larva are predators of Biomphalaria in fishponds and lakes (134). In some cases, the absence of these natural predators may have a detrimental impact on schistosomiasis transmission. For example, the construction Diama Dam on Senegal River Basin obstructed the annual migration of native river prawns, Macrobrachium vollenhoveni, that feed on schistosomes intermediate host snails, leading to massive outbreak of schistosomiasis. Indeed, field experiments showed that reintroduction of the prawns caused a significant reduction in infected snails and human schistosomiasis prevalence (135,136). Moreover, several pilot control studies involving competitor snails, such as Pomacea glauca, Marisa cornuarietis, Melanoides tuberculata, and Helisoma duryi, achieved varying results; characterized mostly by ecological upsets after initial snail reductions (137,138).

Abiotic Factors
Abiotic factors, such as temperature and water chemistry, can have evident effects on Biomphalaria spp. over short distances within a single waterbody (15). In particular, temperature is important for snail survival and reproduction. Variation in water temperature affects distribution of snails not only from season to season but also from year to year (139). Recent studies on the effects of temperature changes on the growth, fecundity and survival of intermediate host snails of schistosomiasis and schistosomes prevalence indicated that temperature increase may alter the distribution, breeding, growth and survival of snails, and consequently may increase the  spread of schistosomiasis (140)(141)(142). In Egypt, high temperatures appear to reduce snail breeding and March is the month of maximal breeding for B. alexandrina (143). Yousif et al. (144) found that B. alexandrina populations exhibited two peaks of populations density that differ in heights depending on the extent of water temperature and winter closing. The first peak is from April-May and the second is from November-December. These two peaks are permeated by two lows following the Winter Closure and during the hot summer season. Under laboratory condition, B. alexandrina has optimal growth and egg laying at 26-28 • C (145). A similar temperature range was also found with B. glabrata (146). Also, a positive correlation was observed between B. sudanica abundance and water temperature (22). Appleton et al. (147) observed a negative correlation between fecundity and increasing above-optimal temperatures (>27 • C) during maturation period of B. pfeifferi. The authors concluded that the change in temperature regime is responsible for the species' absence from pans in some areas of South-Eastern Africa due to the sensitivity of B. pfeifferi to high temperature. Furthermore, the distribution of B. pfeifferi and B. sudanica is limited to north and north-eastern parts of Uganda characterized by suitable temperatures (148). Temperatures higher than optimal values cause retardation in the development of gonads and albumen gland and a decrease in egg-production and viability. Water chemistry is an important factor for snail distribution (149). For example, inorganic salts govern the osmotic properties of the aquatic environment, which in turn are linked to the sensitivity of snail eggs to salinity. Most common ions in natural water include calcium, magnesium, sodium, bicarbonate, carbonate, chlorine, and phosphate. Snails usually prefer environments rich with calcium. The presence of calcium in water is important for snails since it is essential for the construction of the shells (150). Studies on B. pfeifferi showed that the snail is restricted to water with a minimum calcium concentration of 5 mg/l. High ratios of magnesium/calcium and sodium/calcium indicate low bioavailability of calcium and exert a negative impact on the egg production of the snails and can reduce their densities (151). Calcium has been associated with high fecundity of B. glabrata (149). El-Khayat et al. (152) showed that the habitat preferred by B. alexandrina snails contained higher concentration of various common ions such as potassium, sodium, and calcium. Also, field studies by Kloos et al. (35) showed that the widespread distribution of B. glabrata, and its infection with S. mansoni, together with differences in the seasonal distribution of snails is correlated to high calcium levels that appear to promote large B. glabrata populations in wells and springs.
Other environmental conditions such as turbidity and water pollution have an influence on snail abundance. Becker et al. (153) found that turbidity and pesticide pollution, at concentrations similar to or higher than those considered safe in environmental risk assessment, are significant factors in increasing the incidence of B. pfeifferi and Bulinus africanus, the intermediate host for Schistosoma haematobium, the parasite responsible for urogenital schistosomiasis, and hence the likelihood of schistosomiasis transmission. Declines in snail competitors and predators, that are less tolerant to pesticides, increase the availability of food for intermediate snail hosts and decrease their mortality rate (154).

INVASION PATTERNS Long Distance (Global) Dispersal
There are four cases of long-distance dispersal present in the literature; one case was reported for B. straminea (Caribbean islands, China), one for B. glabrata (Egypt), and two cases for B. tenagophila (Romania and Congo).
The dispersal of both B. glabrata and B. tenagophila (Congo) was implicated in local schistosomiasis transmission (Figure 2).

Biomphalaria straminea
B. straminea, one of the intermediate hosts for S. mansoni in South America, expanded its geographic range to colonize almost all the Caribbean islands (155). In Asia, B. straminea was first identified in Hong Kong water systems in the south of China in 1974 (50), in the subsequent years, the snails showed a dispersal capacity in different water courses in southern China. The snail species was found in numerous water bodies in Shenzhen city of Guangdong province, China in 1981 (156), and in the next 2 years showed a growing distribution in Shenzhen rivers, suggesting a spread from Hong Kong rivers systems (52).
Morphological and molecular study for seven populations of Biomphalaria snails collected in Guangdong indicated that five populations were closely related to B. kuhniana, another South American species refractory to schistosomes infection, the other two populations were identified as B. straminea and were more relative to B. straminea from Brazil (157). Controversially, further anatomical and molecular investigation of six Biomphalaria populations from Guangdong showed a close affinity between these populations and B. straminea from Brazil (158). Supporting the latter finding, a more recent study of B. straminea in Hong Kong identified two morphotypes of the species; black-and red-colored shell morphs of B. straminea in different districts in the new territories in Hong Kong, including places close to the mainland China border. Morphological and molecular analyses of the Hong Kong B. straminea showed that they are genetically indistinguishable and are similar to those obtained in mainland China and South America (159). The presence of B. straminea in Guangdong may be the result of multiple and different introduction routes and/or peripheral dispersal from Hong Kong populations via passive transport or container ship traffic or naturally due to connections between the water systems of the two adjacent localities (160).
The spread of B. straminea from Hong Kong to Guangdong confirms its ability to survive and form new colonies in mainland China and its capacity to spread along the rivers (161). B. straminea can adapt to drought periods and higher temperatures, an adaptability that will promote its spread to wider geographic areas in China in view of global warming and continued rise in the mean annual temperature of China (162). Further evidence is the recent invasion of the snail to Guanlan and Dasha rivers in Shenzhen city, Guangdong province, China (53). Moreover, recent maps for realized (Figure 3) and predicted spatial distributions of B. straminea in southern China, based on Geographical Information Systems (GIS) and species distribution modeling software (MaxEnt), showed the presence of B. straminea in many water habitats in Guangdong province and indicated possible suitable habitats in its surrounding provinces such as Guangxi and Fujian (163).  (167) suggesting a recent contact with areas manifested with infected Biomphalaria. This merits further molecular analysis for Egyptian populations of Biomphalaria using mitochondrial and genomic sequences to identify species involved in S. mansoni transmission and to understand their role and biology of infection.

Biomphalaria tenagophila
The invasion of Neotropical snail B. tenagophila to Africa was reported from Kinshasa, Democratic Republic of Congo as confirmed by conchological, anatomical, and molecular studies. It was proposed that this species was introduced at the end of the 1960s (5). In Europe, B. tenagophila snails had been found in 2004 at Rȃbȃgani, Romania, Eastern Europe but had been misidentified as the common European species, Planorbarius corneus (168). In the period between 2005 and 2007, the snail was collected from the same location and its identity was confirmed via morphological and molecular characterization that proved it as B. tenagophila. Molecular data obtained from partial mitochondrial 16S ribosomal RNA gene amplification showed 99.74% similarity to B. tenagophila originated from Brazil. B. tenagophila is not only introduced, but also established in Rȃbȃgani area in Romania. The snail's route of introduction is unknown but it is more likely to be introduced through migrating birds or by plants used in aquariums (66).

Peripheral Dispersal
Continued modifications of humans to aquatic environments through constructions of major reservoirs and hydroelectric dams and expanding irrigation schemes, quarries, drainage ditches, and aquaculture ponds, improve and create new freshwater bodies and potential snail habitats. Biomphalaria spp. rapidly colonize and establish dense populations in such habitats, which in turn facilitate schistosome transmission leading to disease outbreak (136,(169)(170)(171). Snails can be passively dispersed by floating aquatic plants or by human activities over the same lakes and rivers. For example, the invasive floating plant Salvinia was responsible for B. pfeifferi colonization in Lake Kariba in Zambia (172). Passive dispersal of Biomphalaria can also be delivered by water currents both during flooding, where water velocity is high so it sweeps away adhering snails, and also by slower drifting because of the habit of most pulmonates to detach and rise to the surface looking for food or as a deliberately dispersive behavior. In an experiment by Dazo et al. (143) they found that Biomphalaria and Bulinus were recovered as far as 4 km downstream after 1 day following release into a vegetationfree canal flowing rapidly at 0.42 ms −1 . Field observations from some localities in Brazil indicate that seasonal distribution of B. glabrata is characterized by generally lower snail densities in stagnant waters during the dry season however, higher densities in streams and canals during that time appear to be determined largely by the reduction of stagnancy through the addition of rainwater in the former and the flushing out of snails by seasonally increased water velocity in the latter (35). Many records of peripheral dispersal of different Biomphalaria spp. in many countries are found in the literature.

CONSEQUENCES OF INVASIONS Supporting Transmission of S. mansoni
The problem with invasion of Biomphalaria susceptible to schistosomiasis is that one snail can undergo self-fertilization and act as a founder of an entire colony. Because an individual snail carries only part of the total genetic variation of its original population, the colonies established by the recent dispersal of that snail or even a small group of snails are expected to show reduced genetic diversity compared with their parental population (173). For example, B. alexandrina lost allelic diversity at several polymorphic loci after colonizing the Upper Nile in Egypt coming from the Nile Delta region (173). Increased genetic diversity of Biomphalaria tends to reduce the overall parasite transmission rate, supposedly due to a dilution effect where in the presence of high genetic diversity it is more likely that some snails are naturally resistant to Schistosoma infection, whereas reduced host genetic diversity could benefit S. mansoni through an overall increase in transmission rate (174).
Following the introduction of B. tenagophila to Kinshasa, Congo in 1970, S. mansoni infected specimens were collected from the same area indicating the involvement of the snail in S. mansoni transmission and not a native African Biomphalaria (76,175). This finding was confirmed based on a previous experience from Brazil where the first transmission site of S. mansoni through using B. tenagophila as intermediate host was discovered in the Paraiba valley, state of São Paulo. In the subsequent years, schistosomes showed a great adaptation to the new intermediate host and further spread throughout the valley (8).
B. pfeifferi has also been implicated in the increased prevalence of intestinal schistosomiasis in many countries following an extension of its distribution as exemplified by the rise of the disease in Malagasy high plateau, Madagascar after its colonization by B. pfeifferi (176,177). In Egypt, B. glabrata was reported in long distances of water courses in Qalyoubiya, Giza, and Kafr El-Sheikh governorates (44,46). Although no infected snails were collected, laboratory studies on the first generation obtained from field-collected specimens showed its susceptibility to a local strain of S. mansoni originally from Giza. The infection rate of B. glabrata snails was lower than that of B. alexandrina. Also, the incubation period was considerably shorter in B. alexandrina than B. glabrata which reflects the higher compatibility of the indigenous snails to local parasites. However, total number of cercariae produced per snail throughout the shedding period was higher in B. glabrata than in B. alexandrina. The results of experimental infection indicated that B. glabrata is as efficient as B. alexandrina in transmitting local S. mansoni parasites (46). The situation of B. glabrata became more complicated because the snail was able to hybridize with the local B. alexandrina snails producing a susceptible hybrid lineage. Some of the hybrid snails collected from El-Gharbia, El-Behierah, El-Menia, Kafr El-Sheikh, Dakahlia, and Alexandria governorates were found naturally infected with S. mansoni (45). Field and laboratory studies suggested that B. glabrata and hybrid snails have a higher potential in transmitting S. mansoni, which could lead to an increase in schistosomiasis in associated communities (178).
The invasion of Upper Egypt with B. alexandrina following the construction of the High Dam has led to outbreaks of S. mansoni, with tremendous local increase in the prevalence levels in just a few years (179). Also, as a consequence of B. alexandrina introduction to newly reclaimed areas, epidemiological surveys on resident and settler populations showed 49.3% and 40% prevalence of S. mansoni in El-Manayef and El-Morra areas, respectively in Ismailia governorate. The seasonality of Biomphalaria infection in the new areas showed the presence of two peaks in August and November. These results confirmed the occurrence of transmission of S. mansoni which indicated that reclamation of parts of the desert using the Nile water had led to spread of schistosomiasis to these areas (45).
In Northeastern Brazil, a competitive displacement of B. glabrata by B. straminea occurred after the introduction of the latter species. This displacement was considered as a biological control measure since the introduced snails were thought to be resistant to S. mansoni infection and have a greater fecundity (180). However, field data from some endemic areas showed that human infection increased from 35.5 to 61.9% in the locality occupied by B. straminea, and decreased from 40.3 to 20.8% in that occupied by B. glabrata. These data suggest that B. straminea is involved in the transmission of schistosomiasis (181).
Transmission of schistosomiasis can't occur in the absence of a competent intermediate host snail, but once the obligate host has established, schistosomiasis transmission becomes a possibility (2). Although no schistosome larvae have been detected in B. straminea or B. tenagophila introduced to China and Europe (Romania), respectively, there is still a risk for intestinal schistosomiasis to be locally transmitted into these new geographic zones. The two species are susceptible intermediate host for S. mansoni and have been implicated in intestinal schistosomiasis transmission in their native habitats. Thus, global climate change and the possibility of the introduced snails to be in contact with schistosomes, could pose a public health risk. Human travel between countries for business, education or tourism made it possible to find schistosomiasis cases in non-endemic areas (182). For example, many reports of S. mansoni infected cases in immigrants or tourists visiting Romania and neighboring Hungary were reported (183). Also, more than 400 imported cases infected with African schistosomes (including S. mansoni and S. hematobium) were reported from numerous provinces in China between the years 1979 and 2011, owing to the sharp growth in China aided projects in Africa and labor services exported to Africa. It is estimated that over 1 million Chinese workers are now residing in Africa, increasing the risk of exposure to African schistosomiasis (160). Other possible ways of S. mansoni establishment include the introduction of infected snails in the same way by which uninfected ones were introduced and introduction of the parasite through Chinese or European laborers returning from endemic areas or visitors traveling for tourism or trade purposes. Once started it is possible that the life cycle could be maintained through other definitive hosts such as rodents.

Supporting Transmission of Other Helminth Parasites
In addition to its role as intermediate host for S. mansoni, Biomphalaria spp. may also act as intermediate hosts for other parasites of mammals, birds, and fish (Table 2). Moreover, different species of Biomphalaria were found naturally infected with cercariae and metacercariae of a wide range of trematodes of unknown life cycle (73,217). Recently, both B. straminea and B. glabrata were shown to act as intermediate hosts of Austrodiplostomum compactum (Trematoda: Diplostomidae), the causative agent for ocular diplostomiasis in several species of fish in Brazil, a disease which may have potential impacts on native fish species and damage to fish farming. The two species were found infected with strigeid cercariae of the parasite (208). Biomphalaria can also act as intermediate hosts for different species of the nematode Angiostrongylus that infect domestic animals as well as humans. For example, Angiostrongylus

Angiostrongylus siamensis B. glabrata
Experimental (216) vasorum, that parasitizes the right ventricle of the heart and the pulmonary artery of dogs and wild carnivores in different parts of Europe, Canada, South America, and Africa (218,219), is able to infect B. glabrata and B. tenagophila under laboratory conditions as evidenced by emergence of cercariae that could infect the vertebrate host (209,210). The parasite can also cause diseases of the central nervous system in humans (220). B. glabrata and B. tenagophila act as intermediate hosts for the rat lung worms Angiostrongylus cantonensis and A. costaricensis the causative agents of eosinophilic meningitis and meningoencephalitis and abdominal angiostrongyliasis, respectively, in humans in many parts of the world (221). Within the snails, the parasite develops into the infective third-stage larvae and humans are infected after ingestion of infected snails (222). Infection with the rodent schistosome S. rodhaini were found in natural population of B. sudanica in some African countries such as Uganda and Burundi (15). Moreover, natural infections with 11 larvae of different trematode species were found in B. pfeifferi and B. sudanica from Tanzania (223).

CONCLUSIONS
The distribution of the snails will define the potential distribution of schistosomiasis and the likelihood of transmission. Many ecological factors regulate distribution and abundance of Biomphalaria spp. Hence, knowledge of the disease transmission is incomplete without available information on the ecology and biology of this intermediate host.
There is a continuous need to document the changing and dynamic distribution of Biomphalaria due to continued environmental modifications and climatic changes. Long distance dispersal of Biomphalaria is achieved through accidental and/ or deliberate introduction to new geographic areas. Dispersal of snail eggs and uninfected snails will not spread schistosomes, but dispersal of infected snails can spread the disease. Moreover, the new species may enhance disease transmission if it is more susceptible to local parasite than sympatric intermediate hosts. Thus, understanding the geographical origins of introduced snails, their modes of dispersal, and their rates of gene flow might assist efforts to understand the spread and establishment of schistosomiasis in the area of introduction. More studies are needed to identify the introduced species and understand their biology and the combination of morphological and molecular methodologies will be the best approach.
Snail distribution data can be used to develop prediction models for potential schistosomiasis risk areas and risk maps for snail distribution and abundance using species modeling software. For this purpose, geographic coordinates should be collected for utilizing in GIS and remotely sensed data (224). The obtained risk maps can be used to apply the suitable public health strategies, and to guide other fieldwork. Also, the risk map will enable better resource distribution and adequate policies for snail control. The GIS approach is particularly recommended to provide estimates of the potential spread of invasive Biomphalaria species using data of occurrences through time that allow a functional estimation of the spread of the invader, which could then be related to rates of ecological changes and vector activity over time.
For better and effective control initiatives for schistosomiasis, periodic malacological surveys are recommended for the detection of Biomphalaria in new potential habitats and identification of species and infection status of collected snails. Swift actions should be taken to record any new occurrence of these snail intermediate hosts. Community education is another important intervention to aid control. Populations who are in contact with water for agricultural or other purposes should be able to morphologically identify schistosomiasis intermediate snail hosts and understand their role in disease transmission. A surveillance system could be established to monitor the distribution of snails. This system could be used to assist regional policies in controlling snails via application of molluscicides or other control approaches (225,226).

AUTHOR CONTRIBUTIONS
MRH, DR, and X-NZ: conceived and designed the study, and wrote and edited the review. MRH, DR, and SL: data collection and interpretation. All authors read and approved the final manuscript.   (91)