Establishment of an invasive snail Melanoides tuberculata (Müller, 1774) in a Sahelian urban reservoir in Ouagadougou, Burkina Faso

Human land-use plays an important role in the distribution of aquatic invasive species. The establishment of these species may have an unpredictable impact on their new environment. We analyzed the establishment of M. tuberculata, an invasive species, and its effect on the mollusc community in Ouagadougou’s reservoir No.3. Mollusc samples were collected using an Ekman grab through sampling points randomly distributed across the whole reservoir. Collected specimens were sorted, preserved in alcohol at the field site and transported to the laboratory for identification. Species diversity, abundance and distribution were analyzed. Among the five species encountered, M. tuberculata and L. varicus were identified for the first time in this reservoir. M. tuberculata had the highest relative abundance (60.83%) and the highest density. The evenness was less than 0.5 for 72.5% (i.e. 21) of sampling points, reflecting the relative dominance of a single species, M. tuberculata . In terms of spatial distribution, the most widespread species in the study reservoir was M. tuberculata , followed by C. aegyptiaca and B. unicolor. M. tuberculata distribution in the reservoir mostly overlaps that of B. unicolor (0.45). Renewed monitoring efforts are needed to better understand the evolution of mollusc species in freshwaters of Burkina Faso to understand species extinction risks as well as the potential use of mollusk diversity measures as water quality indicators.


Introduction
Disturbance and anthropogenic land use changes are key factors facilitating biological invasions (Schreiber et al. 2003). Invasive alien species (IAS) are among the stressors which threaten both ecosystem biodiversity and integrity. Over the past decade, there has been an increase in research focusing on the impacts of invasive species. Some studies have shown that the increased abundance of invasive species in an environment affects the richness and abundance of native species (Gallardo et al. 2016;Cameron et al. 2016). The increased abundance of invasive species can hinder ecosystem functioning and the provision of ecosystem services (Vilà and Hulme 2017; OPEN ACCESS. Castro-Díez et al. 2019) and increase the extinction risk for native species (Bellard et al. 2016;Blackburn et al. 2019). An increase in IAS affects the phylogenetic and functional diversity of invaded communities and food webs (Guareschi et al. 2021). Invasions by alien species can decrease phylogenetic diversity by replacing native species with closely related invaders, or by homogenizing the evolutionary history of the community (Young et al. 2017). This can reduce the overall resilience and adaptation potential of the community, making it more vulnerable to disturbances. Invasions can also decrease functional diversity by replacing native species that perform unique ecosystem functions with alien species that perform similar functions (Milardi et al. 2020). This can disrupt important ecosystem processes such as nutrient cycling and pest control, and lead to a loss of ecosystem services. In addition, invasive alien species can also disrupt food webs by preying on or out-competing native species, or by becoming predators or prey themselves (David et al. 2017). This can lead to changes in population dynamics and trophic interactions, and can have cascading effects on the entire food web. IAS in Burkinabé reservoirs include plants an animal which can impact native communities, be costly to the human economy, and carry diseases (Cowie and Robinson 2003). Schistosomiasis for example which is caused by a parasitic flatworm called Schistosoma can lead to absenteeism from school and work, decreased productivity, and increased healthcare costs. In addition, the disease can also lead to malnutrition, which can further reduce productivity (Cole and Neumayer 2006). One snail that is invasive in Burkina Faso, Melanoides tuberculata (Müller, 1774), is native to eastern Africa and the Middle East (Williamson 1981). Melanoides tuberculata, is known to be a vector for a number of parasitic species, including the trematode parasite genus Microphallus, Echinostoma and Plagiorchis. Microphallus for example infect the snail's reproductive organs and cause the snail to release infected eggs into the water. These eggs can then infect other snails or aquatic animals, such as fish, amphibians, and crustaceans. Based on 136 articles published between 1896 and 2010, Pinto and Melo (2011) have reported, on M. tuberculata, 37 species of flukes belonging to 25 genera and 17 families. Among them are 11 trematodes reported as adults from man. Their study also mentioned that the greatest proportion of the associations between M. tuberculata and flukes has been recorded in Asia and Africa.
As a vector and invasive species, Melanoides tuberculata may act for the introduction of alien parasite species in areas where it is not native. This generally occurs when the snail is introduced to a new ecosystem through human activities such as aquaculture, pet trade, or accidental transport (Santos and Eskinazi-Sant'Anna 2010;Preston et al. 2022). Once established, the snail can support the development and spread of its associated fluke parasites, which can then infect native aquatic animals and potentially cause harm to the ecosystem.
The first description of its distributional area extends from Africa to southeastern Asia (Pilsbry et al. 1927). It has since then invaded the whole inter-tropical area (Glaubrecht and Salcedo-Vargas 2000), including Benin and Cote d'Ivoire. Melanoides tuberculata is known to be a major pest in horticulture, particularly in areas where it is not native (Cowie et al. 2008). One of the main activities around the Reservoir No.3 of Ouagadougou is horticulture. Exotic plants are often imported and grown in this areas. A survey of a few horticulturists around the reservoirs allows us to hypothesize that this invasion may come from the importation of exotic plants. Prior to this study, neither the work of Ouedraogo (2015) or Kabore et al. (2016) mentioned the presence of this specie. In this paper, we show that M. tuberculata has further extended its range and successfully established itself in Burkina Faso.
Melanoides tuberculata reproduces mainly by parthenogenesis and sexual reproduction, with a resulting increase in genetic variance and/or heterosis effect (Samadi et al. 1999;Facon et al. 2005). This species is viviparous and juveniles are incubated in the female brooding pouch located in the head (Heller and Farstay 1989). The number of young within the brood pouch ranges from 1 to 70 depending on the size of the adult and on the morph considered (Livshits and Fishelson 1983). Reproduction rates are low when compared with pulmonate snails, but the survival of young snails tends to be very high (Pointier et al. 1991).
Melanoides tuberculata can rapidly colonize many types of habitats reaching very high densities up to several thousands of individuals per m 2 (Dundee 1977). It is a ubiquitous species that can tolerate a broad spectrum of environmental conditions and colonize disturbed habitats such as garden ponds, artificial lakes, and irrigation systems. Its reproductive strategy can produce new genotypes that may invigorate its invasive ability (Facon et al. 2008). In its introduced range, there are reports of M. tuberculata outcompeting native species, however, the consequences are not always negative often helping to reduce intermediate host populations.
In Burkina Faso, several reservoirs have been created to minimize the effects of drought during the dry season (generally from October to April). These reservoirs are also used to supply drinking water as well as other activities that include fishing, market gardening, horticulture, and washing, among others. Habitat availability and pollution are known to increase the abundance and diversity of snails in an ecosystem (Shea and Chesson 2002) and these factors are likely to explain the proliferation of M. tuberculata in reservoir No.3 of Ouagadougou. The presence of this IAS is of concern owing to the threat this poses to native species, aquatic ecosystem functioning, and human health because of its role in spreading zoonotic diseases. Because of the invasive and parasitic nature of M. tuberculata, analyzing its distribution and abundance in relation to the other molluscs in this reservoir is key of importance. For this reason, the present study highlights the establishment of M. tuberculata, and analyses the effect of this establishment on the mollusc community in the reservoir No.3 of Ouagadougou.

Study area
The study was conducted in reservoir No.3 of Ouagadougou in Burkina Faso (Figure 1). The reservoir covers a surface of around 88 ha with a capacity of 3 733 334 m 3 . It is located in the central part of the city, a densely populated urban area (1,829 people per square kilometer in 2019), receiving domestic and industrial discharges (including sewage) from neighboring houses. Upstream, this reservoir is connected to reservoir No.2 which in turn is connected to reservoir No.1. Downstream, the water from reservoir No.3 flows through the Bãngr-Weoogo Urban Park. These three reservoirs were created on the Kadiogo, which is connected to Massili, the biggest affluent of the Nakanbé river. The complex formed by the Bãngr-Weoogo Urban Park and the three reservoirs has been classified as a Ramsar Site (Ramsar Site No.2367) on 2 February 2019 (RAMSAR 2019). This forest, is a protected area and a hotspot of plant biodiversity and a refuge for different animal species. These reservoirs were originally used to supply the population of Ouagadougou with drinking water and are increasingly used for fishing, market gardening, horticulture, machine washing, etc.

Molluscs sampling and identification
A mollusc survey was carried out in February 2017 at reservoir No.3 of Ouagadougou. The bottom of the reservoir was not entirely covered with water ( Figure 2). Thirty-eight (40) sampling points randomly distributed across the whole reservoir were sampled using an Ekman grab. Captured specimens were sorted and preserved in ethanol (70% final concentration) at the field site. In the laboratory, mollusc specimens were identified using the following taxonomic guides: Mandahl-Barth (1978), Mandahl-Barth (1988), Leveque (1980), Brown and Kristensen (1993), and Brown (2002). A random selection of specimens were discussed in July 2017 with taxonomic experts at the Department of Animal Ecology and Systematics of Justus Liebig University, Giessen, Germany with Dr. Bert Van Boxclaer (Evo, Eco Paléo of CNRS and Université de Lille, France) and Dr. Christian Albrecth, to confirm identification.

Data analysis
Shannon Wiener Diversity (H') and Equitability Evenness (J) were calculated for each sampling point. H' range from 0 (low diversity) to 5 (high diversity) and J range from 0 (low evenness) to 1 (high evenness). Pie charts were used to represent relative species abundance. Species density refers to the number of individuals of a species found per unit of area (m 2 ). The distribution map  (Sarkar et al. 2015) packages. We used the R package spaa (Zhang et al. 2016) to calculate the Pianka index (Pianka 1973) which indicates niche overlap between the abundance of species pairs at each sampling point. Pianka values range from 0 (no habitat features used in common) to 1 (complete overlap).
At least one mollusc was found at each of the sampling points. The abundance of individuals per sampling point varied from 8 (minimum) to 664 (maximum). In terms of species richness, a single species was found in 27.5% (i.e. 11) of the sampling points; two species in 35% (i.e. 14 points); three species in 35% (i.e. 14), and four species at only one of the sampling points (Supplementary material Table S1).
The Shannon-Wiener index varied from 0 to 0.78, indicating that the species diversity by sampling point is relatively low. The Equitability evenness index could only be calculated for 29 sampling points where the species richness was greater than 1. The evenness was less than 0.5 for 72.5% (i.e. 21) of these points, reflecting the relative dominance of a single species (M. tuberculata).

Spatial distribution and niches overlap
In terms of spatial distribution, M. tuberculata was the most widespread species in the study reservoir, followed by C. aegyptiaca and B. unicolor. The distribution of B. unicolor overlapped entirely with that of M. tuberculata and C. aegyptiaca. However, C. aegyptiaca was absent over some areas occupied by M. tuberculata while other areas were occupied solely by C. aegyptiaca (Figure 2).
The Pianka ecological niche overlap index allowed us to see if the different mollusc species encountered in Ouagadougou reservoir No.3 use the same spaces or not (Table 1). The highest Pianka index value was observed between the two species of bivalves: M. rostrata and C. aegyptiaca (0.52). When analyzing the overlap of niches with the invasive species, M. tuberculata, the index was highest with B. unicolor (0.45), followed by L. varicus (0.28), and finally C. aegyptiaca (0.07).

Discussion
In comparison to the study conducted by Ouedraogo et al. (2015), where a similar survey of molluscs in Reservoir No.3 was conducted, the results of the current study show a change in the diversity and abundance of species ( Figures S1, S2). Among the five species identified in this study, M. tuberculata and L. varicus were not identified in Ouedraogo et al. (2015). In addition, C. bulimoides, which had been recorded by Ouedraogo et al. (2015), was not recorded in the present study. C. bulimoides and L. varicus densities were the lowest while the density of M. tuberculata was the highest of all species. In contrast, no specimens of M. tuberculata were reported in 2012 (Ouedraogo et al. 2015). This situation indicates that M. tuberculata emerged in reservoir No.3 between 2012 and 2017 and rapidly became the dominant species because conditions were favourable for its proliferation. As mentioned in the introduction, M. tuberculata is not native to Burkina Faso (Albrecht et al. 2018). It is an exotic freshwater gastropod species and one of the most successful colonizers and parthenogenetic mollusc species (Strong et al. 2008). A single individual of this species is often sufficient to establish a viable population (Strong et al. 2008). Biological characteristics such as parthenogenicity and viviparous juveniles seem to facilitate the success of M. tuberculata in new locations (Derraik 2008). During this sampling many juveniles were encountered in the reservoir. These observations show that reproduction was occurring. However, this proliferation is not without consequences for other species. It is observed that B. unicolor, which was the most abundant species with about 70% relative abundance during the study conducted by Ouedraogo et al. (2015), passed at the end of these five years in the third position with about 2% as relative abundance after M. tuberculata and C. aegyptiaca. The mapping of the species distribution in the reservoir shows that the distribution of M. tuberculata and B. unicolor overlap suggesting that these species are probably in competition for space. Moreover, the overlap index indicates that of all the species encountered, is the highest with B. unicolor. This supports the idea that M. tuberculata prefers the same microhabitats as B. unicolor. The reproductive performance of M. tubercula, therefore, allows it to get ahead every time. This may explain why the numbers of B. unicolor have been declining since the introduction of M. tuberculata. A review of mollusc feeding habits (Table 2) shows that these species can be in competition for resources (Raw et al. 2016). Indeed, taxa such as M. tuberculata tend to flourish in modified environments where they often outnumber native species or are the only species present (Strong et al. 2008). Marco et al. (2001) found that the density of M. tuberculata was inversely related to all other groups of macroinvertebrates when studying the aquatic invertebrates associated with the water-hyacinth. Since 1983, studies have shown a competitive exclusion of other snails by M. tuberculata, because of its rapid population increase and depletion of resources (Dudgeon 1986;Pointier and McCullough 1989). The low densities of other taxa may be explained by the monopolization of resources and space by M. tuberculata. Possible other reasons for the success of M. tuberculata are that it exhibits trophic plasticity and there is a specialization in diet between individuals within small spatial scales, reducing intraspecific competition (Raw et al. 2016). According to Santos and Eskinazi-Sant'Anna (2010), the eutrophic conditions of the local waterbodies appear to favor the proliferation of M. tuberculata, where it's abundance reaches extremely high densities, sometimes over 10,000 ind. m 2 . As the the Pianka index specifically measures the degree of overlap in the utilization of resources in space between two species, it does not take into account other aspects of the ecological niche such as food resources, predation pressure, or other biotic and abiotic factors (Hurlbert 1978). Then, other aspects of niche overlap could be measured to assess the impact of one species on another (Wandrag et al. 2019). Our results add to the body of evidence suggesting that invasive species are a leading cause of declines in species diversity and ultimately an increase in animal extinctions (Clavero and García-Berthou 2005).

Conclusions
The establishment of M. tuberculata has changed the structure of the mollusc community in reservoir No.3 of Ouagadougou. According to the IUCN red list assessment of this species, its abundance and geographical distribution continue to increase globally (Albrecht et al. 2018). Appropriate actions should be taken to mitigate the impacts of the species, such as controlling its spread, reducing the nutrient load, and restoring the native species. In addition, research should be conducted to better understand the ecology of the species and its impacts on the native species.We recommend that the distribution of M. tuberculata is actively monitored over the entire Nakanbé watershed and rapid action taken to limit the loss of native species stemming from the spread of this invasive species.