Schistosomiasis is a major public health problem, with 700 million people at risk and 251 million cases, mostly in sub-Saharan Africa (SSA) [1]. The disease is caused by the trematodes of the genus Schistosoma [2]. In SSA, schistosomiasis has a complex life cycle involving snails of the genus Bulinus and Biomphalaria as intermediate hosts and a mammal as the definitive host [3]. Control strategies rely primarily on mass drug administration (MDA) of praziquantel (PZQ), the only drug available for the regular treatment of school-age children, the main group at risk [4]. Although PZQ MDA has reduced the disease burden, it is ineffective against the immature stages of the parasite that maintain the schistosomiasis transmission cycle [5], thereby allowing for continued circulation of the parasite in human populations. In response to this limitation, malacological control is increasingly advocated as a complementary strategy to MDA for breaking the schistosomiasis transmission cycle [6] and could even contribute to its elimination in some endemic areas [7]. The regular use of chemical molluscicides such as niclosamide can lead to a rapid reduction in the snail population and, consequently, a drop in the level of disease transmission [8]. Despite some success with chemical molluscicides, their use is hampered by environmental concerns, particularly their impact on wildlife [9], as well as their high implementation costs [10]. To overcome these limitations, approaches to controlling snail populations have been developed using plants or aquatic predators. Among biological predators, the use of fish [11] and shrimp [12] predators has proven to be somewhat effective against snail populations and could help reduce the risk of schistosomiasis transmission. Unlike fish and shrimp, the impact of zooplankton on mollusk intermediate hosts of schistosomiasis remains poorly studied so far, despite some promising results.

Indeed, rotifers of the genus Philodina have been shown to alter significant life traits of Biomphalaria straminea and impact the survival of juvenile snails [13]. Moreover, compounds derived from rotifers could interfere with the motility of schistosomes [14]. Rotifers are metazoans that do not exceed 1 mm in size and are widely found in fresh water bodies [15]. Rotifers are involved in the food chain, particularly for fish in aquaculture [16]. However, despite a long-standing relative understanding of the impact of rotifers on snails and schistosomes [17], the scarcity of research does not provide sufficient information to consider their use in the control of schistosomiasis. To address this gap, we have designed an experimental study to assess the impact of rotifers on the growth and survival of several medically important snails, i.e., snails of the genus Bulinus and Biomphalaria transmitting schistosomiasis in Senegal.

The rotifers used in this experiment were collected in the region of Ziguinchor, located approximately 450 km southwest of Dakar, the capital city of Senegal. Previous investigations have already revealed a high diversity of rotifer species in the region of Ziguinchor [18]. Three samples of 50 mL of water, each containing rotifers, were collected and stored at room temperature for one day before being transported to the IRD malacology platform in Dakar. Then, the water samples were pooled and centrifuged at 12,000 rpm for 2 min to recover the pellet that was observed under a binocular microscope to estimate the density of the rotifers, which was 10 individuals per mL. To increase the density, the rotifers were recovered from the pellet and cultured during 15 days using dechlorinated tap water at a temperature between 26 °C and 28 °C and exposed to artificial light [19]. The final density obtained was approximatively 550 rotifers per mL. In addition, rapid morphological identification revealed a mixture of different genera of rotifers [20].

This study evaluated the impact of rotifers on different species of Biomphalaria and Bulinus snails. It provides new insights into the impact of rotifers on snail intermediate hosts of schistosome in SSA.

Overall, during this study, the exposure of the snails to both rotifers considerably impacted the Biomphalaria and Bulinus egg-mass-laying capacity and hatching rate The ability of rotifers to negatively impact these two parameters may lead to a reduction in the population density of snails and could thus constitute an important breakthrough for the control of intermediate hosts of schistosomes. Previous studies have highlighted the capacity of rotifers of the genus of Philodina to negatively impact the fecundity rate of Bi. straminea [13]. This shows the potential of using rotifers in the biological control of snail intermediate hosts of schistosomes. In this current study, we observed that the juvenile population of Biomphalaria seems particularly sensitive to rotifer exposure compared to adult individuals and the genus of Bulinus. This suggests that rotifers may have a species- and age-specific effect on snail fecundity. In this case, it is possible that the use of rotifers is more suitable for controlling Biomphalaria and consequently S. mansoni. Our study confirms that, in addition to Biomphalaria, rotifers can also be used against a wide range of Bulinus snails of medical importance. Therefore, it is worth exploring the potential of rotifers to control snails in a wide variety of ecological and epidemiological contexts.

The impact on egg-laying capacity and egg viability remains the key element through which rotifers may directly influence the density of snail populations. However, the reduction in growth in exposed snails should not be overlooked, as it could impact their reproductive and survival capacities and thus their population density. For example, growth delay could have an impact on the snails' ability to proliferate, notably when snails are exposed to the chemical molluscicide [22]. The evolution of snail size is also important in their survival process during seasonal changes, particularly during their aestivation in temporary ponds [23,24,25]. Similarly, in the event of thermal stress, larger snails may be more resistant to changing conditions than smaller individuals [24]. Thus, the growth delay caused by exposure to rotifers could indirectly also be beneficial from the perspective of the biological control of snail intermediate hosts of schistosomes.

However, throughout the study, mortality trends were almost identical between infested and non-infested snails. The exposure to rotifers does not seem to have any impact on snail mortality, regardless the species or age. Mortality seems more related to the specificity of each species. The mortality is conditioned by snail species, although it has previously been shown that rotifer infestation can induce excess mortality [13]. These differences could be explained by the nature of the rotifers used, their density, or even the snail species. This raises the question of the biological mechanism used by rotifers to impact snail life traits like size and reproduction or whether snails have defense mechanisms against rotifers. Further research, including studies under natural conditions, are needed to decipher the molecular interactions between rotifers and snail intermediate hosts of schistosomes.

For example, in natural ponds, several snail species are often found in sympatry. It would have been more convincing to study the impact of rotifers, taking into account the interaction between different snail species to see whether rotifers preferentially target molluscs according to species. Similarly, it would be useful to study the effect of rotifers on schistosoma-infested snails. Several models have shown excess mortality in infested Biomphalaria exposed to rotifers and their ability to impact parasite motility [13,14]. This study considered a mixture of rotifer genera; thus, it would be pertinent to study exactly which rotifer species have an impact on snails.

Our study shows that the presence of rotifers affects the growth and egg-laying capacity of snails, although there is no significant difference between the exposed and unexposed groups. Despite the strong trend observed, this lack of significant difference could be due to the limited number of measurements carried out during the study, by the limited sample size used for each snail species, or the density of rotifers. This may be explained by the scope of the study, which not only included five snail species but also investigated three parameters in addition to the viability of the eggs obtained.

This study demonstrates that rotifers of the genera have a major impact on the reproduction and growth of snail intermediate hosts of schistosomiasis, although their effect on snail mortality is limited.

These results suggest that rotifers could be a promising biological control method for reducing snail vector populations of schistosomiasis in sub-Saharan Africa. However, further studies are needed to better understand their ecological interactions and potential for large-scale applications.