The distribution of aquatic molluscs and associated trematodes within the Limpopo Lowveld ecoregion, South Africa

Abstract

The continued rise in global temperature under the current climate change predictions is placing immense pressure on natural freshwater ecosystems, with thousands of freshwater species known to be either threatened or extinct, due to the added pressure on freshwater ecosystems. Freshwater gastropods have an important ecological role as primary consumers and vectors for various medical and veterinary parasitic trematode infections. Shifts in precipitation patterns, a rise in global temperature, habitat availability, water quality and the presence of invasive species can affect the distribution and abundance of native freshwater snail species. The movement of native and invasive species to new ecological niches can extend the current ranges of medically and economically important parasitic trematode species. Southern Africa's rich freshwater snail diversity constitutes approximately 101 native and 14 invasive species although this is based on historical data, with the current status being unclear. To accurately identify freshwater molluscan species from the Limpopo Lowveld region, morphological traits and molecular analysis were used to determine the current distribution of freshwater molluscan species in the region compared to historical data derived from the National Freshwater Snail Collection (NFSC) database. The current distribution was used to indicate how molluscan populations may have changed over an extended period. Thus, providing critical information to model future trends through scientific methods and aid in the development and implementation of management programs to preserve and protect local freshwater ecosystems. When compared to historical data, it was found that the native freshwater snail diversity of South Africa has seen a notable decline and more than 50% of the snails collected are considered invasive species, in contrast to the 14% of invasive species in the historical dataset. This provides clear support that one of the most critical threats to the native freshwater snails of the Limpopo system is the presence of invasive species. Furthermore, these invasive species not only pose a threat to native snail biodiversity but the diversity of the parasitic trematodes that use native snails as intermediate hosts. One of the invasive snail species collected during the current study was Tarebia granifera, a prolific and successful invader from Southeast Asia. The ability of T. granifera to rapidly spread through the aquatic ecosystem, resist unfavourable conditions that are detrimental to native molluscan species, and lack natural predators is concerning for native species. To date, no parasitic infections have been found in T. granifera in South Africa and it is thus not a known vector for any digenean parasites in South Africa. In contrast, native species such as Bulinus and Biomphalaria are vectors for various digenean parasites including Schistosoma sp. that transmits schistosomiasis. The use of morphological and molecular analysis of the COI (Cytochrome c oxidase subunit 1) and ITS2 (Internal transcribed spacer 2) genetic sequences aided in correctly identifying freshwater molluscs to species level. The use of 28S rRNA genetic sequences with specialized primers that amplify trematode rRNA was used to establish prepatent trematode infections within molluscan species. The use of the same extracted DNA sample for both mollusc identification and identification of prepatent trematode infections reduced the cost and increased sample capacity. The combination of morphological and molecular identification provided new insight into the genetic diversity within the same species and genetic mutations between sites of collection. Molluscs that were morphologically identified as Radix natalensis (Krauss, 1848) formed four genetically diverse groups located at different sites. Thus, indicating some form of transportation between sites or a vector transporting the molluscan species between the various locations. Comparing the current distribution to the historically collected specimens in the NFSC database suggested that native genera have critically decreased in spatial distribution and abundance. The combined effect of increased environmental and anthropogenic pressures on native species is of concern to the future health of the natural ecosystem function within the north-eastern provinces of South Africa. The reduction in native freshwater snail vectors could indirectly affect the presence of parasitic trematodes. The most effective method to assess patent infections is by examining snail tissue through dissection. The second method is through by cercarial shedding, where freshwater snail specimens naturally shed cercarial trematodes when exposed to artificial or natural light. This occurs when the sporocyst within the snail reaches maturity and the unsuccessful cercarial shedding tests could indicate that molluscan species may not have a trematode infection or have an immature or early-stage infection. Early-stage trematode infections require molecular monitoring to detect the prepatent trematode infections within specimens collected. In the present study 227 snails were screened for patent trematode infections. No patent infections were detected. However, molecular analysis for the prepatent infections indicated the presence of three different trematode infections within five different molluscan specimens. Trematode species detected were identified as Neofibricola smiti, Orientocreadium batrachoides, Petasiger variospinosus. The current study successfully identified molluscan species at sites of historical significance, thereby allowing to establish the changes in molluscan diversity from historically sampled areas and establish that the native freshwater snail diversity is in a dramatic decline from historically recorded diversity. The decline in native known vectors of medically and economically important parasitic trematodes, could negatively affect the presence and abundance of trematode species. This was evident with none of the molluscan vectors indicating any signs of cercarial shedding. However, prepatent infections of three parasitic trematodes were detected and the current study detected the first reported infection of Neofibricola smiti Achatz, Martens, Kudlai, Junker, Boe & Tkach, 2022 and Orientocradium batrachoides Tubangui, 1931 within molluscan vectors. These findings from the current study indicate the lack of information regarding the life cycle of parasitic trematodes and the need to further examine the relationship between trematode species and their molluscan vectors.