The role of Tarebia granifera as an invasive in freshwater ecosystems of Southern Africa

Abstract

Over the past few decades, the increase in import and trade frequency of exotic aquatic species for aquarium hobby sales have led to the introduction and establishment of several invasive snail species on a global scale. Species become invasive when they are introduced and become established in environments outside of their native ranges where they can cause environmental harm. Invasive species are often responsible for a loss in native biodiversity that result in disrupted ecosystem function. Freshwater snails are considered one of the most endangered groups of species. The main threat to native snail populations is the spread of invasive snail species that have been reported to cause declines and extinctions in native snail populations globally. The establishment of invasive species is one of the major threats to freshwater biodiversity in South Africa. It is therefore of national priority that invasive species should be monitored and managed in order to protect the native biodiversity. The freshwater snail Tarebia granifera (Lamarck, 1822), originally from Southeast Asia, is an invasive aquatic snail on three continents, including Africa as well as North and South America. The snail was first reported in South Africa in 1999 from the northern parts of the KwaZulu-Natal province and it has since rapidly spread into the Mpumalanga and Limpopo provinces, including several important conservation areas within the country. The snail is known to become the dominant species within invaded ecosystems and can reach densities of well over the thousands of individuals/m2. The rapid spread and high densities reached by this invader have raised concerns regarding the possible negative impacts it may have on native snail species, primary benthic production and the trophic dynamics within invaded ecosystems. Previous research has investigated the effects of T. granifera in the coastal lakes and estuaries of KwaZulu-Natal. However, knowledge of the current distribution of this invader and its possible environmental impacts on the aquatic biodiversity and community structures of freshwater ecosystems are understudied. Furthermore, T. granifera is well known to act as the first intermediate host for diverse and prevalent species of disease-causing trematodes within and outside their native ranges and there is a need to investigate its role as a host or diluter for such parasites in South Africa. The first aim of this study was to investigate the current distribution, densities, and population size structures of T. granifera in the Limpopo River system and Phongolo River in South Africa. Each of the 19 selected sites were sampled for water quality and aquatic benthic snails, following standard methodologies. All sampled snails were identified, measured and counted in order to calculate snail density/m2 and determine snail population size structures. No significant correlations were found between any of the water quality variables and T. granifera density during iv this study. It was further found that T. granifera had higher new-born recruitment during the spring and summer months when environmental conditions were more favourable. Molluscs were present at 14 of the 19 selected sites with a total of four species sampled, two invasives: T. granifera and Physella acuta (Draparnaud, 1805), and two natives: Melanoides tuberculata (Müller, 1774) and Corbicula fluminalis (Krauss, 1848). Tarebia granifera was usually the dominant species and the only species sampled from all 14 sites, making up 89% of all collected mollusc samples. Empty shells of three native snail species (Planorbidae sp. Rafinesque, 1815, Bulinus tropicus Krauss, 1848, and Bulinus forskalii Ehrenberg, 1831) were also found at sites where T. granifera dominated. In addition, historical records indicated that numerous native aquatic snail species from the sites sampled during the present study were also missing. Tarebia granifera seem to have displaced these native snail species from these invaded ecosystems. As primary producers, diatoms play a key role in aquatic ecosystems as they are a food source for numerous heterotrophic species such as grazers and filter feeders. Several studies suggested that T. granifera can significantly reduce algal standing stocks, with unknown implications on aquatic consumers and higher trophic levels. Therefore, the second aim of this study was to determine the effects of T. granifera on benthic diatom community structures at selected in situ sites on the Phongolo, Olifants and Limpopo rivers. This aim was achieved by sampling diatoms from the same sites and sediment surfaces where the snails were sampled from. Benthic diatom samples were collected in triplicate from each site, following standard methodologies. The diatoms were identified to the lowest possible taxonomic level and divided into functional groups. A density scale was developed for T. granifera sampled from the selected sites: None, Low, Medium, High and Very high. With the use of a variety of univariate and multivariate statistical analyses and diversity indices, the possible effects of T. granifera density on benthic diatom community structures from the selected sites were assessed. Key findings were that T. granifera alters benthic diatom community structures, at high densities. Benthic diatom communities with high densities of T. granifera had an overall lower benthic diatom species diversity and disrupted functional groups with changes in diatom species abundance and dominance patterns. This was likely due to the high grazing pressure and bioturbation caused by the high densities of T. granifera at these sites. Sites with lower densities of T. granifera and the one site dominated by the native M. tuberculata had higher benthic diatom diversity, more diatom taxa, higher species richness and benthic diatoms that contributed to different diatom functional groups. Benthic diatom functional group analysis indicated that T. granifera may feed more on certain groups of benthic diatoms than others, leading to shifts in benthic diatoms dominance patterns, with higher abundances of diatom species (such as Cocconeis, Gomphonema and Fragilaria) with characteristics that enable them to resist T. granifera grazing pressure. Results also indicated that T. granifera size may also play a role in their diet preference, as sites with high densities of v small T. granifera, had higher abundances of large diatom groups than sites with high densities of larger T. granifera. The effects of T. granifera on benthic diatoms were then further investigated with the use of an experimental microcosm study on the Phongolo River Floodplain. Nine microcosms were filled with water (540 litres) from the Phongolo River, as well as fifty kilograms of dry floodplain sediment. The microcosms were randomly divided into three treatment groups. The first treatment group were seeded with T. granifera, the second with the native M. tuberculata and the last group was free of snails. Snails were seeded to represent the average density from the sites on the Phongolo River. Water and benthic diatom samples were collected in triplicate from each of the microcosm treatments five weeks after snail seeding, following standard methodologies. A variety of univariate and multivariate statistical analyses and diversity indices were used to assess differences in community structures. Results from this study indicated that microcosms containing T. granifera had lower benthic diatom diversity, fewer individuals and diatom species representative of the earlier stages of the colonisation process, leading to altered benthic diatom community structures and functionality. Microcosm treatments without T. granifera had more evenly distributed and diverse benthic diatom species and functional groups, with diatom species representative of the later and final stages of the colonisation process. From both the in situ river and experimental microcosm studies, it can be concluded that T. granifera poses a threat to native biota by disrupting community structures of benthic primary producers within invaded aquatic ecosystems. The final aims of this study were to investigate the role of the invasive thiarid (T. granifera) versus the native thiarid (M. tuberculata) as hosts for parasitic trematodes within the Limpopo River system and Phongolo River and to determine the genetic diversity of T. granifera from the selected sites. Tarebia granifera and M. tuberculata were collected from the selected sites and the infection status of the snails was tested with cercaria shedding experiments to induce the release of trematode cercaria. None of the snails shed cercaria during any of the shedding experiments and ten snails per species per site were randomly selected to determine prepatent trematode infections with the use of molecular analyses. Snails were dissected, whereafter, the hepatopancreas and a sample of each snail’s foot tissue were removed. Snail hepatopancreas samples were used in order to determine trematode infections with the use of molecular (ITS2 and 28S) analyses. Snail foot tissue samples were used to characterise snails by molecular (cox1) and phylogenetic analyses. All dissected T. granifera were found to be females with embryos in their brood pouches and all T. granifera were found to be free from trematode infection within the study area. However, M. tuberculata was found to be infected with two species of trematodes. This study provides the first report of M. tuberculata as an intermediate host for Haplorchis sp. vi and Centrocestus sp. in South Africa. This study further found all T. granifera from the selected sites on the Limpopo River system and Phongolo River to be genetically identical based on mitochondrial DNA (cox1 gene). Furthermore, polygenetic analysis of T. granifera indicated that sequences obtained from T. granifera during the present study were genetically identical to sequences from China and Thailand. Thus, the snail was likely introduced into South Africa from one of these two countries. From these results it can be concluded that T. granifera likely increase reproductive output during favourable environmental conditions that enables them to reach high densities and quickly become the dominant snail species. At high densities, T. granifera poses a threat to native biota by displacing native snail species and disrupting benthic diatom community structures, leading to reduced aquatic biodiversity and disrupted aquatic ecosystem function. Therefore, there is a need to control this invader to avoid further degradation of other freshwater habitats and aquatic biodiversity. This study also provides further evidence that the biodiversity of parasitic trematodes in thiarid snail hosts are understudied in South Africa and that there is a need for future research on these snail hosts and their parasites. Knowledge of the population dynamics and impacts of T. granifera, as well as their role as hosts for parasites, may aid in the development of management plans that may prevent the spread and destruction of these invaders on our native aquatic biota and their ecosystems.