Invasive snails, parasite spillback, and potential parasite spillover drive parasitic diseases of Hippopotamus amphibius in artificial lakes of Zimbabwe

Abstract

Background Humans impose a significant pressure on large herbivore populations, such as hippopotami, through hunting, poaching, and habitat destruction. Anthropogenic pressures can also occur indirectly, such as artificial lake creation and the subsequent introduction of invasive species that alter the ecosystem. These events can lead to drastic changes in parasite diversity and transmission, but generally receive little scientific attention. Results In order to document and identify trematode parasites of the common hippopotamus (Hippopotamus amphibius) in artificial water systems of Zimbabwe, we applied an integrative taxonomic approach, combining molecular diagnostics and morphometrics on archived and new samples. In doing so, we provide DNA reference sequences of the hippopotamus liver fluke Fasciola nyanzae, enabling us to construct the first complete Fasciola phylogeny. We describe parasite spillback of F. nyanzae by the invasive freshwater snail Pseudosuccinea columella, as a consequence of a cascade of biological invasions in Lake Kariba, one of the biggest artificial lakes in the world. Additionally, we report an unknown stomach fluke of the hippopotamus transmitted by the non-endemic snail Radix aff. plicatula, an Asian snail species that has not been found in Africa before, and the stomach fluke Carmyerius cruciformis transmitted by the native snail Bulinus truncatus. Finally, Biomphalaria pfeifferi and two Bulinus species were found as new snail hosts for the poorly documented hippopotamus blood fluke Schistosoma edwardiense. Conclusions Our findings indicate that artificial lakes are breeding grounds for endemic and non-endemic snails that transmit trematode parasites of the common hippopotamus. This has important implications, as existing research links trematode parasite infections combined with other stressors to declining wild herbivore populations. Therefore, we argue that monitoring the anthropogenic impact on parasite transmission should become an integral part of wildlife conservation efforts. Graphical abstract

Paleobiogeographical origins of Fasciola hepatica and F. gigantica in light of new DNA sequence characteristics of F. nyanzae from hippopotamus

“…in the South African reserves is identical to that obtained in snails and in one hippopotamus in an artificial lake of Zimbabwe (30). The numerous mutations in the short cox1 fragments obtained from F. nyanzae in Zimbabwe (30,54) represent a surprising intraspecific variability for specimens from only one place and are difficult to interpret in materials from an artificial lake.…”

“…in the South African reserves is identical to that obtained in snails and in one hippopotamus in an artificial lake of Zimbabwe (30). The numerous mutations in the short cox1 fragments obtained from F. nyanzae in Zimbabwe (30,54) represent a surprising intraspecific variability for specimens from only one place and are difficult to interpret in materials from an artificial lake. Therefore, these numerous mutations should be individually verified in the electropherograms and the geographical origin of the snail and hippopotamus hosts introduced in the artificial lake should be analyzed regarding the sequences in question.…”

“…magna were obtained from GenBank. Concerning F. nyanzae, sequences retrieved included ITS-1 and ITS-2 (MT909820-21, MW046870, MW046872, MT893586-MT893588, MT893595) and partial cox1 sequences (MT909542-MT909550) from Zimbabwe (30). Concerning Fs.…”

“…No adult flukes were produced in experimental infections of calves, goats and rabbits (29), and it was never reported in cattle around areas where it is frequent in Uganda (47). Parasitological studies on hippopotamuses have reported the parasite several times in Uganda (48,49), Kenya (50), South Africa (51), the southern part of Chad (52), Gabon (53), and in an artificial lake in Zimbabwe (30,54). These findings indicate a very wide distribution throughout Africa, which overlaps with that of its specific freshwater lymnaeid snail vector species R. natalensis (29) (Figure 2).…”

Comparative study of the sensitivity of two freshwater gastropods, Lymnaea stagnalis and Planorbarius corneus, to silver nanoparticles: bioaccumulation and toxicity

“…To prevent potential metal contamination, all the glassware was soaked overnight in acid (15% HNO 3 and 5% HCl), and rinsed with ultrapure water three times before experimentation (Croteau et al, 2011a). The gastropods were plunged into hot water (70 • C) for 90s to prevent contraction before dissection (Schols et al, 2021). Hepatopancreas, stomach, kidney, mantle and foot were dissected and frozen at − 20 • C before Ag bioaccumulation analysis.…”