An update on snail and trematode communities in the Sanyati Basin of Lake Kariba: New snail and trematode species but no human schistosomes.

BACKGROUND: The construction of Lake Kariba brought about a rise in the incidence of schistosomiasis in its surrounding towns of Kariba (Zimbabwe) and Siavonga (Zambia). After extensive control programs in Kariba, schistosomiasis prevalence dropped significantly. The objective of this study was to revisit the same localities sampled by Chimbari et al. (2003), and provide an update on the snail community and prevalence of trematodes in the Northern shore of Lake Kariba while focusing on planorbid species. METHODS: Monthly sampling of snails at 16 sites along the Northern shoreline of Lake Kariba, near Kariba town, was undertaken for one year. Minimum one specimen per morphotype was identified using molecular barcoding (sequencing a fragment of cytochrome c oxidase I subunit (COI)). The infection status of snails was assessed by Rapid Diagnostic PCRs (RD-PCR), and trematode infections were genotyped by sequencing COI and 18S rDNA markers. RESULTS: We collected and identified seven snail species: Bulinus truncatus, Bulinus forskalii, Gyraulus sp., Physella acuta, Bellamya sp., Radix affinis plicatula and Pseudosuccinea columella. Physella acuta was the most abundant snail species (comprising 56.95% of the total snail count) and present at all sites. The B. truncatus population was found to be infected with the stomach fluke Carmyerius cruciformis, a Petasiger sp. and a trematode species belonging to the family Notocotylidae. No Schistosoma sp. infections were detected in our collected snail specimens. CONCLUSIONS: We report B. truncatus as an intermediate snail host for Carmyerius cruciformis, and the presence of three non-schistosome trematode species that have not been reported in Lake Kariba before. Furthermore, we detect a possible shift in the snail community when compared to the report by Chimbari et al. (2003): this is the first record of Gyraulus sp. in Lake Kariba, and we did not observe the previously reported B. pfeifferi, B. globosus and Radix natalensis. Although this shift in snail communities might have contributed to the absence of Schistosoma spp. detection in this study, further monitoring of final and intermediate hosts across the Kariba basin is essential to prove a decrease of schistosomiasis in the area.

Sharing is caring? Barcoding suggests co-introduction of dactylogyrid monogeneans with Nile tilapia and transfer towards native tilapias in sub-Saharan Africa.

Invasive Nile tilapias negatively impact native tilapia species through hybridisation and competition. However, the co-introduction of parasites with Nile tilapia, and subsequent changes in parasite communities, are scarcely documented. Monogeneans are known pathogens of cultured Nile tilapia, although little is known about their fate once Nile tilapias establish in new ecosystems. We investigate the parasitological consequences of Nile tilapia introduction on native tilapias in basins in Cameroon, the Democratic Republic of the Congo (DRC), and Zimbabwe, focusing on ectoparasitic dactylogyrids (Monogenea). Using the mitochondrial cytochrome oxidase c subunit I (COI) and nuclear 18S-internal transcribed spacer 1 (18S-ITS1) rDNA region of 128 and 166 worms, respectively, we evaluated transmission of several dactylogyrid species. Parasite spillover from Nile tilapia was detected for Cichlidogyrus tilapiae to Coptodon guineensis in Cameroon, Cichlidogyrus thurstonae to Oreochromis macrochir in the DRC, and Cichlidogyrus halli and C. tilapiae to Coptodon rendalli in Zimbabwe. Parasite spillback to Nile tilapia was detected for Cichlidogyrus papernastrema and Scutogyrus gravivaginus from Tilapia sparrmanii and Cichlidogyrus dossoui from C. rendalli or T. sparrmanii in the DRC, and Cichlidogyrus chloeae from Oreochromis cf. mortimeri and S. gravivaginus from O. macrochir in Zimbabwe. 'Hidden' transmissions (i.e. transmission of certain parasite lineages of species that are naturally present on both alien and native hosts) were detected for C. tilapiae and Scutogyrus longicornis between Nile tilapia and Oreochromis aureus and C. tilapiae between Nile tilapia and Oreochromis mweruensis in the DRC, and Cichlidogyrus sclerosus and C. tilapiae between Nile tilapia and O. cf. mortimeri in Zimbabwe. A high density of Nile tilapia occurring together with native tilapias, and the broad host range and/or environmental tolerance of the transmitted parasites, are proposed as factors behind parasite transmission through ecological fitting. However, continuous monitoring and the inclusion of environmental variables are necessary to understand the long-term consequences of these transmissions on native tilapias and to elucidate other underlying factors influencing these transmissions.

Additional Taxonomic Information for Lamproglena hemprichii (Copepoda: Lernaeidae) Based on Scanning Electron Microscopy and Genetic Characterization, Alongside Some Aspects of Its Ecology.

Additional taxonomic and ecological data for the lernaeid copepod Lamproglena hemprichii Nordmann, 1832 infecting the African tigerfish, Hydrocynus vittatus Castelnau, 1861, are presented with scanning electron micrographs, molecular characterization, and selected ecological parameters. Eighty fish were collected from Lake Kariba between October 2014 and July 2015. Scanning electron microscopy provided additional data for the morphology, including structures on the antennulae, antennae, and legs. The 18S and 28S rDNA fragments of this species were distinct from those of other Lamproglena taxa but placed this species within this genus. Phylogenetically, L. hemprichii appears closest to L. monodi Capart, 1944, the only other African species for which molecular data is available. The anterior part of the second gill filament was the preferred attachment site. There was a positive correlation (Pearson correlation coefficient r2 = 0.64; P = 0.77) between the length of the parasite and the length of the fish. A positive correlation (Pearson correlation coefficient r2 = 0.61; P = 0.03) between the length of the parasite and the length of the gill filament was also observed. Although the specimens studied here are morphologically highly similar to previous reports of L. hemprichii, some morphological variation was observed, and a revision (morphometric and genetic) of the taxon is suggested. This study provides the first detailed genetic characterization and phylogenetic information for the species.

Mosaic or melting pot: The use of monogeneans as a biological tag and magnifying glass to discriminate introduced populations of Nile tilapia in sub-Saharan Africa.

The origin of introduced Nile tilapia stocks in sub-Saharan Africa is largely unknown. In this study, the potential of monogeneans as a biological tag and magnifying glass is tested to reveal their hosts' stocking history. The monogenean gill community of different Nile tilapia populations in sub-Saharan Africa was explored, and a phylogeographic analysis was performed based on the mitogenomes of four dactylogyrid species (Cichlidogyrus halli, C. sclerosus, C. thurstonae, and Scutogyrus longicornis). Our results encourage the use of dactylogyrids as biological tags. The magnifying glass hypothesis is only confirmed for C. thurstonae, highlighting the importance of the absence of other potential hosts as prerequisites for a parasite to act as a magnifying glass. With the data generated here, we are the first to extract mitogenomes from individual monogeneans and to perform an upscaled survey of the comparative phylogeography of several monogenean species with unprecedented diagnostic resolution.

Description of Tresuncinidactylus wilmienae gen. et sp. n. (Monogenea: Gyrodactylidae), from the gills of the bulldog, Marcusenius macrolepidotus (Peters) from Lake Kariba, Zimbabwe.

The African continent has a rich diversity of fish and amphibians in its inland water systems that serve as hosts for monogeneans of seven genera of the Gyrodactylidae van Beneden et Hesse, 1832. In August 2011, eight gyrodactylid parasites were collected from the gills of two specimens of bulldog, Marcusenius macrolepidotus (Peters), from Lake Kariba, Zimbabwe. Morphometric evaluation and sequencing of 18S rDNA confirmed that the specimens represented a species of a new viviparous genus, Tresuncinidactylus wilmienae gen. et sp. n. The attachment apparatus consists of a single pair of large slender hamuli with prominently flattened roots that are connected by a simple, narrow dorsal bar. The ventral bar is small and possesses a thin lingulate membrane but no evident anterolateral processes. There are 16 marginal hooks of one morphological type, but of three different sizes, with large falculate sickles that are proportionaly equal in length to the length of their handles. The two largest pairs of marginal hooks are positioned closest to the opisthaptoral peduncle, the neighbouring two pairs of medium-sized marginal hook sickles are situated along the lateral margins of the opisthaptor. Four pairs of smallest marginal hooks are positioned along the posterior margin of the opisthaptor. The male copulatory organ consists of a muscular pouch armed with approximately 30 gracile spines. Phylogenetic analyses of partial sequences of the 18S rDNA using Maximum Likelihood and Bayesian Inference placed the new genus within the lineage of solely African genera and suggests Afrogyrodactylus Paperna, 1968, Citharodactylus Prikrylová, Shinn et Paladini, 2017 and Mormyrogyrodactylus Luus-Powell, Mashego et Khalil, 2003 as genera most closely related to the new genus.

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

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.

Exposing the Barcoding Void: An Integrative Approach to Study Snail-Borne Parasites in a One Health Context.

Trematodes are snail-borne parasites of major zoonotic importance that infect millions of people and animals worldwide and frequently hybridize with closely related species. Therefore, it is desirable to study trematodiases in a One Health framework, where human and animal trematodes are considered equally important. It is within this framework that we set out to study the snail and trematode communities in four artificial lakes and an abattoir in Zimbabwe. Trematode infections in snails were detected through multiplex PCR protocols. Subsequently, we identified snails by sequencing a partial mitochondrial cytochrome c oxidase subunit I (COI) fragment, and trematodes (adults from the abattoir and larval stages detected in snails) using COI and nuclear rDNA markers. Of the 1,674 collected snails, 699 were molecularly analyzed, in which we identified 12 snail and 19 trematode species. Additionally, three parasite species were sampled from the abattoir. Merely four trematode species were identified to species level through COI-based barcoding. Moreover, identification of members of the superfamilies Opisthorchioidea and Plagiorchioidea required a phylogenetic inference using the highly conserved 18S rDNA marker, as no related COI reference sequences were present in public databases. These barcoding challenges demonstrate a severe barcoding void in the available databases, which can be attributed to the neglected status of trematodiases. Adding to this, many available sequences cannot be used as different studies use different markers. To fill this gap, more studies on African trematodes, using a standardized COI barcoding region, are desperately needed.

Correction: Plague in Zimbabwe from 1974 to 2018: A review article.

[This corrects the article DOI: 10.1371/journal.pntd.0007761.].

Plague in Zimbabwe from 1974 to 2018: A review article.

Plague is a zoonotic disease caused by the bacterium Yersinia pestis and is transmitted through the bites of infected rodent fleas. Plague is well known for causing 3 major human pandemics that have killed millions of people since 541 A.D. The aim of this Review is to provide an overview of the epidemiology and ecology of plague in Zimbabwe with special emphasis on its introduction, its potential reservoirs and vectors, and possible causes of its persistence and cyclic outbreaks. To achieve this, we carried out a search and document reported plague outbreaks in Zimbabwe. In the country, human plague cases have been reported in Hwange, Nkayi, and Lupane since 1974. The highest number of cases occurred in 1994 in the Nkayi district of Matabeleland North Province with a total of 329 confirmed human cases and 28 deaths. Plague is encountered in 2 different foci in the country, sylvatic and rural. Risk factors for contracting plague in the country include man-to-rodent contact, cultivation, hunting, cattle herding, handling of infected materials, camping in forests, and anthropic invasion of new areas. Plague is now enzootic in Zimbabwe, and the most recent case was reported in 2012, hence its effective control requires up-to-date information on the epidemiology and ecology of the disease. This can be achieved through continuous monitoring and awareness programs in plague-prone areas.

Seasonal occurrence of metazoan parasites in Tigerfish, Hydrocynus vittatus Castelnau, 1861 (Characiformes: Alestidae) from Sanyati Basin, Lake Kariba, Zimbabwe.

Lake Kariba is a tropical lake with slight variations in seasonal temperature. Temperature is an important physical variable in the biology of both fish and their parasites. Currently, there is no information on the seasonal occurrence of fish parasites in Lake Kariba. The objective of this study was to investigate the seasonal occurrence of metazoan parasites in Hydrocynus vittatus in Lake Kariba, Zimbabwe. Twenty fish specimens were collected by seine netting per season between October 2014 and July 2015 in the Sanyati Basin, Lake Kariba, and examined for metazoan parasites. Mean water temperatures ranged from 24.1 °C to 31.2 °C with slight variations between the seasons. Metazoan parasites consisting of Monogenea (Annulotrema pikei, Annulotrema pseudonili, Annulotrema bracteatum), Nematoda (Contracaecum larvae), Copepoda (Lamproglena hemprichii), Cestoda (larval cestodes, Ichthybothrium sp.) and Pentastomida (pentastomid larvae) were recorded. Larval cestodes were recorded in autumn and spring, while pentastome larvae were recorded in summer and spring. The Ichthybothrium sp. was recorded once in winter. Annulotrema pikei and A. pseudonili were observed on the gills and A. bracteatum on both the gills and the skin. Contracaecum larvae, L. hemprichii and A. bracteatum (from the skin) were recorded in all the seasons, with slight variations in prevalence, mean abundance and mean intensity. However, these variations were not statistically significant (analysis of variance or ANOVA, p > 0.05). The slight variations in occurrence of the parasites were probably because of the thermal stability of the lake where variation in temperature was small between seasons. Both A. bracteatum and Contracaecum larvae were aggregated on the fish host, whereas L. hemprichii exhibited a random distribution. Parasite diversity was at its highest during winter.

A cascade of biological invasions and parasite spillback in man-made Lake Kariba.

Parasite spillback, the infection of a non-indigenous organism by a native parasite, is a highly important although understudied component of ecological invasion dynamics. Here, through the first analysis of the parasite fauna of lymnaeid gastropods of Lake Kariba (Zimbabwe). We illustrate how the creation of an artificial lake may lead to a cascade of biological invasions in which an invasive aquatic plant promotes the proliferation of invasive gastropods, which in turn alters the epidemiology of trematodiases of potential medical and veterinary importance. Using a new multiplex Rapid Diagnostic PCR assay, we assessed the prevalence of Fasciola sp. infections in the gastropod populations. Both gastropod hosts and trematode parasites were identified using DNA barcoding. We provide the first record of the invasive North-American gastropod Pseudosuccinea columella in Lake Kariba. This species was found at 14 out of 16 sampled sites and its abundance was strongly positively correlated with the abundance of the invasive South-American water hyacinth (Eichhornia crassipes). About 65% of the P. columella specimens analysed were infected with a hitherto unknown Fasciola species. Phylogenetic analyses indicate close affinity to Fasciola hepatica and F. gigantica, which cause fasciolosis, an important liver disease affecting both ruminants and humans. In addition, another non-native Lymnaeid species was found: a Radix sp. that clustered closely with a Vietnamese Radix species. Radix sp. hosted both amphistome and Fasciola trematodes. By linking an invasion cascade and parasite spillback, this study shows how both processes can act in combination to lead to potentially important epidemiological changes.

Emergence of infection with Aphanomyces invadans in fish in some main aquatic ecosystems in Zimbabwe: A threat to national fisheries production.

The first outbreak on the African continent of infection with Aphanomyces invadans (the causative agent of epizootic ulcerative syndrome) in fish was confirmed in the Chobe-Zambezi rivers in 2007. The emergence of massive outbreaks of infection with A. invadans in multiple fish species exposed serious aquatic biosecurity challenges in the Southern African region. This study investigated the incursion of infection with A. invadans in fish from the main aquatic ecosystems of Zimbabwe from 2012 to 2015 using data obtained from the Department of Livestock and Veterinary Services, Zimbabwe. In some outbreaks, fish samples were collected and tested at the University of Zambia, for confirmation by histopathology and species-specific PCR. The infection was first confirmed at Darwendale water impoundment (Mashonaland West Province) in 2012, followed by Matabeleland South Province at Mtshabezi water impoundment and Nkankezi River (both 2013). An apparent southward spread continued in 2014, with virgin outbreaks at Ntalale water impoundment (Matabeleland South Province) and Mwenezi River in Midlands Province. In 2015, inland incursion was confirmed at Dutchman's Pool in Midlands Province and further north-west at the Sanyati River Basin in Lake Kariba (Mashonaland West Province). In all outbreaks, infection with A. invadans was confirmed in seven fish species, namely the African sharptooth catfish (Clarias gariepinus, Burchell, 1822), blunt-toothed African catfish (Clarias ngamensis Castelnau, 1861), yellow belly bream (Serranochromis robustus Gunther, 1864), straight fin barb (Enteromius paludinosus Peters, 1852), dashtail barb (Enteromius poechii Steindachner, 1911), large-mouth bass (Micropterus salmoides Lac'epe'de, 1802) and the three-spot tilapia (Oreochromis andersonii Castelnau, 1861). Cases were most common in the African sharptooth catfish, with mortalities more pronounced in young fish of all species. The results suggested a gradual emergence of an intractable infection with A. invadans in fish in the main aquatic ecosystems of Zimbabwe, which may have negative impact on biodiversity conservation and aquaculture.

Species of Gyrodactylus von Nordmann, 1832 (Platyhelminthes: Monogenea) from cichlids from Zambezi and Limpopo river basins in Zimbabwe and South Africa: evidence for unexplored species richness.

New findings on Gyrodactylus spp. parasitising African cichlids in southern Africa are presented, comprising data from Zimbabwe and South Africa. Morphometry of opisthaptoral hard parts in combination with nuclear ribosomal DNA sequences confirmed the presence of six species of Gyrodactylus von Nordmann, 1832. Three new species are described from fishes in Zimbabwe: Gyrodactylus chitandiri n. sp. from the gill arches of Coptodon rendalli (Boulenger) and Pseudocrenilabrus philander (Weber); Gyrodactylus occupatus n. sp. from the fins of Oreochromis niloticus (L.), Pharyngochromis acuticeps (Steindachner) and P. philander; and Gyrodactylus parisellei n. sp. from the fins of O. niloticus, P. philander and Tilapia sp. Gyrodactylus nyanzae Paperna, 1973 was also identified from the gills of O. niloticus and C. rendalli collected from two localities in Zimbabwe; these findings represent new host and locality records for this parasite. Gyrodactylus sturmbaueri Vanhove, Snoeks, Volckaert & Huyse, 2011 was identified from P. philander collected in South Africa and Zimbabwe thereby providing new host and locality records for this parasite. Finally, Gyrodactylus yacatli García-Vásquez, Hansen, Christison, Bron & Shinn, 2011 was collected from the fins of O. niloticus and P. philander studied in Zimbabwe; this represents the first record of this species from the continent of Africa. Notably, this study improves upon the knowledge of Gyrodactylus spp. parasitising cichlids from these southern African regions. All species studied were recorded from at least two different cichlid host species indicating trend for a wide range of Gyrodactylus hosts in Africa. Accordingly, this supports the idea of intensive host switching in the course of their evolution.

Taxonomy, distribution and prevalence of parasites of tigerfish, Hydrocynus vittatus (Castelnau, 1861) in the Sanyati basin, Lake Kariba, Zimbabwe.

Parasites of the tigerfish (Hydrocynus vittatus) were investigated in the period October 2014 to July 2015 in the Sanyati Basin, Lake Kariba. The fish were collected using seine netting and also during the annual Kariba International Tiger Fishing Tournament. A total of 80 fish specimens (24 males and 56 females) were collected and were infected with the following seven parasite taxa: Monogenea (Annulotrema sp.1 from the gills and Annulotrema sp.2 from the skin), Nematoda (Contracaecum larvae), Cestoda (bothriocephalid, larval cyclophyllid), Copepoda (Lamproglena hemprichii), pentastomid, Myxosporea (Myxobolus sp.,) and unicellular ciliate parasites (Trichodina sp., Tetrahymena sp., and unidentified). Annulotrema sp. 1 was observed in all fish and had the highest prevalence, mean intensity and abundance. The fish organs infected were gills, skin, fin, body cavity, stomach, intestines, mesentery, liver, kidney, brain cavity and swim bladder. No parasites were observed in the muscle, eyes and blood. The distribution of the parasites was highest in the gills and lowest in the brain cavity and swimbladder. Bothriocephalids, pentastomes and Trichodina sp. were not observed in male fish. Sex was not related to the intensity of parasites. The results of the study showed that H. vittatus has a richer parasite community than other previous investigated alestids. Pentastomes, Myxobolus sp., Trichodina sp., Tetrahymena sp. and bothriocephalid cestodes are new records for H. vittatus in Zimbabwe.

Parasite hybridization in African Macrogyrodactylus spp. (Monogenea, Platyhelminthes) signals historical host distribution.

Macrogyrodactylus spp. from the gills of Clarias gariepinus in Zimbabwe and Kenya, and C. anguillaris in Senegal were identified using haptoral sclerite morphology and by sequencing the nuclear ribosomal DNA internal transcribed spacers (ITS) 1 and 2, partial 18S and the complete 5.8S rRNA gene. A molecular phylogeny was constructed using all sequenced Macrogyrodactylus species to date. Based on morphology, Macrogyrodactylus congolensis, M. heterobranchii, M. clarii, and M. karibae were identified, with one specimen from Zimbabwe displaying morphological features that were intermediate between M. heterobranchii and M. clarii. In the intermediate form, the partial 18S and ITS1 sequence was identical to that of M. clarii while the remaining ITS1 and complete ITS2 region was almost identical to M. heterobranchii as was the partial cox1 fragment, thus strongly suggesting a hybrid origin. At present, the catfish host of M. heterobranchii and M. clarii do not co-occur in southern Zimbabwe; this hybridization event is therefore proof of historical sympatry of both fish species.