Nejvíce citovaný článek - PubMed ID 23403992
Two new species of Cichlidogyrus (Monogenea: Dactylogyridae) parasitizing the gills of African cichlid fishes (Perciformes) from Senegal: morphometric and molecular characterization
Owing to the largely unexplored diversity of metazoan parasites, their speciation mechanisms and the circumstances under which such speciation occurs - in allopatry or sympatry - remain vastly understudied. Cichlids and their monogenean flatworm parasites have previously served as a study system for macroevolutionary processes, e.g., for the role of East African host radiations on parasite communities. Here, we investigate the diversity and evolution of the poorly explored monogeneans infecting a West and Central African lineage of cichlid fishes: Chromidotilapiini, which is the most species-rich tribe of cichlids in this region. We screened gills of 149 host specimens (27 species) from natural history collections and measured systematically informative characters of the sclerotised attachment and reproductive organs of the parasites. Ten monogenean species (Dactylogyridae: Cichlidogyrus and Onchobdella) were found, eight of which are newly described and one redescribed herein. The phylogenetic positions of chromidotilapiines-infecting species of Cichlidogyrus were inferred through a parsimony analysis of the morphological characters. Furthermore, we employed machine learning algorithms to detect morphological features associated with the main lineages of Cichlidogyrus. Although the results of these experimental algorithms remain inconclusive, the parsimony analysis indicates that West and Central African lineages of Cichlidogyrus and Onchobdella are monophyletic, unlike the paraphyletic host lineages. Several instances of host sharing suggest occurrences of intra-host speciation (sympatry) and host switching (allopatry). Some morphological variation was recorded that may also indicate the presence of species complexes. We conclude that collection material can provide important insights on parasite evolution despite the lack of well-preserved DNA material.
TITLE: À l’Ouest, rien de nouveau ? L’histoire évolutive des monogènes (Dactylogyridae : Cichlidogyrus, Onchobdella) infectant une tribu de poissons cichlidés (Chromidotilapiini) d’Afrique occidentale et centrale. ABSTRACT: En raison de la nature largement inexplorée de la diversité des parasites métazoaires, leurs mécanismes de spéciation et les circonstances dans lesquelles cette spéciation se produit—allopatrie ou sympatrie—restent très peu étudiés. Les cichlidés et leurs parasites Plathelminthes monogènes ont déjà servi de modèle pour l’étude des processus macro-évolutifs, par exemple pour le rôle des radiations d’hôtes de l’Afrique de l’Est sur les communautés de parasites. Ici, nous étudions la diversité et l’évolution des monogènes peu étudiées qui infestent une lignée de poissons cichlidés d’Afrique occidentale et centrale : les Chromidotilapiini, qui est la tribu de cichlidés la plus riche en espèces dans cette région. Nous avons examiné les branchies de 149 spécimens hôtes (27 espèces) provenant de musées d’histoire naturelle et mesuré systématiquement les caractères informatifs des pièces sclérifiées du hapteur et des organes copulateurs des parasites. Dix espèces de monogènes (Dactylogyridae : Cichlidogyrus et Onchobdella) ont été trouvées ; huit sont nouvelles pour la science et une est redécrite. Les positions phylogénétiques des espèces de Cichlidogyrus infectant les chromidotilapiines ont été déduites par une analyse de parcimonie des caractères morphologiques. En outre, nous avons utilisé des algorithmes d’apprentissage automatique pour détecter les caractéristiques morphologiques associées aux principales lignées de Cichlidogyrus. Bien que les résultats de ces algorithmes expérimentaux restent peu concluants, l’analyse de parcimonie indique que les lignées de Cichlidogyrus et d’Onchobdella de l’Afrique de l’Ouest et Central sont monophylétiques, contrairement aux lignées d’hôtes qui sont paraphylétiques. Plusieurs cas de partage d’hôtes suggèrent des occurrences de spéciation synxénique (sympatrie) et de changement d’hôte (allopatrie). Certaines variations morphologiques ont été enregistrées et peuvent également indiquer la présence de complexes d’espèces. Nous concluons donc que le matériel de collection peut fournir des informations importantes sur l’évolution des parasites malgré le manque d'ADN exploitable.
- Klíčová slova
- Allopatric speciation, Host-parasite evolution, Machine learning, Maximum parsimony, Sympatric speciation,
- MeSH
- cichlidy * parazitologie MeSH
- fylogeneze MeSH
- paraziti * MeSH
- ploštěnci * genetika MeSH
- Trematoda * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Little phylogeographic structure is presumed for highly mobile species in pelagic zones. Lake Tanganyika is a unique ecosystem with a speciose and largely endemic fauna famous for its remarkable evolutionary history. In bathybatine cichlid fishes, the pattern of lake-wide population differentiation differs among species. We assessed the congruence between the phylogeographic structure of bathybatine cichlids and their parasitic flatworm Cichlidogyrus casuarinus to test the magnifying glass hypothesis. Additionally, we evaluated the use of a PoolSeq approach to study intraspecific variation in dactylogyrid monogeneans. The lake-wide population structure of C. casuarinus ex Hemibates stenosoma was assessed based on a portion of the cox1 gene combined with morphological characterisation. Additionally, intraspecific mitogenomic variation among 80 parasite samples from one spatially constrained metapopulation was assessed using shotgun NGS. While no clear geographic genetic structure was detected in parasites, both geographic and host-related phenotypic variation was apparent. The incongruence with the genetic north-south gradient observed in H. stenosoma may be explained by the broad host range of this flatworm including eupelagic bathybatine host species that form panmictic populations across the lake. In addition, we present the first parasite mitogenome from Lake Tanganyika and propose a methodological framework for studying the intraspecific mitogenomic variation of dactylogyrid monogeneans.
- Klíčová slova
- Bathybatini, Cichlidogyrus, PoolSeq, cox1, monogenea,
- Publikační typ
- časopisecké články MeSH
The Lower Congo Basin is characterized by a mangrove-lined estuary at its mouth and, further upstream, by many hydrogeographical barriers such as rapids and narrow gorges. Five localities in the mangroves and four from (upstream) left bank tributaries or pools were sampled. On the gills of Coptodon tholloni, Coptodon rendalli, Hemichromis elongatus, Hemichromis stellifer and Tylochromis praecox, 17 species of parasites (Dactylogyridae & Gyrodactylidae, Monogenea) were found, eight of which are new to science. Six of these are herein described: Cichlidogyrus bixlerzavalai n. sp. and Cichlidogyrus omari n. sp. from T. praecox, Cichlidogyrus calycinus n. sp. and Cichlidogyrus polyenso n. sp. from H. elongatus, Cichlidogyrus kmentovae n. sp. from H. stellifer and Onchobdella ximenae n. sp. from both species of Hemichromis. On Cichlidogyrus reversati a ridge on the accessory piece was discovered that connects to the basal bulb of the penis. We report a putative spillback effect of the native parasites Cichlidogyrus berradae, Cichlidogyrus cubitus and Cichlidogyrus flexicolpos from C. tholloni to the introduced C. rendalli. From our results, we note that the parasite fauna of Lower Congo has a higher affinity with the fauna of West African and nearby freshwater ecoregions than it has with fauna of other regions of the Congo Basin and Central Africa.
Le cours du Bas Congo est caractérisé par un estuaire bordé de mangroves et, plus en amont, par de nombreuses barrières hydro-géographiques formées de rapides ou de gorges étroites. Nous avons échantillonné dans cinq localités au niveau des mangroves et dans quatre autres en amont sur la rive gauche du fleuve, dans des affluents ou des étangs. Nous avons trouvé, sur les branchies de Coptodon tholloni, Coptodon rendalli, Hemichromis elongatus, Hemichromis stellifer et Tylochromis praecox, 17 espèces de parasites (Dactylogyridae et Gyrodactylidae, Monogenea), dont huit sont nouvelles pour la science. Six d’entre elles sont décrites ici : Cichlidogyrus bixlerzavalai n. sp. et Cichlidogyrus omari n. sp. sur T. praecox, Cichlidogyrus calycinus n. sp. et Cichlidogyrus polyenso n. sp. sur H. elongatus, Cichlidogyrus kmentovae n. sp. sur H. stellifer et Onchobdella ximenae n. sp. sur les deux espèces d’Hemichromis. Nous décrivons, chez Cichlidogyrus reversati, une arête sur la pièce accessoire qui la connecte avec l’ampoule basale basal du pénis. Nous notons un probable transfert latéral des espèces autochtones Cichlidogyrus berradae, Cichlidogyrus cubitus et Cichlidogyrus flexicolpos de C. tholloni vers l’espèce introduite C. rendalli. Nos résultats montrent que la faune parasitaire du Bas Congo présente plus d’affinités avec les faunes d’Afrique de l’Ouest ou des écorégions d’eau douce voisines, qu’avec celles des autres parties du bassin du Congo ou de l’Afrique Centrale.
- MeSH
- biodiverzita MeSH
- cichlidy anatomie a histologie parazitologie MeSH
- fylogeneze MeSH
- fylogeografie MeSH
- infekce červy třídy Trematoda epidemiologie parazitologie veterinární MeSH
- nemoci ryb epidemiologie parazitologie MeSH
- ploštěnci klasifikace genetika izolace a purifikace MeSH
- sladká voda parazitologie MeSH
- žábry parazitologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Kongo epidemiologie MeSH
Seven new species of Cichlidogyrus Paperna, 1960 (Monogenea: Dactylogyridae) isolated from the gills of six cichlid host species belonging to four tribes and sampled from the Congolese coastline of Lake Tanganyika (LT) are described: Cichlidogyrus adkoningsi sp. nov. from Cyphotilapia frontosa (tribe Cyphotilapiini); C. koblmuelleri sp. nov. from Cardiopharynx schoutedeni (Ectodini); C. habluetzeli sp. nov. from C. schoutedeni and C. frontosa; C. antoineparisellei sp. nov. from Interochromis loocki (Tropheini); C. masilyai sp. nov. from Petrochromis orthognathus (Tropheini); C. salzburgeri sp. nov. from P. trewavasae, and C. sergemorandi sp. nov. from Tylochromis polylepis (Tylochromini). This study represents the first parasitological examination of cyphotilapiine cichlid hosts. Representatives of the Tanganyikan ectodine, tropheine, and tylochromine cichlids previously sampled from various localities in the lake yielded nine, twelve, and two described species of Cichlidogyrus, respectively. The study further includes a morphological characterization of the male copulatory organ of six undescribed species of Cichlidogyrus found on the gills of the tropheines I. loocki and P. orthognathus, and on those of Callochromis melanostigma and Xenotilapia flavipinnis (both Ectodini). Geographical variation in the monogenean fauna of I. loocki was observed. The most closely related cichlid species investigated in this study harboured Cichlidogyrus spp. exhibiting some similarities in their sclerotized structures. Thus, our paper provides additional evidence of the high species richness of Cichlidogyrus and the link with their hosts's phylogenetic affinities in LT.
- Klíčová slova
- C. adkoningsi sp. nov., C. antoineparisellei sp. nov., C. habluetzeli sp. nov., C. koblmuelleri sp. nov., C. masilyai sp. nov., C. salzburgeri sp. nov., C. sergemorandi sp. nov., Callochromis, Cardiopharynx, Cichlidae, Congo, Cyphotilapia, Interochromis, Petrochromis, Platyhelminthes, Tylochromis, Xenotilapia,
- Publikační typ
- časopisecké články MeSH
BACKGROUND: Lake Tanganyika harbours the most diverse cichlid assemblage of the Great African Lakes. Considering its cichlid flocks consist of approximately 250 endemic species, we can hypothesize a high species-richness in their often quite host-specific monogenean ectoparasites belonging to Cichlidogyrus Paperna, 1960. Yet, only 24 species were described from Tanganyikan hosts and some host tribes have never been investigated for monogeneans. This study presents the first parasitological examination of species of the tribes Cyprichromini (Cyprichromis microlepidotus (Poll, 1956)), Eretmodini (Eretmodus marksmithi Burgess, 2012 and Tanganicodus irsacae Poll, 1950) and Ectodini (Aulonocranus dewindti (Boulenger, 1899)). Specimens of the ectodine Ophthalmotilapia nasuta (Poll & Matthes, 1962) from which four Cichlidogyrus spp. have been previously described from more southern localities were also studied. Further, we discuss the haptor configuration in Tanganyikan Cichlidogyrus spp. and highlight the morphological diversity of the vagina, and that of the heel, a sclerotized part of the male copulatory organ, absent in some species of Cichlidogyrus. METHODS: Cichlidogyrus spp. were isolated from gills and fixed using GAP. Haptoral and genital hard parts were measured and drawn by means of a phase contrast microscopic examination. RESULTS: We describe eight new species: Cichlidogyrus milangelnari n. sp. on C. microlepidotus; C. jeanloujustinei n. sp. on E. marksmithi; C. evikae n. sp. on T. irsacae; C. aspiralis n. sp., C. glacicremoratus n. sp. and C. rectangulus n. sp. on O. nasuta; and C. pseudoaspiralis n. sp. and C. discophonum n. sp. on A. dewindti. Three haptoral morphotypes were recognized among the new species. Species of Cichlidogyrus from closely related hosts exhibited the same morphotypes. Geographical variation in Cichlidogyrus spp. fauna as observed in O. nasuta and three morphotypes were distinguished. Finally, we listed 111 Cichlidogyrus species, of which 27 and three Tanganyikan species lack sclerotized vagina and heel, respectively, just like 19 and seven species outside of the lake. CONCLUSIONS: Haptoral and genital features in the Tanganyikan Cichlidogyrus fauna reflect the phylogenetic relationships of their cichlid hosts. It seems that several lineages of Cichlidogyrus spp. exist in Lake Tanganyika but further studies are necessary to confirm this hypothesis and answer questions related to Lake Tanganyika and its cichlids.
- Klíčová slova
- Africa, Burundi, Cichlidae, Cichlidogyrus, Cyprichromini, Ectodini, Eretmodini, Monogenea, Platyhelminthes,
- MeSH
- cichlidy parazitologie MeSH
- infekce červy třídy Trematoda epidemiologie parazitologie veterinární MeSH
- jezera parazitologie MeSH
- mužské pohlavní orgány anatomie a histologie MeSH
- nemoci ryb epidemiologie parazitologie MeSH
- Trematoda anatomie a histologie klasifikace genetika MeSH
- vagina anatomie a histologie MeSH
- žábry parazitologie MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Tanzanie epidemiologie MeSH
Four new species of Dactylogyrus Diesing, 1850 are described from the gills of three species of Luciobarbus Heckel collected from various hydrographical basins in northern Morocco: Dactylogyrus scorpius n. sp. from Luciobarbus rifensis Doadrio, Casal-Lopez & Yahyaoui; D. benhoussai n. sp. from L. moulouyensis Pellegrin; and D. varius n. sp. and D. falsiphallus n. sp. from L. maghrebensis Doadrio, Perea & Yahyaoui. The descriptions of the new species are confirmed by molecular data (partial 18S rDNA, ITS1, and partial 28S rDNA sequences). All four species belong to the group of Dactylogyrus species, possessing a cross-shaped ventral bar and a male copulatory organ composed of a loosely coiled copulatory tube and an accessory piece with a capsule-like base and recurved distal portion. Given the high shape variability of the haptoral anchors reported among specimens of D. varius n. sp., three morphological forms within this species (D. varius f. vulgaris, D. varius f. magnus, and D. varius f. dromedarius) are recognised. However, specimens belonging to D. benhoussai n. sp. and D. varius f. vulgaris were morphologically very similar and were discriminated with certainty, only when using molecular data.
- MeSH
- Cyprinidae parazitologie MeSH
- druhová specificita MeSH
- mezerníky ribozomální DNA genetika MeSH
- RNA ribozomální 18S genetika MeSH
- RNA ribozomální 28S genetika MeSH
- Trematoda anatomie a histologie klasifikace genetika MeSH
- žábry parazitologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Maroko MeSH
- Názvy látek
- mezerníky ribozomální DNA MeSH
- RNA ribozomální 18S MeSH
- RNA ribozomální 28S MeSH
The flatworms of the genus Cichlidogyrus Paperna, 1960 (Monogenea: Ancyrocephalidae) are gill parasites of freshwater fish, affecting predominantly the family Cichlidae. Cichlidogyrus tiberianus Paperna, 1960 and Cichlidogyrus dossoui Douëllou, 1993 are among the most widely distributed species of the genus, occurring in several African river basins and infecting many different host species, including the economically important Nile tilapia Oreochromis niloticus (Linnaeus) and redbreast tilapia Coptodon rendalli (Boulenger). Despite their wide distribution, C. tiberianus and C. dossoui have so far been studied only by light microscopy. In this paper they are redescribed on the basis of scanning electron microscopy of newly-collected material. The new material was obtained from redbreast tilapia caught in the Luapula River (D. R. Congo). The haptoral sclerites and genitalia are redescribed and illustrated in detail. Special attention is given to the complex morphology of the male copulatory organ.
- MeSH
- druhová specificita MeSH
- mikroskopie elektronová rastrovací MeSH
- mužské pohlavní orgány ultrastruktura MeSH
- Tilapia parazitologie MeSH
- Trematoda klasifikace izolace a purifikace ultrastruktura MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Kongo MeSH
Lake Tanganyika is well-known for its high species-richness and rapid radiation processes. Its assemblage of cichlid fishes recently gained momentum as a framework to study parasite ecology and evolution. It offers a rare chance to investigate the influence of a deepwater lifestyle in a freshwater fish-parasite system. Our study represents the first investigation of parasite intraspecific genetic structure related to host specificity in the lake. It focused on the monogenean flatworm Cichlidogyrus casuarinus infecting deepwater cichlids belonging to Bathybates and Hemibates. Morphological examination of C. casuarinus had previously suggested a broad host range, while the lake's other Cichlidogyrus species are usually host specific. However, ongoing speciation or cryptic diversity could not be excluded. To distinguish between these hypotheses, we analysed intraspecific diversity of C. casuarinus. Monogeneans from nearly all representatives of the host genera were examined using morphometrics, geomorphometrics and genetics. We confirmed the low host-specificity of C. casuarinus based on morphology and nuclear DNA. Yet, intraspecific variation of sclerotized structures was observed. Nevertheless, the highly variable mitochondrial DNA indicated recent population expansion, but no ongoing parasite speciation, confirming, for the first time in freshwater, reduced parasite host specificity in the deepwater realm, probably an adaptation to low host availability.
- MeSH
- analýza hlavních komponent MeSH
- Bayesova věta MeSH
- biologická evoluce MeSH
- cichlidy genetika parazitologie MeSH
- fylogeneze MeSH
- genetická variace MeSH
- haplotypy MeSH
- hostitelská specificita MeSH
- jezera MeSH
- paraziti genetika MeSH
- ploštěnci genetika MeSH
- populační dynamika MeSH
- žábry parazitologie MeSH
- zeměpis MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Tanzanie MeSH
BACKGROUND: Lake Tanganyika is the world's second deepest lake. Its diverse cichlid assemblage offers a unique opportunity for studying a deep-water host-parasite model in freshwater. Low host specificity and a broad host range including representatives of the Bathybatini tribe in the only monogenean parasite described from this habitat, Cichlidogyrus casuarinus Pariselle, Muterezi Bukinga & Vanhove, 2015 suggest a link between lower specificity and lower host density. Conversely, high host specificity and species richness are reported for monogeneans of the lake's littoral cichlids. We further investigated whether the deep-water environment in Lake Tanganyika is really monogenean species-depauperate by investigating the monogenean fauna of Trematocara unimaculatum (a representative of the tribe Trematocarini, the sister lineage of the Bathybatini) and Benthochromis horii, a member of the tribe Benthochromini, found in the same deep-water habitat as the already known hosts of C. casuarinus. METHODS: Sclerotised structures of the collected monogenean individuals were characterised morphologically using light microscopy and morphometrics. RESULTS: Both examined cichlid species are infected by a single monogenean species each, which are new to science. They are described as Cichlidogyrus brunnensis n. sp., infecting T. unimaculatum, and Cichlidogyrus attenboroughi n. sp., parasitising on B. horii. Diagnostic characteristics include the distal bifurcation of the accessory piece in C. brunnensis n. sp. and the combination of long auricles and no heel in C. attenboroughi n. sp. In addition C. brunnensis n. sp. does not resemble C. casuarinus, the only species of Cichlidogyrus thus far reported from the Bathybatini. Also Cichlidogyrus attenboroughi n. sp. does not resemble any of the monogenean species documented from the pelagic zone of the lake and is among the few described species of Cichlidogyrus without heel. CONCLUSIONS: As two new and non-resembling Cichlidogyrus species are described from T. unimaculatum and B. horii, colonisation of the deep-water habitat by more than one morphotype of Cichlidogyrus is evident. Based on morphological comparisons with previously described monogenean species, parasite transfers with the littoral zone are possible. Therefore, parasites of pelagic cichlids in the lake do not seem to only mirror host phylogeny and the evolutionary history of this host-parasite system merits further attention.
- Klíčová slova
- Benthochromis horii, Cichlidae, Cichlidogyrus, Monogenea, Trematocara unimaculatum,
- MeSH
- biodiverzita * MeSH
- cichlidy parazitologie MeSH
- fylogeneze MeSH
- hostitelská specificita MeSH
- infekce červy třídy Trematoda parazitologie veterinární MeSH
- interakce hostitele a parazita MeSH
- jezera * parazitologie MeSH
- nemoci ryb parazitologie MeSH
- Trematoda anatomie a histologie klasifikace izolace a purifikace ultrastruktura MeSH
- žábry parazitologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Tanzanie MeSH
Monogenea is one of the most species-rich groups of parasitic flatworms worldwide, with many species described only recently, which is particularly true for African monogeneans. For example, Cichlidogyrus, a genus mostly occurring on African cichlids, comprises more than 100 nominal species. Twenty-two of these have been described from Lake Tanganyika, a famous biodiversity hotspot in which many vertebrate and invertebrate taxa, including monogeneans, underwent unique and spectacular radiations. Given their often high degrees of host specificity, parasitic monogeneans were also used as a potential tool to uncover host species relationships. This study presents the first investigation of the monogenean fauna occurring on the gills of endemic 'Gnathochromis' species along the Burundese coastline of Lake Tanganyika. We test whether their monogenean fauna reflects the different phylogenetic position and ecological niche of 'Gnathochromis' pfefferi and Gnathochromis permaxillaris. Worms collected from specimens of Limnochromis auritus, a cichlid belonging to the same cichlid tribe as G. permaxillaris, were used for comparison. Morphological as well as genetic characterisation was used for parasite identification. In total, all 73 Cichlidogyrus individuals collected from 'G.' pfefferi were identified as C. irenae. This is the only representative of Cichlidogyrus previously described from 'G.' pfefferi, its type host. Gnathochromis permaxillaris is infected by a species of Cichlidogyrus morphologically very similar to C. gillardinae. The monogenean species collected from L. auritus is considered as new for science, but sample size was insufficient for a formal description. Our results confirm previous suggestions that 'G.' pfefferi as a good disperser is infected by a single monogenean species across the entire Lake Tanganyika. Although G. permaxillaris and L. auritus are placed in the same tribe, Cichlidogyrus sp. occurring on G. permaxillaris is morphologically more similar to C. irenae from 'G.' pfefferi, than to the Cichlidogyrus species found on L. auritus. Various evolutionary processes, such as host-switching or duplication events, might underlie the pattern observed in this particular parasite-host system. Additional samples for the Cichlidogyrus species occuring on G. permaxillaris and L. auritus are needed to unravel their evolutionary history by means of (co-)phylogenetic analyses.
- Klíčová slova
- Cichlidogyrus, Ectoparasites, Lake Tanganyika, Limnochromini, Tropheini,
- Publikační typ
- časopisecké články MeSH