Volodimir Sarabeev

DESCRIPTION AND MORPHOMETRICAL VARIABILITY OF A NEW SPECIES OF LIGOPHORUS AND OF LIGOPHORUS CHABAUDI (MONOGENEA: DACTYLOGYRIDAE) ON MUGIL CEPHALUS (TELEOSTEI) FROM THE MEDITERRANEAN BASIN

A comparative morphological study of specimens of Ligophorus spp. from Mugil cephalus in western Mediterranean and the Black Sea localities has been carried out, indicating the presence of 2 distinct forms, i.e., Ligophorus chabaudi and Ligophorus cephali n. sp. A detailed description of the latter and an up-to-date redescription of L. chabaudi are provided. The existence of these 2 morphological species was additionally supported by principal component analysis based on 19 metric characters of 87 specimens arranged in samples defined by parasite species and geographical locality. The analysis indicated consistent differences between species but not between localities; this pattern was well supported by jackknife procedures. Linear discriminant analyses showed that the main metric differences between the 2 species were attributable to the lengths of the dorsal and ventral bars and to the uncinulus length; use of the first 2 variables was enough to allocate all specimens studied to either form. The erection of L. cephali n. sp. raises the number of sympatric Mediterranean species of Ligophorus on M. cephalus to 3. The known geographical ranges of these species are compared.

LIGOPHORUS PILENGAS N. SP. (MONOGENEA: ANCYROCEPHALIDAE) FROM THE INTRODUCED SO-IUY MULLET, MUGIL SOIUY (TELEOSTEI: MUGILIDAE), IN THE SEA OF AZOV AND THE BLACK SEA

The monogenean Ligophorus chabaudi was originally described on the gills of the flathead mullet, Mugil cephalus, and was subsequently reported on the So-iuy mullet, Mugil soiuy. However, the morphology of sclerotized parts and multivariate statistical analyses suggest that the form from the So-iuy mullet represents a new species. This study provides a description of the new species Ligophorus pilengas n. sp. and provides additional morphological data concerning the morphology of the ventral bar that might be useful for the diagnosis of Ligophorus. Ligophorus pilengas n. sp. is the second species of Ligophorus reported on the So-iuy mullet. Zoogeographical records indicate that L. pilengas n. sp. was probably introduced to the Black Sea and the Sea of Azov from the western Pacific Ocean together with its host.

TAXONOMIC STATUS OF LIGOPHORUS MUGILINUS (HARGIS, 1955) (MONOGENEA: ANCYROCEPHALIDAE), WITH A DESCRIPTION OF A NEW SPECIES OF LIGOPHORUS FROM MUGIL CEPHALUS (TELEOSTEI: MUGILIDAE) IN THE MEDITERRANEAN BASIN

Ligophorus mugilinus was originally described on the flathead mullet Mugil cephalus from the Gulf of Mexico. The species was later recorded in the Mediterranean Sea on the flathead mullet and in the Caribbean Sea on the white mullet Mugil curema. After examination of the type material and additional specimens of Ligophorus from the northwest Atlantic coast, the Caribbean Sea, and the Mediterranean and Black Sea, we observed morphological differences concerning haptoral and male copulatory structures between L. mugilinus from the northwest Atlantic and the forms from the Mediterranean and Black Seas. Accordingly, the latter specimens are described as a new species, Ligophorus mediterraneus n. sp. A redescription of L. mugilinus, including new morphometric data, is also given. The morphometric analysis of the Caribbean specimens suggested that their ascription to L. mugilinus is uncertain, but additional material is needed to clarify their specific identity. The results of this study, together with previous zoogeographical evidence, indicate that flathead mullets from different seas harbor different species complexes of Ligophorus. Given the coastal habits of the host, it is suggested that open oceans could act as geographical barriers favoring speciation within disjointed flathead mullet populations.

Three new species of Ligophorus (Monogenea: Dactylogyridae) on the gills of Mugil cephalus (Teleostei: Mugilidae) from the Japan Sea

Comparative morphology and multivariate morphometric analysis of monogeneans collected on flathead mullets Mugil cephalus from 2 Russian localities of the Japan Sea revealed the presence of 3 new species of Ligophorus, namely, L. domnichi n. sp., L. pacificus n. sp., and L. cheleus n. sp., which are described herein. So far, only 1 species of dactylogyrid monogenean identified as Ligophorus chabaudi was known on flathead mullets in this sea, but after comparison with the present material, we propose that this form actually represents L. domnichi n. sp. Results support previous zoogeographical evidence, suggesting that flathead mullets from different seas harbor different species complexes of Ligophorus. One interesting finding is that the 3 new species have a U-shaped ovary, whereas ovate ovaries have been reported in previous descriptions of species of the genus, e.g., L. vanbenedenii, L. parvicirrus, L. imitans, and L. chongmingensis. The U-shaped ovary was revealed only when the worms were observed in lateral view. The additional examination of L. vanbenedenii, L. parvicirrus, L. imitans, and L. pilengas specimens from our collections also revealed a U-shaped ovary in these forms as well. Further studies should establish whether or not this character is shared by all members of the genus.

Molecular phylogeny of species of Ligophorus (Monogenea: Dactylogyridae) and their affinities within the Dactylogyridae

The taxonomic framework of Ligophorus, monogenean specialists of the gills of grey mullets (Mugilidae), is evaluated and its interspecific relationships are assessed for the first time using molecular data. The position of Ligophorus within the paraphyletic Ancyrocephalinae is re-assessed based on newly sequenced species. Furthermore, the relationship between morphometric and genetic interspecific similarities is evaluated. Partial 28S and complete ITS1 rDNA sequences from representatives of 14 of the 16 nominal species of Ligophorus from the Mediterranean, Black and Azov Seas were analysed together with published sequences of members of the Dactylogyridae. The phylogenetic analyses of the Dactylogyridae (i) confirmed the position of Ligophorus within the marine Ancyrocephalinae; (ii) revealed a sister relationship between Ergenstrema and Ligophorus, whose species are all exclusive parasites of grey mullets; and (iii) substantiated the affinities of Ergenstrema with the marine Ancyrocephalinae. The phylogenetic analysis restricted to Ligophorus confirmed the distinct status of the included species. The ITS1 region provided the highest divergence between species and phylograms with the strongest branch support. Both the 28S and ITS1 phylograms revealed two main clades. One included species from hosts with Mediterranean and NE Atlantic distribution and another was formed by species parasitising several Liza spp., including Lz. haematocheilus from the Northwestern Pacific, and Mugil cephalus, which suggests an origin outside the Mediterranean for the latter clade. The phylogenetic evidence presented herein indicated that a combination of host-switching and lineage duplication events accounted for the diversification of this genus in the Mediterranean basin. The agreement between molecular and morphological interspecific similarities observed in Ligophorus supports the validity of morphometric characters used for species identification.

Phylogeny of the Atlantic and Pacific species of Ligophorus (Monogenea: Dactylogyridae): morphology vs. molecules.

Within ectoparasitic fish monogeneans, the genus Ligophorus contains a high number of species from which several were recently described. The precise determination of their taxonomic status requires robust diagnostic morphologic features that rely predominantly on a restricted set of sclerotized structures. In the present study, these morphological characters were used for the reconstruction of a phylogenetic tree, which was compared with a tree built from molecular data (28S and ITS1 DNA sequences). Thirty-eight morphological characters were used in 29 species of Ligophorus from the Atlantic and Pacific regions and 5 species within close genera of Dactylogyridae. The morphological and molecular phylogenetic trees are congruent and suggest that the genus Ligophorus is monophyletic, and that species parasitizing Liza spp. and Chelon labrosus occupy basal positions. The present study suggests that host switching is a common event in this host-parasite association, because about half of the species infecting the same host species are not close relatives. Following host switching, dispersal with vicariance is probably an important force shaping the present distribution and diversity of Ligophorus. The pattern of occurrence of Ligophorus spp. on Mugil cephalus supports that reproductive isolation and therefore parallel speciation are taking place among these parasitic organisms.

Ligophorus pilengas Sarabeev & Balbuena, 2004 (Monogenea: Ancyrocephalidae) is proposed as the senior synonym of L. gussevi Miroshnichenko & Maltsev, 2004

Ligophorus pilengas Sarabeev & Balbuena, 2004 and L. gussevi Miroshnichenko & Maltsev, 2004, both recently described as new species from the so-iuy mullet Mugil soiuy in the Sea of Azov and Black Sea, were compared. A morphometric analysis of both forms strongly suggests that they represent the same species. According to the ‘Principle of priority’, L. pilengas is proposed as a senior synonym of L. gussevi.

Helminth species richness of introduced and native grey mullets (Teleostei: Mugilidae).

Quantitative complex analyses of parasite communities of invaders across different native and introduced populations are largely lacking. The present study provides a comparative analysis of species richness of helminth parasites in native and invasive populations of grey mullets. The local species richness differed between regions and host species, but did not differ when compared with invasive and native hosts. The size of parasite assemblages of endohelminths was higher in the Mediterranean and Azov-Black Seas, while monogeneans were the most diverse in the Sea of Japan. The helminth diversity was apparently higher in the introduced population of Liza haematocheilus than that in their native habitat, but this trend could not be confirmed when the size of geographic range and sampling efforts were controlled for. The parasite species richness at the infracommunity level of the invasive host population is significantly lower compared with that of the native host populations that lends support to the enemy release hypothesis. A distribution pattern of the infracommunity richness of acquired parasites by the invasive host can be characterized as aggregated and it is random in native host populations. Heterogeneity in the host susceptibility and vulnerability to acquired helminth species was assumed to be a reason of the aggregation of species numbers in the population of the invasive host.

Testing the enemy release hypothesis: abundance and distribution patterns of helminth communities in grey mullets (Teleostei: Mugilidae) reveal the success of invasive species

The abundance and aggregation patterns of helminth communities of two grey mullet hosts, Liza haematocheilus and Mugil cephalus, were studied across 14 localities in Atlantic and Pacific marine areas. The analysis matched parasite communities of (i) L. haematocheilus across its native and introduced populations (Sea of Japan and Sea of Azov, respectively) and (ii) the introduced population of L. haematocheilus with native populations of M. cephalus (Mediterranean, Azov-Black and Japan Seas). The total mean abundance (TMA), as a feature of the infection level in helminth communities, and slope b of the Taylors power law, as a measure of parasite aggregation at the infra and component-community levels, were estimated and compared between host species and localities using ANOVA. The TMA of the whole helminth community in the introduced population of L. haematocheilus was over 15 times lower than that of the native population, but the difference was less pronounced for carried (monogeneans) than for acquired (adult and larval digeneans) parasite communities. Similar to the abundance pattern, the species distribution in communities from the invasive population of L. haematocheilus was less aggregated than from its native population for endoparasitic helminths, including adult and larval digeneans, while monogeneans showed a similar pattern of distribution in the compared populations of L. haematocheilus. The aggregation level of the whole helminth community, endoparasitic helminths, adult and larval digeneans was lower in the invasive host species in comparison with native ones as shown by differences in the slope b. An important theoretical implication from this study is that the pattern of parasite aggregation may explain the success of invasive species in ecosystems. Because the effects of parasites on host mortality are likely dose-dependent, the proportion of susceptible host individuals in invasive species is expected to be lower, as the helminth distribution in the invasive host was featured by a higher number of uninfected hosts and a shorter distribution tail when compared with native species.

Invasive parasites are detectable by their abundance-occupancy relationships: the case of helminths from Liza haematocheilus (Teleostei: Mugilidae)

The biogeographic patterns of abundance and prevalence of helminths from Liza haematocheilus were studied across its native (Sea of Japan) and introduced (Sea of Azov) distribution ranges. Abundance-occupancy relationships (AORs) were tested for the core-satellite and enemy release (ERH) species hypotheses in eight and 14 host samples from the native and introduced host ranges, respectively. The AOR model fitted parasite data extremely well, irrespective of whether the host or the parasite species were native or invasive. Except for co-introduced monogeneans, species were less abundant and prevalent in the introduced host population than in the native one, which agrees well with the ERH. Two occupancy patterns were observed. A unimodal, right-skewed distribution of prevalence frequency was common for the acquired groups of helminth parasites in the introduced range, whereas a bimodal distribution was more common in the native range. Core species in the native range were monogeneans, adult and larval digeneans, whereas host-specific, co-introduced monogeneans were the only core species in the introduced range. Acquired grey-mullet specialists and host generalists infected only a small portion of the introduced host population with low mean abundance. These results indicate that strict host specificity, together with a direct life cycle, are the traits that enabled helminth species to entirely occupy the invasive host population. The AORs showed that parasite individuals tend to accumulate in a relatively small fraction of susceptible introduced hosts, probably as an adaptation to enhance mating opportunities, thereby providing a mechanistic explanation of the ERH. All this evidence suggests that co-introduced and acquired species use the introduced host population in very different ways. Therefore, we posit that the examination of AORs can be instrumental in understanding the role of co-introduced parasites in invasion theory.