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Scanning electron micrographs of food items found in the digestive tract of Aglajidae specimens: (A) Kynorhyncha sp. in Melanochlamys diomedea USNM 771859; (B) ?exoskeleton of Isopoda in Odontoglaja guamensis ZMBM 94030; (C) Enoploidea nematodes in Melanochlamys diomedea USNM 771859; (D) detail of the mouth of the nematodes in Melanochlamys diomedea USNM 771859; (E) ?fragment of a spicule of Holothuria in Odontoglaja guamensis ZMBM 94030; (F) complete specimen of Gobiidae fish in Navanax inermis CNMO 1818. Scale bars A: 20 m m; B: 30 m m: C and E: 100 m m; D: 10 m m, F: 5 mm.
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Aglajidae is a family of tropical and temperate marine Cephalaspidea gastropod slugs regarded as active predators. In order to better understand their food habits and trophic interactions, we have studied the diet of all genera through the examination of gut contents. Specimens were dissected for the digestive tract and gut contents were removed an...
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... Aglajids, including members of the Chelidonura genus, detect these mucus trails using specialised sensory organs, allowing them to hunt down mobile prey and feed on it by ingesting it whole as they lack a radula (Paine, 1963;Rudman, 1978;Kohn et al., 1983;Davies and Blackwell, 2007;Ng et al., 2013). Notably, observations have indicated that Chelidonura species prefer epifaunal organisms, including flatworms, slugs, and shelled gastropods (Silva and Malaquias, 2016). This dietary preference highlights the selective feeding behaviour of Chelidonura, emphasising their ecological role as predators within marine ecosystems. ...
... C. livida utilizes advanced visual capabilities, sensory cilia, and Hancock's chemosensory organ to enhance its olfactory and overall sensory perception. This adaptation enables the detection of various epifaunal prey organisms such as flatworms, slugs, and shelled gastropods which have been reported by Silva and Malaquias (2016) as the primary prey for this species. This dietary preference underscores the selective feeding behaviour of Chelidonura and highlights its ecological role as a predator within marine ecosystems. ...
Chelidonura livida, commonly known as the blue velvet headshield slug, is a sea slug within the family Aglajidae of the phylum Mollusca. This species was first described by Yonow in 1994 from the Red Sea coast of Israel. It exhibits a wide distribution, ranging from Africa to the Indo-Pacific region, extending to the coasts of Japan. This study documents the first occurrence of C. livida from the Gujarat coast of India where the specimens were observed at dusk, moving through sand flats adjacent to a Halophila decipiens seagrass bed off the coast of Mithapur. This report provides a detailed morphological description of C. livida and offers comprehensive insights into its ecology. Observations include the species’ burrowing behaviour, feeding habits, prey preferences, and reproductive strategies. The addition of this species elevates the total count of sea slug species in Gujarat to 97.
... Heterobranch sea slugs of the family Aglajidae typically represent colorful and active predators (Rudman, 1972a;Yonow, 1992;Malaquias, 2014;Zamora-Silva, Malaquias, 2016). Commonly the radula and gizzard plates are absent, the shell is internal, fragile, and reduced, and rarely used in species identification (Rudman, 1972b;Gosliner, 2011Gosliner, , 2015Cooke et al., 2014). ...
Philinopsis gigliolii (Tapparone Canefri, 1874) was described under the name Aglaja gigliolii based on preserved material from the Pacific coast of Japan, collected during an expedition of the Italian warship Magenta in 1864-1868. Currently, this species is considered a subjective synonym of P. speciosa Pease, 1860, described from Hawaii, despite their morphological differences. To clarify the species status of P. gigliolii we have conducted a molecular phylogenetic analysis of the genus Philinopsis using COI, 16S, and histone H3 molecular markers, which included a specimen of P. gigliolii from Peter the Great Bay, the Sea of Japan. Our results confirm that P. gigliolii represents a distinct valid species, which shows both morphological and molecular differences with P. speciosa. The latter species is recovered paraphyletic and clearly needs further taxonomical revision. At the same time, the molecular analysis indicates that Australian species P. taronga (Allan, 1933) is conspecific to P. gigliolii (only two molecular substitutions were identified in 16S), and these species show many similarities in both external and internal morphology. We consider P. taronga a junior subjective synonym of P. gigliolii. Formally Chelidonura aureopunctata Rudman, 1968, described from New Zealand, is considered a junior subjective synonym of P. gigliolii as well. Philinopsis gigliolii has an antitropical distribution, its range includes subtropical and temperate areas of the Pacific Ocean in both hemispheres (the Sea of Japan, the Yellow Sea, the Pacific coast of Japan; SouthEast Australia and the northern coast of New Zealand). Three hypotheses may explain this distribution pattern. (1) The antitropical distribution results from the historical disjunction across tropical latitudes following the abiotic or biotic factors. (2) Philinopsis gigliolii may be widely distributed in temperate and tropical waters of the Pacific Ocean but be overlooked in the central part of its geographic range due to external similarities to other species of the genus. (3) The last hypothesis suggests the anthropogenic transportation of P. gigliolii. Further sampling activity and comparative genetic analyses may contribute to a better understanding of this very interesting biogeographic pattern. How to cite this article: Chaban E.M., Ekimova I.A., Chernyshev A.V. 2024. Philinopsis gigliolii (Gastropoda: Heterobranchia: Aglajidae) from the Sea of Japan: validity, synonymy and biogeography // Invert. РЕЗЮМЕ: Philinopsis gigliolii (Tapparone Canefri, 1874) был описан как Aglaja gigliolii по фиксированному материалу, собранному у тихоокеанского побережья Японии во время экспедиции на итальянском военном корабле «Маджента» в 1864-1868 гг. В настоящее время этот вид считается младшим субъективным синонимом P. speciosa Pease, 1860, описанного с Гавайских островов, несмотря на их морфологические различия. Для уточнения таксономического статуса P. gigliolii мы провели молекулярно-филогенетический анализ рода Philinopsis, включая экземпляр P. gigliolii из залива Петра Великого Японского моря, с использованием трех молекулярных маркеров, представляющих частичные фрагменты цитохром с оксидазы субъединицы I (COI), 16S rRNA и гистона H3 (H3). Наши результаты подтверждают, что P. gigliolii представляет собой валидный вид, который имеет молекулярные и морфологические отличия от P. speciosa. Последний вид признан парафилетическим и явно нуждается в дальнейшей таксономической ревизии. В то же время молекулярный анализ показывает, что австралийский вид P. taronga (Allan, 1933) конспецифичен P. gigliolii (в 16S выявлены всего 2 молекулярные замены), и эти виды обнаруживают большое сходство как во внешней, так и во внутренней морфологии. Мы считаем P. taronga младшим субъективным синонимом P. gigliolii. Формально, Chelidonura aureopunctata Rudman, 1968, описанную из прибрежья Но-вой Зеландии, также следует считать младшим субъективным синонимом P. gigliolii. Philinopsis gigliolii имеет антитропическое распространение: его ареал включает субтропические и умеренные районы Тихого океана в обоих полушариях (Японское и Желтое моря, тихоокеанское побережье Японии; юго-восточная Австралия и северное побережье Новой Зеландии). Три гипотезы могут объяснить такую картину распре-деления: 1) антитропическое распределение является результатом исторического разделения ареала через тропические широты как следствие действия абиотических или биотических факторов; 2) Philinopsis gigliolii может быть широко распространен в тропических и умеренных водах Тихого океана, но не отмечен в центральной части ареала из-за внешнего сходства с другими видами рода; 3) последняя гипотеза предполагает антропогенный перенос P. gigliolii. Дополнительный сбор образцов и дальнейший генетический анализ могут способствовать лучшему пониманию этой очень интересной биогеографической модели. Как цитировать эту статью: Chaban E.M., Ekimova I.A., Chernyshev A.V. 2024. Philinopsis gigliolii (Gastropoda: Heterobranchia: Aglajidae) from the Sea of Japan: validity, synonymy and biogeography // Invert.
... Although histochemical and ultrastructural data are available only for a limited number of species, it seems that the digestive system of aglajids differs from that of anaspideans and other cephalaspideans, both herbivores and carnivores, not only in the histology of salivary glands but also in other aspects, such as the absence of a gizzard and lack of radula in all but one genus. Thus, in what concerns the digestive system, aglajids can be regarded as highly derived cephalaspideans, which is probably related with their particular feeding strategy by prey suction (Lobo-da- Cunha et al., 2009Cunha et al., , 2016Zamora-Silva and Malaquias, 2016). ...
... In aglajids, preys are digested in the voluminous crop (Figure 7a-g). The larger prey shells clean of soft tissues are regurgitated after digestion but smaller indigestible hard parts of prey can pass through the intestine (Rudman, 1972;Zamora-Silva and Malaquias, 2016). In the aglajid P. depicta, the crop contains mucous cells that only secrete polysaccharides (Figures 7d and 8a; Lobo-da- Cunha et al., 2011a), and the crop of the aglajid A. tricolorata is devoid of any secretory cells (Figure 7f,g). ...
In most euopisthobranchs, the buccal cavity contains the radula. A pair of salivary glands releases into the buccal cavity a fluid for agglutination and lubrication of the food during feeding and ingestion. The esophagus can include a crop to accommodate ingested food, and many euopisthobranchs possess a gizzard with hard plates for food grinding. The stomach is embedded in the digestive gland and linked to it by a system of ducts. The digestive tract lumen is lined by an epithelium formed by ciliated and nonciliated absorptive cells, intermingled with different kinds of secretory cells. The absorptive epithelial cells are covered by microvilli and contain several lysosomes for intracellular digestion of particles captured by endocytosis. The digestive gland comprises multiple digestive diverticula formed by digestive cells engaged in intracellular digestion, and basophilic cells that secrete enzymes for extracellular digestion. The intestine is usually long ending in the anus.
... They are common on sandy bottoms or can be found on growing algae. Flatworms are the main prey of Chelidonura; at the same time, representatives of this genus also prey on small bivalves and gastropods (Zamora-Silva and Malaquias, 2016). The Badenian Ch. radwanskii was found in sediments of the littoral zone (Bałuk, 2018). ...
The Sarmatian Paleaglaja jolkii V. Anistratenko from the family Aglajidae is transferred to the genus Chelidonura A. Adams. Additional morphological characteristics and data on the stratigraphic range are given for this species. It is proposed assumption the Sarmatian Ch. jolkii derived from the Badenian Ch. radwanskii Bałuk, 2018.
... Some species are much better studied morphologically than others (Tchang-Si, 1934;Rudman, 1972aRudman, , b, c, 1974Rudman, , 1978. Several studies have considered the feeding (Yonow, 1992;Zamora-Silva & Malaquias, 2016) and reproductive behaviour (Leonard & Lukowiak, 1985;Anthes & Michiels, 2007;Anthes et al., 2008;Turner & Wilson, 2012) of aglajids. ...
In this paper we describe the new genus Aglaona, the first abyssal genus of the family Aglajidae, comprising two new species: Aglaona rudmani sp. nov. from the Sea of Okhotsk (inhabiting a depth of 3206 m) and Aglaona valdesi sp. nov. from the Pacific slope of the Kuril Islands (at a depth of 3374–3580 m). For species descriptions and inference of relationships, we have followed an integrative approach, including molecular phylogenetic analyses based on four markers (COI, 16S, H3 and 28S) and a morphological analysis based on traditional anatomical dissections and scanning electron microscopy. The new genus is characterized by a well-developed radula with marginal teeth (2:1:0:1:2) and an internal bulloid shell with a wing-like parietal callus. External and internal morphology of Aglaona gen. nov. species is similar to that of the philinoid genus Laona (family Laonidae). Phylogenetic analyses support the inclusion of the new genus in the family Aglajidae, but its sister-relationships are unresolved. Our results suggest that Aglaona gen. nov. possesses several plesiomorphic characters, and that the reduction of shell and radula in Aglajidae occurred in parallel in different lineages.
... In 1998, two related depsipeptides within the kulolide superfamily, kulomo'opunalide-1 (5) and -2 (6), were isolated from the marine gastropod Philinopsis speciosa, collected in the intertidal area offshore of O'ahu, Hawai'i (Nakao et al., 1998). P. speciosa is a generalist carnivore, predating on opisthobranch molluscs, including S. striatus (Nakao et al., 1998;Zamora-Silva and Malaquias, 2016). In feeding experiments, Nakao et al. (1998) demonstrated that P. speciosa fed on S. striatus, and they were able to isolate kulolide-1, a related depsipeptide, from both the predator and its prey. ...
A multidisciplinary approach was used to assess chemical ecological dietary interactions between marine organisms as a tool to isolate novel ecologically relevant compounds with biotechnological potential. First, laboratory-based feeding preference assays of the sea hare Dolabrifera nicaraguana (previously known as D. dolabrifera ), an anaspidean mollusc, were conducted by simultaneously offering six food options collected from nearby tidal pools in the Coiba National Park in the Tropical Eastern Pacific of Panama. An evaluation of preferred dietary repertoire revealed D. nicaraguana significantly preferred cf. Lyngbya sp. over the cyanobacterium Symploca sp., green alga Chaetomorpha sp., and red alga Spyridia sp. A no-choice feeding assay using cf. Lyngbya sp. or green alga Cladophora sp. supported this finding. Secondly, we conducted bioactivity-guided fractionation using the preferred food source of D. nicaraguana , the ‘hair-like” cf. Lyngbya sp. from which we also isolated and elucidated two new depsipeptide compounds, veraguamide M ( 1 ) and veraguamide N ( 2 ). Veraguamides M ( 1 ) and N ( 2 ) showed in vitro activity toward the malaria-causing parasite Plasmodium falciparum with GI 50 values of 4.2 and 4.3 μM, respectively, and therapeutic windows of 7.0–8.0 (based on moderate cytotoxicities to mammalian Vero cells with GI 50 values of 29.3 and 34.1 μM, respectively). Veraguamide N ( 2 ) was also active against Leishmania donovani , the causative agent of visceral leishmaniasis, with a GI 50 value of 6.9 μM. We then evaluated sequestration of these new compounds by D. nicaraguana used in the feeding assays and found trace amounts of the dietary sequestered compounds. Finally, we evaluated sequestration of these new compounds by the sea hare Stylocheilus rickettsi (previously known as S. striatus ) that were grazing on the cf. Lyngbya sp. used in the feeding assays and found both to be sequestered. This study is the first example whereby compounds with significant activity against tropical parasites have been found in both the sea hare S. rickettsi and its cyanobacterial food source. These results suggest that chemical ecological studies involving sea hares and cyanobacteria continue to provide a diverse source of bioactive compounds with biotechnological potential.
... Cephalaspideans include a variety of species commonly referred to as headshield slugs and bubble snails. They range in diet from herbivory to carnivory (Eilertsen and Malaquias, 2013;Zamora-Silva and Malaquias, 2016;Gosliner et al., 2018), with different groups possessing adaptations related to feeding and diet, 1996; Kabat, 1998;Smith, 1998). Historically, this similarity of structures led to many of the head shield-bearing heterobranchs being grouped together taxonomically within Cephalaspidea, but more recent work has reassigned some of these species into other clades (see below). ...
Cephalaspidea is an order of marine gastropods found worldwide, often in sandy or muddy habitats, which has a convoluted taxonomic history based on convergent or ill-defined morphological characters. The cephalaspidean shell—which can be external and robust, internal, or altogether absent in the adult—is of particular interest in this group, and a well-resolved phylogeny can give us greater insight into the evolution of this character. Molecular data have clarified many relationships within Cephalaspidea, but studies involving just a few Sanger sequenced phylogenetic markers remain limited in the resolution they provide. Here we take a phylogenomic approach, the first to address internal cephalaspidean relationships, sequencing and assembling transcriptomes de novo from 22 ingroup taxa—representing the five currently accepted superfamilies, 10 of the 21 currently recognized families, and 21 genera—and analyzing these along with publicly available data. We generated two main datasets varying by a minimum taxon occupancy threshold (50% and 75%), and analyzed these using maximum likelihood, Bayesian inference and a coalescence-based method. We find a consistent, well-supported topology, with full support across most nodes including at the family and genus level, which also appears to be robust to the effect of compositional heterogeneity among amino acids in the dataset. Our analyses find Newnesioidea as the sister group to the rest of Cephalaspidea. Within the rest of the order, Philinoidea is the sister group to a clade that comprises (Bulloidea (Haminoeoidea, Cylichnoidea)). There is strong support for several previously suggested, but tenuously supported relationships such as the genus Odontoglaja nesting within the family Aglajidae, and a sister group relationship between Gastropteridae and Colpodaspididae, with Philinoglossidae as their sister group. We discuss these results and their implications in the context of current cephalaspidean taxonomy and evolution. Genomic-scale data give a backbone to this group of snails and slugs, and hold promise for a completely resolved Cephalaspidea.
... Several species of nudibranchs, such as Armina spp., are widely distributed in the Mediterranean and Atlantic coasts, namely Armina maculata Rafinesque, 1814 and Armina tigrina Rafinesque, 1814 [7]. The cephalaspidean Aglaja tricolorata Renier, 1807 shares a similar geographical distribution, being also recorded along the Atlantic coast [8]. Despite their ubiquitous distribution, inhabiting sub-tropical and temperate shores [9], the above-mentioned species are considered scarce and/or seldom found, the chemical investigation of both genera being virtually absent [10]. ...
... Being evident that dietary sources impact fatty acids content of marine invertebrates, it is relevant to refer that the three species are carnivorous but differ on their feeding behavior. Despite the reports on the dietary habits of Aglaja felis, feeding upon foraminiferans, the specific diet of A. tricolorata is unknown [8]. Concerning the Arminidae under study, A. maculata often feeds on the pennatulacean Veretillum cynomorium [23]. ...
Bioprospection of marine invertebrates has been predominantly biased by the biological richness of tropical regions, thus neglecting macro-organisms from temperate ecosystems. Species that were not the object of studies on their biochemical composition include the Heterobranchia gastropods Armina maculata, Armina tigrina and Aglaja tricolorata, inhabitants of the Portuguese Atlantic coastal waters. Here, we present for the first time the fatty acid profile of neutral lipids and homarine content of these three species. Qualitative and quantitative differences in the fatty acid content among species points to the existence of a fatty acid profile of neutral lipids, particularly of each genus. The results from cytotoxicity assays, using the acetonic extracts of the gastropods on human gastric adenocarcinoma (AGS) and human lung adenocarcinoma (A549) cell lines, revealed a pronounced cytotoxic effect of the A. tigrina extract on both cell lines (IC50 values of 68.75 and 69.77 μg mL−1 for AGS and A549, respectively). It is worth noting the significant reduction of NO levels in LPS-challenged RAW 264.7 macrophages exposed to A. tricolorata extract, at concentrations as low as 125 μg mL−1.
... Besides taxonomic diversity, species living in marine, freshwater and terrestrial ecosystems, both herbivores and carnivores, were included to cover habitat and diet diversity. These herbivores include species feeding on microalgae, macroalgae or plants, whereas the carnivores include species eating protozoans or metazoans [20,21]. Ultrastructural observations were undertake in species containing mannitol oxidase activity, in order to investigate the correlation between this enzyme and the presence of tubular structures in digestive gland cells. ...
Mannitol oxidase and polyol dehydrogenases are enzymes that convert polyalcohols into sugars. Mannitol oxidase was previously investigated in terrestrial snails and slugs, being also present in a few aquatic gastropods. However, the overall distribution of this enzyme in the Gastropoda was not known. Polyol dehydrogenases are also poorly studied in gastropods and other mollusks. In this study, polyalcohol oxidase and dehydrogenase activities were assayed in the digestive gland of 26 species of gastropods, representing the clades Patellogastropoda, Neritimorpha, Vetigastropoda, Caenogastropoda and Heterobranchia. Marine, freshwater and terrestrial species, including herbivores and carnivores were analyzed. Ultrastructural observations were undertake in species possessing mannitol oxidase, in order to investigate the correlation between this enzyme and the presence of tubular structures known to be associated with it. Mannitol oxidase activity was detected in the digestive gland of herbivores from the clades Caenogastropoda and Heterobranchia, but not in any carnivores or in herbivores from the clades Patellogastropoda, Neritimorpha and Vetigastropoda. In most of the species used in this study, dehydrogenase activities were detected using both D-mannitol and D-sorbitol as substrates. Nevertheless, in some carnivores these activities were not detected with both polyalcohols. Ultrastructural observations revealed tubular structures in digestive gland cells of some species having mannitol oxidase activity, but they were not observed in others. Based on our results, we suggest that mannitol oxidase first occurred in a herbivorous or omnivorous ancestor of Apogastropoda, the clade formed by caenogastropods and heterobranchs, being subsequently lost in those species that shifted towards a carnivorous diet.
... Traditionally, researchers adopt gut content and morphometric analyses to study of the feeding modes and growth of marine organisms, including gastropods (Ismail et al. 2000;Malaquias et al. 2004;Zamora-Silva and Malaquias 2016). Over the last decade, stable isotopes ( 13 C/ 12 C and 15 N/ 14 N) have been increasingly used as biomarkers to analyze the trophic position of marine organisms, so as to better understand how they interact within the food web of an ecosystem (Post 2002;del Rio et al. 2009;Won et al. 2013). ...
Using 13C/12C, 15N/14N and 18O/16O isotopes, the trophic relationship and growth estimation were analyzed in gastropods Nassarius siquijorensis, Murex trapa and Turritella bacillum and their potential food sources and predators in summer and winter from estuarine and oceanic environments in subtropical Hong Kong. Results of δ13C and δ15N values and isotopic mixing model revealed N. siquijorensis and M. trapa were one trophic level higher than T. bacillum, in which its main food source was particulate organic matter (POM) whereas N. siquijorensis largely consumed POM and polychaetes and M. trapa also preyed on other gastropods. Crabs were the major predator of gastropods. Organisms collected from oceanic waters were more 13C enriched than from estuarine waters, reflecting different carbon food sources from marine or terrestrial origin. The δ18O profile from shell carbonate suggested these gastropods were one to two years old. T. bacillum exhibited faster summer growth than the other two species.
