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The ‘scaly-foot gastropod’, Chrysomallon squamiferum, mantle cavity overview (shell and mantle tissue removed). Scale bar: 1 cm
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The 'scaly-foot gastropod' (Chrysomallon squamiferum Chen et al., 2015) from deep-sea hydrothermal vent ecosystems of the Indian Ocean is an active mobile gastropod occurring in locally high densities, and it is distinctive for the dermal scales covering the exterior surface of its foot. These iron-sulfide coated sclerites, and its nutritional depe...
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... Longqi-1 stands out as unique in the Indian Ocean due to the presence of exceptionally large sulfide structures 5 m in width and 15 m in height that feature substantial flanges approximately 1-5 m in width ( Fig. 5a; Liang et al., 2023a). Unlike the high-temperature chimneys growing on top of the flanges in Endeavour and Cleft (Delaney et al., 1992;Robigou et al., 1993;Kelley et al., 2012), a large abundance of low-temperature beehive diffusers have developed at the top of the flanges in Longqi-1 (Fig. 5b), hosting numerous organisms such as barnacles, mussels, and snails, particularly the scaly-foot gastropod ( Fig. 5c; (Chen et al., 2015a;Chen et al., 2015b). A chimney sample collected at the top of a flange (Fig. 5d) displays a reddish-brown Fe-Si oxide surface covered with a large number of barnacles. ...
... The use of micro CT for illustration of the anatomy (especially the shell, though rarely the inner organs) of dead specimens has been demonstrated already (22)(23)(24)(25)(26)(27)(28). The animals were mostly stained with iodine to guarantee sufficient soft tissue differentiation. ...
Giant African land snails (GALS) have become increasingly popular, for example, as pets or in kindergartens in Europe, but little is known about their clinically relevant anatomy, diseases, or further details in diagnostic imaging. The present study focuses on the techniques and image interpretation of radiography, computed tomography, and sonography in GALS. The aim of the study is to find the most appropriate imaging tool to visualize the various organs within the mantle cavity (also known as visceral mass) in GALS. The detailed anatomy of GALS is presented with numerous figures of the different imaging techniques. The sensory organs and nervous system will not be part of the present study.
... large-scale surveys of the seafloor with the few existing data collected through ISA mineral exploration contracts (Perez et al., 2021) (Figure 2A). Due to intense human activities in the area, newly discovered species in the Longqi field, like the scaly-foot snail Chrysomallon squamiferum (Chen et al., 2015), has already been listed as endangered under criteria B2ab(iii) of the IUCN Red List in 2018 (Sigwart et al., 2019). Against the growing economic interest in bottom fishing and in pursuance of the recalled UNGA resolution on the protection of VMEs in this wide ABNJ, few initiatives for its protection have been adopted only within the framework of the CBD and of some competent RFMOs. ...
Marine areas beyond national jurisdiction (ABNJ) are under the growing threat of cumulative anthropogenic impacts including fishing, shipping, energy extraction, certain forms of marine scientific research, and the imminent deep seabed mining that prefigure a critical scenario in terms of biodiversity loss and environmental degradation. This article offers a contribution to the discussion on the best approaches to effectively implement environmental protection and conservation in ABNJ, also in the light of ongoing intergovernmental negotiations on the conclusion of an agreement implementing the United Nations Convention on the Law of the Sea on the conservation and sustainable use of biological diversity in ABNJ. The paper first analyzes the current legal gaps in the protection and conservation of ABNJ and the tools developed by some regional and universal regimes to preserve vulnerable marine ecosystems. It then presents two case studies, relating to hydrothermal vent fields of the Mid Atlantic Ridge (Lost City) and the South-West Indian Ridge (Longqi field) to discuss the fragmentation of the legal regimes applicable to ABNJ as well as the difficult cooperation among the regional, global and sectoral frameworks involved in their governance. The case studies show that a coordination mechanism, based on mutual recognition of the protection and conservation measures taken by each competent organization in a specific field, is of utmost urgency. Only a more structured system of cooperation among States and international organizations, that the new implementation agreement will hopefully develop, will allow for the identification of the most appropriate tools for the protection of a given marine area from the cumulative impacts of human activities.
... One adult individual each of Provanna clathrata, Rubyspira osteovora, and Ifremeria nautilei were subjected to μ-CT at the SPring-8 synchrotron facility in Hyogo, Japan, following the methods of Sasaki et al. (2018), where the soft parts were stained with 1% iodine solution (see Appendix S1 for expanded methods). We hypothesized that the digestive system and key respiratory organs linked to symbiosis (ventricle, auricle, and gill) were likely to exhibit diet-linked adaptations (Chen et al., 2015) and targeted them for three-dimensional (3D) reconstruction. We processed the scans in Amira version 2021, where the target organs and the overall soft body parts were reconstructed and their relative volumes calculated. ...
... We found the hearts of Rubyspira and Ifremeria (1.63% and 1.43%, respectively) to be over a magnitude larger relative to body volume compared to Provanna (0.09%), but the ventricle was only obviously enlarged in Ifremeria (Figure 2b). The Ifremeria heart is still smaller than that of the peltospirid snail Chrysomallon, whose heart occupies over 4% of the body volume (Chen et al., 2015). Chrysomallon hosts endosymbionts in an internalized esophageal gland while Ifremeria hosts symbionts on its gill, and the symbionts therefore obtain oxygen both directly from the vent fluid (Childress & Girguis, 2011) and from the host, reducing the need for a heart as large as Chrysomallon. ...
Specializing in different dietary niches via morphological adaptation underpins the success of animal radiation when invading a new environment, as seen in examples such as Darwin's finches (De León et al., 2014). Ecomorphological studies of various animal groups, from mammals to arthropods, illustrate adaptations to different food sources, which are often coupled with shifts in internal anatomy, particularly the digestive system (Duque-Correa et al., 2021; Griffen & Mosblack, 2011). A widely accepted pattern in terrestrial systems is that herbivorous mammals require longer and more voluminous gastrointestinal tracts in order to digest plant matter, whereas carnivorous mammals have smaller intestines since meat is much more digestible (Duque-Correa et al., 2021). Such research has mostly focused on animals in land-based ecosystems powered by photosynthesis, but these ecosystems only account for a fraction of the broad diversity of ecosystems on Earth. “Extreme” deep-sea ecosystems, such as hydrothermal vents, hydrocarbon seeps, and organic falls, are powered by microbial chemosynthesis (Childress & Girguis, 2011) and host numerous endemic fauna with special adaptations (Sogin et al., 2020), offering an opportunity to explore how the anatomy of animals evolved to specialize in unusual diets. Our results demonstrated that adapting to each peculiar deep-sea food source is linked to specific anatomical shifts, expanding the applicability of ecomorphology to a range of unusual diets. The deep sea remains little known and unexplored, despite its many habitats, including hydrothermal vents, which are being targeted for deep-sea mining, threatening endemic species (Thomas et al., 2022). Understanding the trophic dynamics in these systems and the role each species plays is crucial to successful conservation, yet numerous species have never been observed in their natural habitat. The accurate reconstruction of organ volumetrics using noninvasive methods, such as μ-CT scans, can be a useful tool in predicting the diet of deep-sea animals even when only preserved specimens are available, similarly to how ecomorphology has been used to reconstruct habitat preferences in fossil mammals (DeGusta & Vrba, 2005). This would clearly require the future accumulation of 3D anatomical data from a wide range of deep-sea species with various unique diets, which will undoubtedly reveal many anatomical surprises.
... The scaly-foot snail Chrysomallon squamiferum is a peltospirid vent snail distributed in the Indian Ocean and houses a sulphuroxidising gammaproteobacteria as the endosymbiont [15]. Vent molluscs normally house symbionts in the gill that is in direct contact with vent fluid, but the scaly-foot snail hosts the endosymbiont in a hypertrophied oesophageal gland deep inside its body and has a much enlarged circulatory system which delivers sulphide and carbon dioxide to the endosymbiont [16]. Previous analyses of its hologenome showed that the symbiont can utilise sulphuric substances from the vent fluid and synthesise nutrients for the host [15,17]. ...
... However, Alviniconcha snails host symbionts in the gill, which is in direct contact with the ambient environment; therefore, the host cannot regulate a stable intracellular environment. By hosting the endosymbiont in an organ deep inside the body, scaly-foot snails can regulate and likely maintain a steady concentration of key chemicals, such as hydrogen sulphide and oxygen [16]. In addition, they require a high specificity of endosymbionts at the species level to constrain its function in this specific intracellular habitat, whereas Alviniconcha retains flexibility in species-level associations [77]. ...
... Our results are congruent with a previous physiology experiment where scalyfoot snails can maintain a steady metabolic demand in two different experimental temperatures where Alviniconcha failed to do so [78]. Hence, scaly-foot snails can buffer shifts in the environmental conditions for the endosymbionts, a trait likely supported by their hypertrophied circulation system [16]. Overall, these results suggest that the scaly-foot snail hosts actively buffer the environmental differences and changes by moderating their gene expression to provide a stable intracellular environment in the oesophageal gland to the symbionts. ...
The scaly-foot snail (Chrysomallon squamiferum) inhabiting deep-sea hydrothermal vents in the Indian Ocean relies on its sulphur-oxidising gammaproteobacterial endosymbionts for nutrition and energy. In this study, we investigate the specificity, transmission mode, and stability of multiple scaly-foot snail populations dwelling in five vent fields with considerably disparate geological, physical and chemical environmental conditions. Results of population genomics analyses reveal an incongruent phylogeny between the endosymbiont and mitochondrial genomes of the scaly-foot snails in the five vent fields sampled, indicating that the hosts obtain endosymbionts via horizontal transmission in each generation. However, the genetic homogeneity of many symbiont populations implies that vertical transmission cannot be ruled out either. Fluorescence in situ hybridisation of ovarian tissue yields symbiont signals around the oocytes, suggesting that vertical transmission co-occurs with horizontal transmission. Results of in situ environmental measurements and gene expression analyses from in situ fixed samples show that the snail host buffers the differences in environmental conditions to provide the endosymbionts with a stable intracellular micro-environment, where the symbionts serve key metabolic functions and benefit from the host’s cushion. The mixed transmission mode, symbiont specificity at the species level, and stable intracellular environment provided by the host support the evolutionary, ecological, and physiological success of scaly-foot snail holobionts in different vents with unique environmental parameters.
... The diversity of vent specific communities has been described by many researchers (Haymon et al., 1993;Hashimoto et al., 2001;Van Dover et al., 2001;Nakamura et al., 2012;Beedessee et al., 2013;Chen et al., 2015;Copley et al., 2016;Watanabe et al., 2018;Zhou et al., 2018;Jang et al., 2020;Sun et al., 2020). However, most of the known hydrothermal vents sites are located in the Pacific and Atlantic Oceans, and very few active vent fields have been discovered in the Indian Ocean Hashimoto et al., 2001;Van Dover et al., 2001;Tao et al., 2011Tao et al., , 2012Tao et al., , 2014Nakamura et al., 2012Nakamura et al., , 2013Copley et al., 2016;Ji et al., 2017). ...
... Even though hydrothermal vents along the CIR and SWIR are located within a limited area, they are considered to be reasonably diverse in terms of biological communities associated with them (Nakamura and Takai, 2015b). The diversity of vent-specific communities has been described by many researchers (Haymon et al., 1993;Hashimoto et al., 2001;Van Dover et al., 2001;Nakamura et al., 2012;Beedessee et al., 2013;Chen et al., 2015;Copley et al., 2016;Watanabe et al., 2018;Zhou et al., 2018;Jang et al., 2020;Sun et al., 2020). Based on published reports ~100 macrobenthic and megabenthic species/genera occur at the eight known active hydrothermal vent sites in the Indian Ocean (Table 14.2). ...
... Although hydrothermal vent fauna of the Indian Ocean represents some of very unusual endemic species such as the Scaly-foot gastropod C. squamiferum, the biodiversity of this region is poorly understood compared with the well-studied Pacific and Atlantic vent systems (Sun et al., 2020). Nevertheless, analogous to the fauna of the other vents, a number of the species are believed to be endemic and are known to occur within the area of individual vents (Chen et al., 2015). In contrast, the vent crab A. rodriguezensis, vent shrimps Rimicaris kairei, and M. indica, the deep-sea mussel B. marisindicus and the Scaly-foot gastropods (C. ...
The Indian mid‐oceanic ridge system is under explored for hydrothermal vent fields. Most vent fields are discovered along the slow to intermediate spreading Central Indian and ultra‐slow spreading Southwest Indian ridges (CIR and SWIR). Detailed geological studies of Dodo, Solitaire, Edmond, Kairei, and Longqi vent fields and their fluids characteristics show that they are basalt‐hosted systems. However, high hydrogen and methane concentrations in Kairei and Longqi fluids indicate fluid circulation through mafic–ultramafic lithologies. Abundant populations of (hyper)thermophilic hydrogenotrophic chemolithoautotrophs are associated with Dodo, Solitaire, and Kairei fluids. The Fe/Mn‐oxidizing chemolithoautotrophs belonging to Zetaproteobacteria or various metal‐tolerant genera within class Alphaproteobacteria and Gammaproteobacteria thrive on metal‐rich Edmond and Longqui vent fluids. Therefore, the chemical composition of fluid and associated biosphere depend mainly on subsurface water–rock reactions and are independent of the spreading rate of the ridge. A very unusual animal community such as (i) vent crab Austinograea rodriguezensis , (ii) vent shrimps ( Rimicaris kairei , and Mirocaris indica ), (iii) deep‐sea mussel ( Bathymodiolus marisindicus ), (iv) scaly‐foot gastropods ( Chrysomallon squamiferum , Alviniconcha sp.), and (v) barnacle ( Neolepas sp.) are found at Indian Ocean vent fields. Most of the vent‐specific fauna representing vent sites at the Central and Southwest Indian Ridges are found at Kairei field (> 24% of the total), making it biologically diverse and supporting the hypothesis that the Rodriguez Triple Junction (RTJ) could be an essential connecting point for dispersal of larvae to the nearby vent fields. Further, the Southwest–Southeast Indian Ridges could act as a corridor for dispersal of vent fauna between Atlantic, Indian and Pacific Oceans. Interestingly, similar chemosynthetic vent fauna (associated with Galatheidae, Neolepadidae, and Mitilidae families) have also been found at cold‐seep methane hydrate systems in Indian continental margins. Detailed genomic studies of cold‐seep community and its comparison with vent community and water column hydrothermal tracer‐based studies are required to establish the ecosystem connectivity.
... Active hydrothermal vents exhibit high biomass of a few dominant species, species rarity (many species comprise < 5% of total abundance in samples), and high endemism, with about 70% of megaand macrofaunal species endemic to vents and/or symbiotrophic [113,124,143]. Detailed ecological information (i.e., on trophic relationships and life histories) has been collected for a few charismatic species, including the identification of foundation species that play a crucial role in structuring and maintaining communities and novel symbiotic relationships [113,130,[144][145][146][147][148][149][150][151][152][153][154][155][156]. However, most species inhabiting active vents, especially those of small size classes, remain poorly understood ( Fig. 1). ...
A comprehensive understanding of the deep-sea environment and mining’s likely impacts is necessary to assess whether and under what conditions deep-seabed mining operations comply with the International Seabed Authority’s obligations to prevent ‘serious harm’ and ensure the ‘effective protection of the marine environment from harmful effects’ in accordance with the United Nations Convention on the Law of the Sea. A synthesis of the peer-reviewed literature and consultations with deep-seabed mining stakeholders revealed that, despite an increase in deep-sea research, there are few categories of publicly available scientific knowledge comprehensive enough to enable evidence-based decision-making regarding environmental management, including whether to proceed with mining in regions where exploration contracts have been granted by the International Seabed Authority. Further information on deep-sea environmental baselines and mining impacts is critical for this emerging industry. Closing the scientific gaps related to deep-seabed mining is a monumental task that is essential to fulfilling the overarching obligation to prevent serious harm and ensure effective protection, and will require clear direction, substantial resources, and robust coordination and collaboration. Based on the information gathered, we propose a potential high-level road map of activities that could stimulate a much-needed discussion on the steps that should be taken to close key scientific gaps before any exploitation is considered. These steps include the definition of environmental goals and objectives, the establishment of an international research agenda to generate new deep-sea environmental, biological, and ecological information, and the synthesis of data that already exist.
... A third SFSs morphotype, with brown shells and dark scales, was observed at Longqi, a hydrothermal vent field located on the ultraslow-spreading Southwest Indian Ridge (SWIR; Zhou et al., 2018). Despite the color discrepancy, genetic and morphological results reveal that all three morphotypes are genetically the same species (Chen et al., 2015b). ...
The microbial communities of the hydrothermal Scaly-foot Snails (SFSs) from independent hydrothermal vent fields have not been investigated in depth. In this study, we collected SFSs from two different hydrothermal environments located on the Central Indian Ridge (CIR) and the Southwest Indian Ridge (SWIR), the Kairei and Longqi vent fields, respectively. Additionally, one SFS collected from the Kairei vent field was reared for 16 days with in situ deep-sea seawater. The epibiotic and internal samples of SFSs, including ctenidium, esophageal gland, visceral mass, shells, and scales, were examined for microbial community compositions based on the 16S rRNA gene. Our results revealed significant differences in microbial community composition between SFSs samples collected from Kairei and Longqi vent fields. Moreover, the microbial communities of epibiotic and internal SFS samples also exhibited significant differences. Epibiotic SFS samples were dominated by the bacterial lineages of Sulfurovaceae, Desulfobulbaceae, Flavobacteriaceae, and Campylobacteraceae. While in the internal SFS samples, the genus Candidatus Thiobios, affiliated with the Chromatiaceae, was the most dominant bacterial lineage. Furthermore, the core microbial communities of all samples, which accounted for 78 ∼ 92% of sequences, were dominated by Chromatiaceae (27 ∼ 49%), Sulfurovaceae (10 ∼ 35%), Desulfobulbaceae (2 ∼ 7%), and Flavobacteriaceae (3 ∼ 7%) at the family level. Based on the results of random forest analysis, we also found the genera Desulfobulbus and Sulfurovum were the primary bacterial lineages responsible for the dissimilarity of microbial communities between the SFS samples collected from the Kairei and Longqi vent fields. Our results indicated that the microbial lineages involved in the sulfur cycle were the key microorganisms, playing a crucial role in the hydrothermal vent ecosystems. Our findings expand current knowledge on microbial diversity and composition in the epibiotic and internal microbial communities of SFS collected from different hydrothermal vent fields.
... The endosymbionts housed in internal organs without direct contact with the vent fluid are likely to be reliant on the host for transporting substances such as oxygen, sulfide, and methane; although diffusion may also play a role in their delivery to the symbionts. The anatomical organisation of the endosymbionts in these two peltospirid snails are more similar to tubeworms than other known molluscan symbioses in vents 14,18 and indeed, the endosymbionts housed in the internal trophosome of the giant tubeworm R. pachyptila rely on the host's haemoglobins to transport oxygen and sulfide 19 . ...
Animals endemic to deep-sea hydrothermal vents often form obligatory symbioses with bacteria, maintained by intricate host–symbiont interactions. Most genomic studies on holobionts have not investigated both sides to similar depths. Here, we report dual symbiosis in the peltospirid snail Gigantopelta aegis with two gammaproteobacterial endosymbionts: a sulfur oxidiser and a methane oxidiser. We assemble high-quality genomes for all three parties, including a chromosome-level host genome. Hologenomic analyses reveal mutualism with nutritional complementarity and metabolic co-dependency, highly versatile in transporting and using chemical energy. Gigantopelta aegis likely remodels its immune system to facilitate dual symbiosis. Comparisons with Chrysomallon squamiferum, a confamilial snail with a single sulfur-oxidising gammaproteobacterial endosymbiont, show that their sulfur-oxidising endosymbionts are phylogenetically distant. This is consistent with previous findings that they evolved endosymbiosis convergently. Notably, the two sulfur-oxidisers share the same capabilities in biosynthesising nutrients lacking in the host genomes, potentially a key criterion in symbiont selection.
... Vent gastropods host their endosymbionts in an enlarged internal organ while vent mussels house their symbiotic bacteria in the gills (Chen et al., 2017;Duperron et al., 2016). Trace metal uptake pathways may well vary with the different physiological and morphological adaptations of vent gastropods and mussels (Chen et al., 2015;Goffredi et al., 2004;Won et al., 2003), with resulting differences in the biogeochemical cycling of trace metals in the different hydrothermal vent species. Although several attempts have been made to understand trace metal biogeochemical cycling in vent organisms by culturing them under laboratory conditions (Kádár et al., 2005a;Page et al., 1991), these results may not be informative for they cannot represent the in situ status of the natural hydrothermal vent environment. ...
... In the scaly-foot snail, higher Zn concentrations were measured in the VM while in the peltospirid snail, raised Zn concentrations were seen in the gill. Chen et al. (2015) reported a great ability of the ctenidium (i.e., gill) in scaly-foot snail to exchange gases between host and environment to sustain an abundant supply of sulfide to the bacteria hosted in an internal tissue (Chen et al., 2017). This may lead to the larger amount of Zn accumulated in the snail gill than in other tissues. ...
... It is worthy of mention that nutrient acquisition to symbiotrophy has been found in the vent gastropods in adult stage even though snail G. aegis may be mixotroph in its juvenile life (Chen et al., 2017). The endosymbionts are harboured in an internal organ in these gastropods (Chen et al., 2015(Chen et al., , 2017. Rather than obtaining nutrients directly from the environment, a continuous supply of nutrients is required for the chemosynthesis of their symbionts, which can only be transported through the blood circulation system of the host to the organ harbouring the symbionts (Chen et al., 2017). ...
Hydrothermal vent represents an extreme environment where metal-enriched fluids are in contact with chemosymbiotic animals. In the present study, Zn isotopic compositions were determined in multiple tissues of three dominant hydrothermal vent mollusks (the mussel Bathymodiolus marisindicus and two gastropods Chrysomallon squamiferum and Gigantopelta aegis) collected from a hydrothermal vent field (Southwest Indian Ridge in the Indian Ocean). We found approximately 1.78‰ differences in the δ⁶⁶Zn values among the three vent mollusks despite of their similar range of Zn concentrations. The significant variation in the δ⁶⁶Zn values was considered to be indicative of different Zn uptake sources among the three species as a result of their morphological adaptations. Zinc uptake associated with symbiotic activities may be more relevant in the vent gastropods, whereas Zn uptake from hydrothermal fluids during filter-feeding may also play a role in the vent mussels. However, no significant difference in δ⁶⁶Zn values was observed among tissues of any of the mollusks, showing the absence of Zn isotope fractionation during internal Zn transport. Our results demonstrated that variable Zn uptake pathways existed among different hydrothermal vent mollusks and could be differentiated by determining the Zn isotopic compositions in their tissues. We also highlight that Zn isotope ratios can be used to track Zn sources to the vent mollusks.
