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![Global distribution of hydrothermal vent shrimp belonging to the genus Rimicaris . The occurrence of these shrimp at two ridge systems: (A) Mid-Atlantic Ridge (colonized by Rimicaris exoculata [black] & Rimicaris cf. exoculata [black-white]) and (B) Central Indian Ridge [colonized by Rimicaris kairei (white)] is indicated in the enlarged maps (for details, see Table 1).](profile/Nadine-Le-Bris/publication/232688170/figure/fig1/AS:300350427942917@1448620530578/Global-distribution-of-hydrothermal-vent-shrimp-belonging-to-the-genus-Rimicaris-The.png)
Global distribution of hydrothermal vent shrimp belonging to the genus Rimicaris . The occurrence of these shrimp at two ridge systems: (A) Mid-Atlantic Ridge (colonized by Rimicaris exoculata [black] & Rimicaris cf. exoculata [black-white]) and (B) Central Indian Ridge [colonized by Rimicaris kairei (white)] is indicated in the enlarged maps (for details, see Table 1).
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The vent shrimp Rimicaris exoculata thrives around many hydrothermal vent sites along the Mid-Atlantic Ridge (MAR), where it aggregates into dense swarms. In contrast to hydrothermal vent fields at the East Pacific Rise (EPR), where the biomass is dominated by tubeworms, clams, and mussels, this shrimp is one of the major animal species at MAR vent...
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... vent shrimp Rimicaris exoculata dominates the vagile fauna at most Mid-Atlantic Ridge hydrothermal vent sites ( Fig. 1). This species lives within steep chemical and thermal gra- dients, where hot, reduced hydrothermal fluid mixes turbulently with oxygenated seawater. First described by Williams and Rona (1986), this species was observed to colonize black smoker complexes in the rift valley at the TAG site (26 ° 08.3 # N, 44 ° 49.6 # W; depth: 3,620–3,650 m). Rimicaris exoculata was subsequently found at several MAR-vent sites in the depth- range of 2,300–3,900 m (Rainbow, Broken Spur, TAG, Snake Pit, Logatchev, 5 ° S; Fig. 1, Table 1). In comparison with the hydrothermal environment on the East Pacific Rise where tubeworms, clams, and mussels dominate the vent fauna (Van Dover 1995), Rimicaris exoculata is by far one of the most abundant invertebrates at the Mid-Atlantic ridge vents (Williams & Rona 1986, Van Dover 1995, Van Dover et al. 2002, Desbruye ` res et al. 2000, Desbruye ` res et al. 2001). The two MAR-sites where this species has not been observed are the shallower vent fields Menez Gwen (860 m) and Lucky Strike (1,700 m). Although it was first believed that R. exoculata were present at the latter one (Van Dover et al. 1996), the existence of the shrimp at this site has not been reported after further expeditions (Table 1). Dense swarms of Rimicaris cf. exoculata were investigated at recently discovered hydrothermal vent fields along the southern Mid-Atlantic Ridge (Turtle Pits and Red Lion 5 ° S, 3,000m; References in Fig. 1 & Table 1). Recently, the existence of dense shrimp swarms at the active Kairei and Edmond hydrothermal vent fields (Central Indian Ridge, 2,451–3,320-m depth) (Fig. 1, Table 1) was described (Hashimoto et al. 2001a, Hashimoto et al. 2001b). Van Dover et al. (2001) reported that shrimp tissue from these sites is isotopically indistinguishable from those of R. exoculata on the Mid-Atlantic Ridge. Further studies demonstrated that the shrimp found at the Central Indian Ridge are very close to Rimicaris exoculata but still clearly distinguishable by some morphological differences and therefore classified as Rimicaris kairei (Watabe & Hashimoto 2002). The abundance of R. exoculata varies between different sites. For example, at Rainbow, shrimp assemble in depressions between chimney structures (Fig. 2B), whereas at TAG, black smoker complexes were almost entirely covered by dense agglomerations. Contrarily, at Broken Spur, low shrimp biomass was found (Copley et al. 1997). At the site Red Lion an unusual flange growth was investigated that appears to support a thriving shrimp community (Koschinsky et al. 2006). Other chimneys, that lack the flange growth, show a low abundance of Rimicaris cf. exoculata (Koschinsky et al. 2006). It is still unknown to what extent hydrothermal flow rates and composition influence the distribution of R. exoculata . However, they presumably play a role in the adaptation strategies of this species to such extreme environments. In particular, large variations in chemical composition of the endmember fluid have been observed between different MAR sites (Von Damm et al. 2001, Charlou et al. 2002, Douville et al. 2002). Rimicaris exoculata form large aggregations on solid sulfide surfaces around warm vent water emissions (Fig. 2). ...
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... vent shrimp Rimicaris exoculata dominates the vagile fauna at most Mid-Atlantic Ridge hydrothermal vent sites ( Fig. 1). This species lives within steep chemical and thermal gra- dients, where hot, reduced hydrothermal fluid mixes turbulently with oxygenated seawater. First described by Williams and Rona (1986), this species was observed to colonize black smoker complexes in the rift valley at the TAG site (26 ° 08.3 # N, 44 ° 49.6 # W; depth: 3,620–3,650 m). Rimicaris exoculata was subsequently found at several MAR-vent sites in the depth- range of 2,300–3,900 m (Rainbow, Broken Spur, TAG, Snake Pit, Logatchev, 5 ° S; Fig. 1, Table 1). In comparison with the hydrothermal environment on the East Pacific Rise where tubeworms, clams, and mussels dominate the vent fauna (Van Dover 1995), Rimicaris exoculata is by far one of the most abundant invertebrates at the Mid-Atlantic ridge vents (Williams & Rona 1986, Van Dover 1995, Van Dover et al. 2002, Desbruye ` res et al. 2000, Desbruye ` res et al. 2001). The two MAR-sites where this species has not been observed are the shallower vent fields Menez Gwen (860 m) and Lucky Strike (1,700 m). Although it was first believed that R. exoculata were present at the latter one (Van Dover et al. 1996), the existence of the shrimp at this site has not been reported after further expeditions (Table 1). Dense swarms of Rimicaris cf. exoculata were investigated at recently discovered hydrothermal vent fields along the southern Mid-Atlantic Ridge (Turtle Pits and Red Lion 5 ° S, 3,000m; References in Fig. 1 & Table 1). Recently, the existence of dense shrimp swarms at the active Kairei and Edmond hydrothermal vent fields (Central Indian Ridge, 2,451–3,320-m depth) (Fig. 1, Table 1) was described (Hashimoto et al. 2001a, Hashimoto et al. 2001b). Van Dover et al. (2001) reported that shrimp tissue from these sites is isotopically indistinguishable from those of R. exoculata on the Mid-Atlantic Ridge. Further studies demonstrated that the shrimp found at the Central Indian Ridge are very close to Rimicaris exoculata but still clearly distinguishable by some morphological differences and therefore classified as Rimicaris kairei (Watabe & Hashimoto 2002). The abundance of R. exoculata varies between different sites. For example, at Rainbow, shrimp assemble in depressions between chimney structures (Fig. 2B), whereas at TAG, black smoker complexes were almost entirely covered by dense agglomerations. Contrarily, at Broken Spur, low shrimp biomass was found (Copley et al. 1997). At the site Red Lion an unusual flange growth was investigated that appears to support a thriving shrimp community (Koschinsky et al. 2006). Other chimneys, that lack the flange growth, show a low abundance of Rimicaris cf. exoculata (Koschinsky et al. 2006). It is still unknown to what extent hydrothermal flow rates and composition influence the distribution of R. exoculata . However, they presumably play a role in the adaptation strategies of this species to such extreme environments. In particular, large variations in chemical composition of the endmember fluid have been observed between different MAR sites (Von Damm et al. 2001, Charlou et al. 2002, Douville et al. 2002). Rimicaris exoculata form large aggregations on solid sulfide surfaces around warm vent water emissions (Fig. 2). ...
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... vent shrimp Rimicaris exoculata dominates the vagile fauna at most Mid-Atlantic Ridge hydrothermal vent sites ( Fig. 1). This species lives within steep chemical and thermal gra- dients, where hot, reduced hydrothermal fluid mixes turbulently with oxygenated seawater. First described by Williams and Rona (1986), this species was observed to colonize black smoker complexes in the rift valley at the TAG site (26 ° 08.3 # N, 44 ° 49.6 # W; depth: 3,620–3,650 m). Rimicaris exoculata was subsequently found at several MAR-vent sites in the depth- range of 2,300–3,900 m (Rainbow, Broken Spur, TAG, Snake Pit, Logatchev, 5 ° S; Fig. 1, Table 1). In comparison with the hydrothermal environment on the East Pacific Rise where tubeworms, clams, and mussels dominate the vent fauna (Van Dover 1995), Rimicaris exoculata is by far one of the most abundant invertebrates at the Mid-Atlantic ridge vents (Williams & Rona 1986, Van Dover 1995, Van Dover et al. 2002, Desbruye ` res et al. 2000, Desbruye ` res et al. 2001). The two MAR-sites where this species has not been observed are the shallower vent fields Menez Gwen (860 m) and Lucky Strike (1,700 m). Although it was first believed that R. exoculata were present at the latter one (Van Dover et al. 1996), the existence of the shrimp at this site has not been reported after further expeditions (Table 1). Dense swarms of Rimicaris cf. exoculata were investigated at recently discovered hydrothermal vent fields along the southern Mid-Atlantic Ridge (Turtle Pits and Red Lion 5 ° S, 3,000m; References in Fig. 1 & Table 1). Recently, the existence of dense shrimp swarms at the active Kairei and Edmond hydrothermal vent fields (Central Indian Ridge, 2,451–3,320-m depth) (Fig. 1, Table 1) was described (Hashimoto et al. 2001a, Hashimoto et al. 2001b). Van Dover et al. (2001) reported that shrimp tissue from these sites is isotopically indistinguishable from those of R. exoculata on the Mid-Atlantic Ridge. Further studies demonstrated that the shrimp found at the Central Indian Ridge are very close to Rimicaris exoculata but still clearly distinguishable by some morphological differences and therefore classified as Rimicaris kairei (Watabe & Hashimoto 2002). The abundance of R. exoculata varies between different sites. For example, at Rainbow, shrimp assemble in depressions between chimney structures (Fig. 2B), whereas at TAG, black smoker complexes were almost entirely covered by dense agglomerations. Contrarily, at Broken Spur, low shrimp biomass was found (Copley et al. 1997). At the site Red Lion an unusual flange growth was investigated that appears to support a thriving shrimp community (Koschinsky et al. 2006). Other chimneys, that lack the flange growth, show a low abundance of Rimicaris cf. exoculata (Koschinsky et al. 2006). It is still unknown to what extent hydrothermal flow rates and composition influence the distribution of R. exoculata . However, they presumably play a role in the adaptation strategies of this species to such extreme environments. In particular, large variations in chemical composition of the endmember fluid have been observed between different MAR sites (Von Damm et al. 2001, Charlou et al. 2002, Douville et al. 2002). Rimicaris exoculata form large aggregations on solid sulfide surfaces around warm vent water emissions (Fig. 2). ...
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... vent shrimp Rimicaris exoculata dominates the vagile fauna at most Mid-Atlantic Ridge hydrothermal vent sites ( Fig. 1). This species lives within steep chemical and thermal gra- dients, where hot, reduced hydrothermal fluid mixes turbulently with oxygenated seawater. First described by Williams and Rona (1986), this species was observed to colonize black smoker complexes in the rift valley at the TAG site (26 ° 08.3 # N, 44 ° 49.6 # W; depth: 3,620–3,650 m). Rimicaris exoculata was subsequently found at several MAR-vent sites in the depth- range of 2,300–3,900 m (Rainbow, Broken Spur, TAG, Snake Pit, Logatchev, 5 ° S; Fig. 1, Table 1). In comparison with the hydrothermal environment on the East Pacific Rise where tubeworms, clams, and mussels dominate the vent fauna (Van Dover 1995), Rimicaris exoculata is by far one of the most abundant invertebrates at the Mid-Atlantic ridge vents (Williams & Rona 1986, Van Dover 1995, Van Dover et al. 2002, Desbruye ` res et al. 2000, Desbruye ` res et al. 2001). The two MAR-sites where this species has not been observed are the shallower vent fields Menez Gwen (860 m) and Lucky Strike (1,700 m). Although it was first believed that R. exoculata were present at the latter one (Van Dover et al. 1996), the existence of the shrimp at this site has not been reported after further expeditions (Table 1). Dense swarms of Rimicaris cf. exoculata were investigated at recently discovered hydrothermal vent fields along the southern Mid-Atlantic Ridge (Turtle Pits and Red Lion 5 ° S, 3,000m; References in Fig. 1 & Table 1). Recently, the existence of dense shrimp swarms at the active Kairei and Edmond hydrothermal vent fields (Central Indian Ridge, 2,451–3,320-m depth) (Fig. 1, Table 1) was described (Hashimoto et al. 2001a, Hashimoto et al. 2001b). Van Dover et al. (2001) reported that shrimp tissue from these sites is isotopically indistinguishable from those of R. exoculata on the Mid-Atlantic Ridge. Further studies demonstrated that the shrimp found at the Central Indian Ridge are very close to Rimicaris exoculata but still clearly distinguishable by some morphological differences and therefore classified as Rimicaris kairei (Watabe & Hashimoto 2002). The abundance of R. exoculata varies between different sites. For example, at Rainbow, shrimp assemble in depressions between chimney structures (Fig. 2B), whereas at TAG, black smoker complexes were almost entirely covered by dense agglomerations. Contrarily, at Broken Spur, low shrimp biomass was found (Copley et al. 1997). At the site Red Lion an unusual flange growth was investigated that appears to support a thriving shrimp community (Koschinsky et al. 2006). Other chimneys, that lack the flange growth, show a low abundance of Rimicaris cf. exoculata (Koschinsky et al. 2006). It is still unknown to what extent hydrothermal flow rates and composition influence the distribution of R. exoculata . However, they presumably play a role in the adaptation strategies of this species to such extreme environments. In particular, large variations in chemical composition of the endmember fluid have been observed between different MAR sites (Von Damm et al. 2001, Charlou et al. 2002, Douville et al. 2002). Rimicaris exoculata form large aggregations on solid sulfide surfaces around warm vent water emissions (Fig. 2). ...
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... Particularly important in explaining these small-scale patterns are the available concentrations of reduced chemical compounds (e.g. hydrogen sulfide, methane and hydrogen) that are involved in chemosynthetic pathways (Jannasch, 1985;Matabos et al., 2008;Schmidt et al., 2008;Luther et al., 2012) as well as those of metals and oxygen (Desbruyères et al., 2000;Cuvelier et al., 2011a;Martins et al., 2011;). Although vital for the hydrothermal fauna, these chemicals can also have deleterious effects, depending on their concentrations (Martins et al., 2011). ...
To date, two main vent faunal assemblages have been described on active sulfide edifices along the northern Mid-Atlantic Ridge (nMAR): one dominated by bathymodiolin mussels in low temperature areas and the other dominated by alvinocaridid shrimp in warmer habitats. In this study, we describe the ecology of new types of assemblage, dominated by gastropods, that are recurrent in several nMAR vent fields, from ~830 m to 3500 m depth. We assessed and compared the composition, abundance, diversity and trophic niche of these assemblages from three vent fields (Menez Gwen, Lucky Strike and Snake Pit) and characterized their habitats in terms of key environmental conditions. These assemblages, first seen during the Momarsat cruise in 2012 at the Lucky Strike vent field, were investigated during several subsequent cruises. They appear to be widespread along the nMAR, forming two distinct assemblages, one dominated by Lepetodrilus atlanticusat the shallowest vent field Menez Gwen, and the other by Peltospira smaragdina at the other investigated fields. Our data seem to indicate that these gastropods dominate an intermediate habitat at MAR vents and may play an important ecological role in these communities.
... Besides light and food supply, temperature has also been recognized as an important external timing cue in marine organisms (Mat, 2019) but observations from long-term observatories deployed in a few vent fields did not reveal any seasonal variations in temperature at an annual scale (Barreyre et al., 2014;Cuvelier et al., 2017). Moreover, hydrothermal vent ecosystems, compared to most of the deep sea where temperature is relatively constant within regions, exhibit heat anomalies with steep and unpredictable gradients at small spatial scales even within the same animal aggregation (Schmidt et al., 2008). In the current state of our knowledge, the synchronizing factors driving reproductive cycles in Rimicaris shrimps from the MAR and the CIR remain unclear. ...
Variations in offspring production according to feeding strategies or food supply have been recognized in many animals from various ecosystems. Despite an unusual trophic structure based on non-photosynthetic primary production, these relationships remain largely under-studied in chemosynthetic ecosystems. Here, we use Rimicaris shrimps as a study case to explore relationships between reproduction, diets, and food supply in these environments. For that, we compared reproductive outputs of three congeneric shrimps differing by their diets. They inhabit vents located under oligotrophic waters of tropical gyres with opposed latitudes, allowing us to also examine the prevalence of phylogenetic vs environmental drivers in their reproductive rhythms. For this, we used both our original data and a compilation of published observations on the presence of ovigerous females covering various seasons over the past 35 years. We report distinct egg production trends between Rimicaris species relying solely on chemosymbiosis-R. exoculata and R. kairei-and one relying on mixo-trophy, R. chacei. Besides, our data suggest a reproductive periodicity that does not correspond to seasonal variations in surface production, with substantial proportions of brooding females during the same months of the year, despite those months corresponding to either boreal winter or austral summer depending on the hemisphere. These observations contrast with the long-standing paradigm in deep-sea species for which periodic reproductive patterns have always been attributed to seasonal variations of photosynthetic production sinking from the surface. Our results suggest the presence of an intrinsic basis for biological rhythms in the deep sea, and bring to light the importance of having year-round observations in order to understand the life history of vent animals.
... Rimicaris exoculata and Rimicaris chacei (Williams and Rona, 1986) co-occur at the active vents of many MAR sites (Zbinden and Cambon Bonavita, 2020) ( Figure 1A). R. exoculata live in dense aggregations near the emitted fluids, and are therefore exposed to high temperatures and high concentrations of toxic compounds such as heavy metals or minerals (Schmidt et al., 2008a;Schmidt et al., 2008b) ( Figure 1B). Juveniles of R. exoculata also occur within these aggregations or adjacent to them (Hernańdez-Ávila et al., 2021;Methou et al., 2022). ...
The shrimp Rimicaris exoculata and Rimicaris chacei are visually dominant fauna co-occurring at deep-sea hydrothermal sites of the Mid-Atlantic Ridge (MAR). Their co-existence was related to contrasted life-history traits, including differences in their diet and reliance on chemoautotrophic symbionts at the adult stage. Both species of shrimp are colonized by diversified chemosynthetic symbiotic microbial communities in their cephalothoracic cavity. Symbiotic association with bacteria was also evidenced in their digestive system, and the major lineages were identified through sequencing (with Mycoplasmatales in the foregut and Deferribacteres in the midgut) but their precise distribution within each host species was not assessed. For the first time, we used Fluorescence in situ Hybridization (FISH) to visualize these lineages and describe their association with digestive structures of their host. The aim of the study was to identify possible differences between host species that could be related to their different life-history traits. For this purpose, we developed new specific FISH probes targeting Deferribacteres and Mycoplasmatales lineages identified in the digestive system of these shrimp. Our FISH results showed a partitioning of the bacterial lineages according to the digestive organ corroborating sequencing data, and highlighted their association with specific anatomical structures. Despite morphological differences between the foreguts of R. exoculata and R. chacei that could be related to the adult diet, our FISH results showed overall similar distribution of digestive symbionts for the two host species. However, a more comprehensive study is needed with specimens at different life or molt stages to reveal potential host specific patterns. Such comparisons are now possible thanks to our newly designed FISH probes. The tools used in our study are valuable for tracking symbiont lineages in the environment, allowing a better understanding of their relationship with their host along its life cycle, including their acquisition mechanisms.
... Higher concentrations in some metallic elements in hydrothermal fluids could force the shrimps to allocate more metabolic energy to detoxification processes, at the expense of reproductive functions. TAG fluids have higher iron, copper and manganese concentrations than those from Snake Pit (Desbruyères et al., 2000;Schmidt et al., 2008;Charlou et al., 2010), which could explain the lower reproductive output of shrimps at this vent field. However, both bioenergetics and vent processes are complex and physiological tolerance of reproductive shrimps must be experimentally tested (e.g. ...
The shrimp Rimicaris exoculata is the most conspicuous component of vent communities developing around hydrothermal fluid emissions below 2000 m on the northern Mid-Atlantic Ridge (nMAR). Its high genetic connectivity suggests a remarkable ability to produce dispersing larval stages. However, so far brooding females have been rarely observed and reproduction remained enigmatic. Spatially complex population structures related to the heterogeneity of local habitat conditions are described for many vent species, this information being fundamental to gain a better understanding of their life history. Here our aim was to assess such complexity along with reproductive development in R. exoculata populations within two vent fields, TAG and Snake Pit (3620m and 3470m depth respectively). We compared samples collected in January–February 2014 among visually distinct assemblages with different degrees of exposure to vent fluids. Dense aggregations located near active venting included mostly females and immature individuals, while inactive peripheries harbored low density assemblages of large males. Small juveniles gathering around low temperature diffusions belonged to another species, Rimicaris chacei. One third of the sexually mature females were ovigerous at the two vent fields during our sampling period, with lower fecundities and egg sizes in the TAG population. Overall, the observed shrimp distribution patterns were consistent across both vent fields, although a high degree of heterogeneity in population structure was observed locally within dense aggregations, probably reflecting micro-scale variations in environmental conditions. Our results thus highlight spatially complex population structures where R. exoculata females brood eggs within dense aggregations exposed to vent fluids, while peripheral inactive areas may be important mating grounds for adults. In addition, we suggest temporal variability in reproductive activity, increasing in the winter season, which questions potential seasonality in a deep-sea species.
... Rimicaris exoculata and Rimicaris chacei (Williams and Rona, 1986) co-occur at the active vents of many MAR sites (Zbinden and Cambon Bonavita, 2020) ( Figure 1A). R. exoculata live in dense aggregations near the emitted fluids, and are therefore exposed to high temperatures and high concentrations of toxic compounds such as heavy metals or minerals (Schmidt et al., 2008a;Schmidt et al., 2008b) ( Figure 1B). Juveniles of R. exoculata also occur within these aggregations or adjacent to them (Hernańdez-Ávila et al., 2021;Methou et al., 2022). ...
The shrimps Rimicaris exoculata and Rimicaris chacei are visually dominant fauna co-occurring at deep-sea hydrothermal sites of the Mid-Atlantic Ridge (MAR). Their co-existence was related to contrasted life-history traits, among which differences in their diet and reliance on chemoautotrophic symbionts at adult stage. Both shrimps are colonized by diversified chemosynthetic symbiotic microbial communities in their cephalothoracic cavity. Symbiotic association with bacteria was also evidenced in their digestive system, and the major lineages were identified through sequencing (Mycoplasmatales lineages mainly in the foregut and Deferribacteres lineages mainly in the midgut) but their clear distribution within each host species was not assessed. For the first time, we used Fluorescence in situ Hybridization (FISH) to visualize these lineages. Then, we described their association with digestive structures of both Rimicaris species. The aim was to identify possible differences between host species that could be related to their different life-history traits. For this purpose, we first developed specific FISH probes targeting Deferribacteres and Mycoplasmatales lineages identified in the digestive system of these shrimps. After signal specificity validation for each the new probe, we showed a partitioning of the bacterial lineages according to the digestive organ. Despite morphological differences between the foregut of R. exoculata and R. chacei that could be related to the adult diet, our FISH results showed overall similar distribution of digestive symbionts for the two host species. However, a more comprehensive study is needed with specimens at different life or molt stages to bring potentially host specific patterns out. Such comparative approach using FISH is now warranted thanks to our newly designed probes. These will be valuable tools to track symbiont lineages in the environment, allowing a better understanding of their relationship with their host along its life cycle, including acquisition mechanisms.
... Our temperature measurements indicate that thermal conditions around the different R. exoculata assemblages of TAG and Snake Pit ranged between 3.4 and 22.5°C, with maximal peaks of temperatures up to 38.1°C (Table 3). These results slightly extend the known thermal range occupied by these shrimps compared with previous in situ temperature measurements in R. exoculata aggregations, which reported average thermal conditions between 4.6 and 16°C, and up to 25°C at maximum (Desbruyères et al. 2001, Geret et al. 2002, Zbinden et al. 2004, Schmidt et al. 2008. Although R. exoculata experiences 100% of mortality when exposed for 1 h to 33°C in closed pressurized chambers, these shrimps tolerate shorter exposures of 10 min at 39°C with only 35% mortality (Ravaux et al. 2019). ...
Among the endemic and specialized fauna from hydrothermal vents, Rimicaris shrimps constitute one of the most important and emblematic components of these ecosystems. On the Mid-Atlantic Ridge, 2 species belonging to this genus co-occur: R. exoculata and R. chacei that differ in their morphology, trophic regime and abundance. R. exoculata forms large and dense aggregations on active vent chimney walls in close proximity to vent fluid emissions, whereas R. chacei is much less conspicuous, living mostly in scattered groups or solitary further away from the fluids. However, the recent revision of Rimicaris juvenile stages from the Mid-Atlantic Ridge shows that R. chacei abundance would be higher than expected at these early life stages. Here, we describe and compare the population structure of R. exoculata and R. chacei at the Snake Pit and Trans-Atlantic Geotraverse (TAG) vent fields. We show distinct population demographics between the 2 co-occurring shrimp species with a large post-settlement collapse in R. chacei populations suggesting high juvenile mortality for this species. We describe important spatial segregation patterns between the 2 species and their different life stages. Additionally, our results highlight distinct niches for the earliest juvenile stages of both R. exoculata and R. chacei , compared with all other life stages. Finally, we discuss the potential factors, including predation and competitive interactions, that could explain the differences we observed in the population structure of these 2 species.
... Invertebrate shrimp are one of the biomass-dominant groups that have been discovered in a wide range of sedimentary open ocean environments as well as at hydrothermal vent and cold seep sites (Dubilier et al., 2008;Stevens et al., 2008;Plouviez et al., 2015). Previous studies have provided information on morphological characteristics (Van Dover et al., 1988;Schmidt et al., 2008;Machon et al., 2019), gene expression patterns (Zhang et al., 2017;Hui et al., 2018;Zhu et al., 2020), and associated microbial community structure (Polz and Cavanaugh, 1995;Jiang et al., 2020;Cambon-Bonavita et al., 2021), which may help to explain the deep-sea adaptation mechanism of shrimp. ...
Invertebrate shrimp are one of the dominant benthic macrofaunae in the deep-sea environment. The microbiota of shrimp intestine can contribute to the adaptation of their host. The impact of surrounding sediment on intestinal microbiota has been observed in cultured shrimp species, but needs to be further investigated in deep-sea shrimp. The characterization of bacterial, archaeal, and fungal community structure and their interrelationships is also limited. In this study, wild-type deep-sea shrimp and the surrounding sediment were sampled. Shrimp individuals incubated in a sediment-absent environment were also used in this study. Microbial community structure of the shrimp intestine and sediment was investigated through amplicon sequencing targeting bacterial 16S rRNA genes, archaeal 16S rRNA genes, and fungal ITS genes. The results demonstrate distinct differences in community structure between shrimp intestine and the surrounding sediment and between surface and deep (5 mbsf) sediment. The composition of the intestinal microbiota in shrimp living without sediment was different from that of wild-type shrimp, indicating that the presence or absence of sediment could influence the shrimp intestinal microbiota. Carbohydrate metabolism, energy metabolism (carbon fixation, methane metabolism, nitrogen metabolism, and sulfur metabolism), amino acid metabolism, and xenobiotic biodegradation were the most commonly predicted microbial functionalities and they interacted closely with one another. Overall, this study provided comprehensive insights into bacterial, archaeal, and fungal community structure of deep-sea shrimp intestine as well as potential ecological interactions with the surrounding sediment. This study could update our understanding of the microbiota characteristics in shrimp and sediment in deep-sea ecosystems.
... In larvae of the crab Rhithropanopeus harrisii, vertical migration in the water column is triggered by temperature changes from 0.29 to 0.49 °C [66]. In the area where the hydrothermal fluid mixes with the surrounding seawater, the temperature can vary abruptly from 2 °C to over 30 °C [67]. At the periphery of the rising hydrothermal plume, and in the buoyant hydrothermal plumes spreading over 100 m, the temperature differences with seawater can be less than 0.03 °C [20,68]. ...
Deep-sea species endemic to hydrothermal vents face the critical challenge of detecting active sites in a vast environment devoid of sunlight. This certainly requires specific sensory abilities, among which olfaction could be a relevant sensory modality, since chemical compounds in hydrothermal fluids or food odors could potentially serve as orientation cues. The temperature of the vent fluid might also be used for locating vent sites. The objective of this study is to observe the following key behaviors of olfaction in hydrothermal shrimp, which could provide an insight into their olfactory capacities: (1) grooming behavior; (2) attraction to environmental cues (food odors and fluid markers). We designed experiments at both deep-sea and atmospheric pressure to assess the behavior of the vent shrimp Rimicaris exoculata and Mirocaris fortunata, as well as of the coastal species Palaemon elegans and Palaemon serratus for comparison. Here, we show that hydrothermal shrimp groom their sensory appendages similarly to other crustaceans, but this does not clean the dense bacterial biofilm that covers the olfactory structures. These shrimp have previously been shown to possess functional sensory structures, and to detect the environmental olfactory signals tested, but we do not observe significant attraction behavior here. Only temperature, as a signature of vent fluids, clearly attracts vent shrimp and thus is confirmed to be a relevant signal for orientation in their environment.
... Besides light and food supply, temperature has also been recognized as an important external time-giving cue in marine organisms [46]. Compared to most of the deep sea where temperature is relatively constant within regions, hydrothermal vents constitute heat anomalies with steep and unpredictable gradients at small spatial scales, even within a same animal aggregation [47]. Thermal variability at an annual scale could perhaps serve as a time-synchronising cue for these Rimicaris shrimps. ...
Variations in reproductive patterns according to feeding strategies or food supply have been recognized in many animals from various ecosystems. Despite an unusual trophic structure, these relationships remain largely under-studied in chemosynthetic ecosystems. Here, we use Rimicaris shrimps as a study case to explore relations between reproduction, diets and food supply in these environments. For that, we compiled data on presence of reproductive individuals from the past 35 years and compared reproductive outputs of three shrimps differing by their diets and regions. We report distinct reproductive patterns between Rimicaris species according to their trophic regime regardless of variations related to body size. Besides, we observed a reproductive period mostly between January and early April whatever the region. Intriguingly, this periodicity does not correspond to seasonal variations with presence of ovigerous females during either boreal winter or austral summer. These observations contrast with the long-standing paradigm in deep-sea species for which periodic reproductive patterns have always been attributed to seasonal variations of photosynthetic production sinking from surface. Our results suggest the presence of intrinsic basis for biological rhythms in the deep sea, and bring to light the importance of having year-round observations in order to understand life history of vent animals.
... The shrimp Rimicaris exoculata dominates the faunal communities of several hydrothermal sites along the Mid-Atlantic Ridge (MAR) [2][3][4]. This species lives in dense aggregates in quite a warm part of the hydrothermal environment, 3-25°C, with nearly neutral pH [5], and slightly lower oxygen content than deep seawater [6]. It can be retrieved from geochemically contrasting environments. ...
... Both strains seem capable of using several electron donors. The detection, for the first time, of canonical cyc2 iron oxidizing genes (Additional File 12) in both MAGs strengthens the possibility that these epibionts oxidize iron, as suggested by several authors [5,8,14,21,23,24]. It is noteworthy that cyc2 genes, and splits containing them, showed a slightly lower average coverage compared with the remaining Zetaproteobacteria genes for RB_ MAG_00008 (Additional File 13A). ...
Background
Free-living and symbiotic chemosynthetic microbial communities support primary production and higher trophic levels in deep-sea hydrothermal vents. The shrimp Rimicaris exoculata , which dominates animal communities along the Mid-Atlantic Ridge, houses a complex bacterial community in its enlarged cephalothorax. The dominant bacteria present are from the taxonomic groups Campylobacteria , Desulfobulbia (formerly Deltaproteobacteria ), Alphaproteobacteria , Gammaproteobacteria , and some recently discovered iron oxyhydroxide-coated Zetaproteobacteria . This epibiotic consortium uses iron, sulfide, methane, and hydrogen as energy sources. Here, we generated shotgun metagenomes from Rimicaris exoculata cephalothoracic epibiotic communities to reconstruct and investigate symbiotic genomes. We collected specimens from three geochemically contrasted vent fields, TAG, Rainbow, and Snake Pit, to unravel the specificity, variability, and adaptation of Rimicaris –microbe associations.
Results
Our data enabled us to reconstruct 49 metagenome-assembled genomes (MAGs) from the TAG and Rainbow vent fields, including 16 with more than 90% completion and less than 5% contamination based on single copy core genes. These MAGs belonged to the dominant Campylobacteria , Desulfobulbia , Thiotrichaceae , and some novel candidate phyla radiation (CPR) lineages. In addition, most importantly, two MAGs in our collection were affiliated to Zetaproteobacteria and had no close relatives (average nucleotide identity ANI < 77% with the closest relative Ghiorsea bivora isolated from TAG, and 88% with each other), suggesting potential novel species. Genes for Calvin-Benson Bassham (CBB) carbon fixation, iron, and sulfur oxidation, as well as nitrate reduction, occurred in both MAGs. However, genes for hydrogen oxidation and multicopper oxidases occurred in one MAG only, suggesting shared and specific potential functions for these two novel Zetaproteobacteria symbiotic lineages. Overall, we observed highly similar symbionts co-existing in a single shrimp at both the basaltic TAG and ultramafic Rainbow vent sites. Nevertheless, further examination of the seeming functional redundancy among these epibionts revealed important differences.
Conclusion
These data highlight microniche partitioning in the Rimicaris holobiont and support recent studies showing that functional diversity enables multiple symbiont strains to coexist in animals colonizing hydrothermal vents.
