Sea Slug Species Research Articles

Chromosome-level genome assembly of the sacoglossan sea slug Elysia timida (Risso, 1818)

BackgroundSequencing and annotating genomes of non-model organisms helps to understand genome architecture, the genetic processes underlying species traits, and how these genes have evolved in closely-related taxa, among many other biological processes. However, many metazoan groups, such as the extremely diverse molluscs, are still underrepresented in the number of sequenced and annotated genomes. Although sequencing techniques have recently improved in quality and quantity, molluscs are still neglected due to difficulties in applying standardized protocols for obtaining genomic data.ResultsIn this study, we present the chromosome-level genome assembly and annotation of the sacoglossan sea slug species Elysia timida, known for its ability to store the chloroplasts of its food algae. In particular, by optimizing the long-read and chromosome conformation capture library preparations, the genome assembly was performed using PacBio HiFi and Arima HiC data. The scaffold and contig N50s, at 41.8 Mb and 1.92 Mb, respectively, are approximately 30-fold and fourfold higher compared to other published sacoglossan genome assemblies. Structural annotation resulted in 19,904 protein-coding genes, which are more contiguous and complete compared to publicly available annotations of Sacoglossa with respect to metazoan BUSCOs. We found no evidence for horizontal gene transfer (HGT), i.e. no photosynthetic genes encoded in the sacoglossan nucleus genome. However, we detected genes encoding polyketide synthases in E. timida, indicating that polypropionates are produced. HPLC–MS/MS analysis confirmed the presence of a large number of polypropionates, including known and yet uncharacterised compounds.ConclusionsWe can show that our methodological approach helps to obtain a high-quality genome assembly even for a "difficult-to-sequence" organism, which may facilitate genome sequencing in molluscs. This will enable a better understanding of complex biological processes in molluscs, such as functional kleptoplasty in Sacoglossa, by significantly improving the quality of genome assemblies and annotations.

The Complete Genome Sequences of 7 Species of Nudibranchs (Nudibranchia, Gastropoda).

We present genome sequences of 7 species of sea slugs from 4 genera. Illumina sequencing was performed on tissue from wild-collected museum specimens. The reads were assembled using a de novo method followed by a finishing step. The raw and assembled data are publicly available via Genbank.

Food shaped photosynthesis: Photophysiology of the sea slug Elysia viridis fed with two alternative chloroplast donors.

Some Sacoglossa sea slugs steal and integrate chloroplasts derived from the algae they feed on into their cells where they continue to function photosynthetically, a process termed kleptoplasty. The stolen chloroplasts - kleptoplasts - can maintain their functionality up to several months and support animal metabolism. However, chloroplast longevity can vary depending on sea slug species and algal donor. In this study, we focused on Elysia viridis, a polyphagous species that is mostly found associated with the macroalga Codium tomentosum, but that was reported to eat other macroalgae, including Chaetomorpha sp. We have investigated the changes in E. viridis physiology when provided with the two different food sources to evaluate to which extent the photosynthetic and photoprotective mechanisms of the algae chloroplasts matched those of the plastids once in the animal cells. To perform the study, we rely on the evaluation of chlorophyll a variable fluorescence to study the photophysiological state of the integrated kleptoplasts and high-performance liquid chromatography (HPLC) to study variations in the photosynthetic pigments. We observed that the photosynthetic efficiency of E. viridis is lower when fed with Chaetomorpha. Also, significant differences were observed in the non-photochemical quenching (NPQ) abilities of the sea slugs. While sea slugs fed with C. tomentosum react similarly to high-light stress as the alga, E. viridis hosting Chaetomorpha chloroplasts were unable to properly recover from photoinhibition or perform a functional xanthophyll cycle (XC). Our results showed that, even if the sea slugs fed with the two algae show photosynthetic activities like the respective algal donors, not all the photoprotective mechanisms present in Chaetomorpha can be maintained in E. viridis. This indicates that the functionality of the kleptoplasts does not depend solely on their origin but also on the degree of compatibility with the animal species integrating them.

A new species of head-shield sea slug, Melanochlamys droupadi (Heterobranchia: Aglajidae) from the north-western Bay of Bengal, India

ABSTRACT A new species of the head-shield sea slug is described herein from an examination of the morphological and anatomical characters. A molecular analysis supported the novel status of the species. This species is named Melanochlamys droupadi n. sp. in the honour of the Hon'ble president of India, Shrimati (Mrs) Droupadi Murmu. It is the second species from the Indian region and the third true tropical species. All the specimens were collected from the Digha coast of West Bengal and the Udaipur coast of Odisha state, along the north-western Bay of Bengal. ZooBank registration number with the article number as: http://www.zoobank.org/urn:lsid:zoobank.org:pub:CB84F7F1-5EA7-4631-AFA0-0E057D8380FE

The Complete Genome Sequences of seven species of sea slugs (Nudibranchia, Gastropoda, Mollusca).

We present the complete genome sequences of seven species of sea slugs. Illumina sequencing was performed on tissue from wild-collected museum specimens. The reads were assembled using a de novo method followed by a finishing step. The raw and assembled data are publicly available via Genbank.

Seasonal abundance of the nudibranch Dondice jupiteriensis on the colonial hydroid Eudendrium carneum

Benthic colonial hydroids often serve as a host to a large variety of invertebrate taxa. The colonial hydroid Eudendrium carneum Clarke, 1882 is host to a variety of epifauna, including the recently described nudibranch Dondice jupiteriensis García—Méndez & Valdés, 2022. Like many species of heterobranch sea slugs, little is known about the natural history and population biology of D. jupiteriensis. Here we describe a year—long study recording the population density and size structure of D. jupiteriensis on E. carneum colonies in Tampa Bay, FL USA. We found that the D. jupiteriensis population persists year—round but is the densest during the summer months. This coincides with the time period when individual slugs were the smallest, suggesting the population increase in the summer is likely due to larval recruitment. Additionally, 13 other species of heterobranch sea slugs were found inhabiting E. carneum over the course of the study, although none of them were as numerous as D. jupiteriensis. This study provides the first available information on the ecology and population biology of the recently described nudibranch D. jupiteriensis.

A reference genome for the long-term kleptoplast-retaining sea slug Elysia crispata morphotype clarki.

Several species of sacoglossan sea slugs possess the incredible ability to sequester chloroplasts from the algae they consume. These "photosynthetic animals" incorporate stolen chloroplasts, called kleptoplasts, into the epithelial cells of tubules that extend from their digestive tracts throughout their bodies. The mechanism by which these slugs maintain functioning kleptoplasts in the absence of an algal nuclear genome is unknown. Here, we report a draft genome of the sacoglossan slug Elysia crispata morphotype clarki, a morphotype native to the Florida Keys that can retain photosynthetically active kleptoplasts for several months without feeding. We used a combination of Oxford Nanopore Technologies long reads and Illumina short reads to produce a 786-Mb assembly (N50 = 0.459 Mb) containing 68,514 predicted protein-coding genes. A phylogenetic analysis found no evidence of horizontal acquisition of genes from algae. We performed gene family and gene expression analyses to identify E. crispata genes unique to kleptoplast-containing slugs that were more highly expressed in fed versus unfed developmental life stages. Consistent with analyses in other kleptoplastic slugs, our investigation suggests that genes encoding lectin carbohydrate-binding proteins and those involved in regulation of reactive oxygen species and immunity may play a role in kleptoplast retention. Lastly, we identified four polyketide synthase genes that could potentially encode proteins producing UV- and oxidation-blocking compounds in slug cell membranes. The genome of E. crispata is a quality resource that provides potential targets for functional analyses and enables further investigation into the evolution and mechanisms of kleptoplasty in animals.

Food shaped photosynthesis: Photophysiology of the sea slug Elysia viridis fed with two alternative chloroplast donors

Background: Some Sacoglossa sea slugs integrate intracellular chloroplasts derived from the algae they feed on, a process termed kleptoplasty. The stolen chloroplasts – kleptoplasts – can maintain their functionality up to several months and support animal metabolism. However, chloroplast longevity can vary depending on sea slug species and algal donor. In this study, we focus our attention on Elysia viridis, a polyphagous species that is mostly found associated to the macroalga Codium tomentosum, but that was reported to eat other macroalgae, including Chaetomorpha sp. Methods: We have investigated the changes in E. viridis physiology when provided with the two different food sources to evaluate to which extent the photosynthetic and photoprotective mechanisms of the algae chloroplasts matched those of the plastids once in the animal cells. To perform the study, we rely on the evaluation of chlorophyll a variable fluorescence to study the photophysiologic state of the integrated kleptoplasts and the high-performance liquid chromatography (HPLC) to study variations in the photosynthetic pigments. Results: We observed that the photosynthetic efficiency of E. viridis specimens is similar to the one of the respective algal donor but specimens fed with Chaetomorpha tend to have lower performances. Significant differences appear in the non-photochemical quenching (NPQ) abilities. While sea slugs fed with C. tomentosum react to high-light stress as the algae, E. viridis hosting Chaetomorpha chloroplasts are unable to properly recover from photoinhibition or perform a functional xanthophyll cycle (XC). Conclusions: Our results showed that, even if the sea slugs fed with the two algae show photosynthetic activities like the respective algal donors, not all the photoprotective mechanisms present in Chaetomorpha can be maintained in E. viridis. This indicates that the functionality of the kleptoplasts does not depend solely on their origin but also on the degree of compatibility with the animal species integrating them.

Six species of sea slugs (Gastropoda: Heterobranchia) new for the marine fauna of Bosnia and Herzegovina

Abstract In this paper six heterobranch mollusc species are reported for the first time for Bosnia and Herzegovina: Berthellina edwardsi (Vayssiere, 1896), Felimida luteorosea (Rapp, 1827), Thuridilla hopei (Verany, 1853), Dendrodoris grandiflora (Rapp, 1827), Camachoaglaja africana (Pruvot-Fol, 1953) and Felimare villafranca (Risso, 1818). The study was conducted in October 2021 on Klek Peninsula and in Neum Bay (eastern Adriatic Sea, Bosnia and Herzegovina). This paper significantly extends the knowledge of the national marine heterobranch molluscs fauna, almost doubling the number of species known for the country, as only seven heterobranch species were reported for Bosnia and Herzegovina until now.

OPISTHOBRANCH (MOLLUSCA: GASTROPODA) FAUNA OF ROCKY REEF ECOSYSTEMS OF KERALA COAST, INDIA

Opisthobranchs are the one of the least studied marine taxonomic group in Kerala. The present study was carried out to explore the opisthobranch diversity of rocky reefs of Kerala. And the study able to record the 13 species of sea slugs belongs to 3 Order 8 Families and 10 Genera. Out of 13 species recorded in the study, 8 species identified as new to Kerala coast. Among the 3 Orders recorded in the study Nudibranchia was noted with highest species contribution of 10 species and among the 8 families, the Dentrodoridae with maximum of 3 species.

Photographic Checklist, DNA Barcoding, and New Species of Sea Slugs and Snails from the Faafu Atoll, Maldives (Gastropoda: Heterobranchia and Vetigastropoda)

Baseline biodiversity data are key for ecological and evolutionary studies and are especially relevant for areas such as the Maldivian Archipelago in the Indian Ocean, which can act as a stepping-stone for the transport of widely distributed marine species. We surveyed the islands and reefs of the Faafu and Malé Atolls with snorkeling and scuba diving, collecting the two gastropod subclasses, Heterobranchia and Vetigastropoda. Our inventory comprises 104 species photographed alive to create an identification guide. We also provide COI barcodes for most species, adding novel sequence data for the Maldivian malacofauna. Half of our species represent new records for the Maldives, emphasizing how much diversity remains to be discovered. Species distributions reflect ecological rarity, with almost 60% of taxa only found in one site. We also compiled a comprehensive checklist of heterobranchs and vetigastropods of the Maldives based on literature records, resulting in 320 species, which, together with barcoding data, indicate several potential cryptic species in the Indo-Pacific. Six new species are described, the nudibranchs Limenandra evanescenti n. sp., Eubranchus putnami n. sp., Sakuraeolis marhe n. sp., Moridilla maldivensis n. sp., Tergiposacca perspicua n. sp., and the sacoglossan Costasiella fridae n. sp.

Sea bunnies as a potential marine ecotourism in sumberkima, Buleleng Regency, Bali

The Sumberkima Village has a vital coral reef ecosystem since the ecosystem has become home to some incredible marine biotas, including sea bunnies, a sea slug or Nudibranch species. The Nudibranch community can indicate the health of the ecosystem from its diversity and structure. This study aims to determine the distribution and value of the Nudibranchia Ecological Index and provide an example informative infographic of sea bunnies to support marine ecotourism at Sumberkima Village, Gerokgak District, Buleleng Regency, Bali Province. The research method applied is observation by visual census with an underwater camera (underwater visual census) and SCUBA diving equipment at a depth range of 5-25 meters. Observation data were collected in April 2021. A total of 15 species were found at ten dive sites.: Chromodoris annae, Chromodoris magnifica, Goniobranchus reticulatus, Hypselodoris apolegma, Hypselodoris bullockii, Nembrotha cristata, Nembrotha kubaryana, Nembrotha sp, Notodoris serenae, Phyllidia elegans, Phyllidia varicosa, Phyllidiopsis pipecki, Phyllidiopsis shireenae. The most dominant species was a member of Phyllidia genus, and an uncommon species is Goniobranchus reticulatus.

Sea slugs (Gastropoda: Heterobranchia) associated with Autonomous Reef Monitoring Structures (ARMS) in southern Gulf of Mexico and Mexican Caribbean Sea

Abstract Cryptic species in coral reefs, such as sea slugs, represent an important portion of their biodiversity, which is usually underestimated. Autonomous Reef Monitoring Structures (ARMS) have been implemented to estimate cryptic diversity in coral reefs. Therefore, this research aimed to contribute to the southern Gulf of Mexico (GM) and the Caribbean Sea (CAR) coral reefs’ sea slugs’ diversity and distribution using ARMS as a collection method. Fifty-eight ARMS were placed at three coral reefs in the GM and CAR, recovered after 1–2 years and then, disassembled at the laboratory. Plates were individually placed in trays with seawater, where we searched for sea slugs. A total of 242 organisms were found belonging to 31 species; 20 of them were identified to the species level, while 11 were determined up to genus or family. More than half of the species (19) were found in Bajo de 10 (GM), while 15 species were found in the CAR localities. Unlike previous studies, we assessed sea slugs’ diversity exclusively by an indirect sampling method. In this work, we found 9.4% of the sea slug diversity recorded in the Caribbean, and we report four determined species for the first time in the country. New records of species, and even one family for the GM stress the gap of information that we still need to fulfil in the area. We recognize ARMS as a useful tool to find juvenile, cryptic and rare species of sea slugs, as well as to standardize their quantification and record their diversity.

The effect of environmental factors on spatial-temporal variation of heterobranch sea slug community in northern Taiwan

Sea slug (Subclass Heterobranchia) biodiversity is an important element of marine coral reef communities. However, due to their small size and cryptic behavior, few studies have examined their spatiotemporal variation. Taiwan is in the middle of East Asia Island Arcs, where it is one of the hotspots of sea slug diversity. Meanwhile, the northeast coast of this island lies within the subtropical monsoon region, where the climate shifts from a warm southwest monsoon (SW: May to Sep) to a cold northeast monsoon (NE: Oct to Apr). Between the monsoons, distinct temperatures and currents result in different community structures. To understand how those environmental factors (i.e., monsoon season, diel period and water depth) influence sea slug species richness and assemblages, we surveyed these invertebrates monthly at both night and day by diving in a marine protection area (CJ) and at a nearby non-protected site (MR) from May 2020 to Apr 2021. We showed that the species composition in our sampling area was highly consistent with what was found in Okinawa and Pescadores island, but less similar to those in southern Taiwan or Hong Kong. On the northeast coast of Taiwan, sea slug number and abundance were both higher in CJ than MR, but biodiversity (H’) and the species evenness indexJ’ was lower in CJ than MR. Additionally, cluster analysis indicated that the sea slug assemblages differed between the two sites. Monsoon season significantly influenced both species richness and species assemblages, with species richness during SW being significantly higher than in the NE monsoon and species assemblages also being distinct between these two seasons. Moreover, species richness increased with water depth (within the surveyed range of 0-25 m). Diel period did not exert a strong impact on sea slug biodiversity, except for species richness at CJ, where it was higher during the day than at night. Our study suggested that changing currents between the monsoon seasons could transport individuals originating from either the north or south of these island arcs. Furthermore, temperature and food sources may differ between seasons and depths, thereby influencing sea slug assemblages in this region.

A new species of cephalaspidean sea slug of the genus Melanochlamys Cheeseman, 1881 (Heterobranchia: Aglajidae) from the Bay of Bengal, India

ABSTRACT A new species of head-shield sea slug, Melanochlamys bengalensis, is described from the northern part of the eastern coast of India using both external and internal morphological characters. Its novel status is supported by a molecular analysis. The maximum likelihood (ML) genetic tree (COI gene sequence) indicates that the new species represents a distinct clade compared to the other species of the genus Melanochlamys. The K2P distance of the new species is 16.2–23.7%, which is considerably more than the other congeners. This species was collected from the intertidal zone of the sandy beaches of Bakkhali, Tajpur, New Digha, Udaipur, Talsari, Chandipur and Kanika Island. Additionally, the list of valid species and distribution of all members of the genus Melanochlamys is presented herein.

Citizen Scientists Record Significant Range Extensions for Tropical Sea Slug Species in Subtropical Eastern Australia

The Sea Slug Census program in Australia engages with citizen scientists to record the diversity and distribution of sea slugs across multiple locations. The program has consistently recorded shifts in distribution patterns but a recent, nine-day census in subtropical eastern Australia recorded unprecedented range extensions of tropical species. Seven species (six chromodorids and one polycerid) were found further south of their previously known distribution with Hypselodoris bertschi being recorded for the first time in Australia. These observations suggested the recent transport of larvae via the East Australian Current with recruitment to coastal sites possibly promoted by a protracted period of strong onshore winds associated with the 2021/22 La Niña in the western Pacific. With the increasing frequency of poleward range extensions of marine taxa, citizen science programs such as the Sea Slug Census provide the opportunity to substantially increase monitoring efforts. Linking with iNaturalist strengthens the value of the observations through online peer review to confirm species identities as well as the incorporation of substantiated (Research Grade) records into international biodiversity databases such as GBIF.

New records of nudibranchs and a sacoglossan (Gastropoda: Heterobranchia) from Sempu Strait, Indonesia

Abstract. Andrimida A. 2022. New records of nudibranchs and a sacoglossan (Gastropoda: Heterobranchia) from Sempu Strait, Indonesia. Indo Pac J Ocean Life 6: 1-9. This study reports the additional records of fourteen heterobranch sea slug species from Sempu Strait, East Java, Indonesia, in which thirteen species belong to the nudibranchia order, and one species belongs to the sacoglossa order. These species belong to seven families: Plakobranchidae (1 species), Polyceridae (1 species), Discodorididae (2 species), Chromodorididae (7 species), Flabellinidae (1 species), Eubranchidae (1 species), and Facelinidae (1 species). All of these species are recorded for the first time from the Sempu Strait. There are two species that only could be identified to its genus, which are Chromodoris sp. and Eubranchus sp. This study also found additional record of Plocamopherus imperialis Angas, 1864 on the tropical waters, where this species formerly believed only exclusively distributed along the subtropical waters of Eastern Australia and Northern New Zealand. Combined with the previous study on Sempu Strait, to date, 59 species of heterobranch sea slug have been reported and recorded in this area. Species identification was conducted by carefully examining the morphological features of each specimens encountered during the surveys.

Sea slug night fever: 39 new records of elusive heterobranchs in the western Mediterranean (Mollusca: Gastropoda)

ABSTRACT Citizen (or community) science has provided copious and valuable information about charismatic marine taxa such as heterobranch gastropods, thus contributing enormously to the known geographic distribution of many sea slug species. This study reports new records of elusive sea slugs in the coastal western Mediterranean (especially on the Catalan and French Mediterranean coasts) and contributes to new ecological information regarding their phenology, diet and behaviour. Out of 39 species reported here, 23 are new records for the Catalan coast (NE Spain), three are new records of pelagic pteropods for the Spanish Iberian coast, and eight are new records for the French Mediterranean coast. With 25 species found active at night, this study highlights the importance of sampling at night and in shallow, often under-sampled waters with high species diversity. Shallow waters usually have less diving activity and are harder to survey with heavy scuba equipment. We believe that the high-quality photos herein and the related species information will enable researchers, divers and the community to find and recognise these rare species in the Mediterranean basin.

Transcriptomics provides a robust framework for the relationships of the major clades of cladobranch sea slugs (Mollusca, Gastropoda, Heterobranchia), but fails to resolve the position of the enigmatic genus Embletonia

BackgroundThe soft-bodied cladobranch sea slugs represent roughly half of the biodiversity of marine nudibranch molluscs on the planet. Despite their global distribution from shallow waters to the deep sea, from tropical into polar seas, and their important role in marine ecosystems and for humans (as targets for drug discovery), the evolutionary history of cladobranch sea slugs is not yet fully understood.ResultsTo enlarge the current knowledge on the phylogenetic relationships, we generated new transcriptome data for 19 species of cladobranch sea slugs and two additional outgroup taxa (Berthella plumula and Polycera quadrilineata). We complemented our taxon sampling with previously published transcriptome data, resulting in a final data set covering 56 species from all but one accepted cladobranch superfamilies. We assembled all transcriptomes using six different assemblers, selecting those assemblies that provided the largest amount of potentially phylogenetically informative sites. Quality-driven compilation of data sets resulted in four different supermatrices: two with full coverage of genes per species (446 and 335 single-copy protein-coding genes, respectively) and two with a less stringent coverage (667 genes with 98.9% partition coverage and 1767 genes with 86% partition coverage, respectively). We used these supermatrices to infer statistically robust maximum-likelihood trees. All analyses, irrespective of the data set, indicate maximal statistical support for all major splits and phylogenetic relationships at the family level. Besides the questionable position of Noumeaella rubrofasciata, rendering the Facelinidae as polyphyletic, the only notable discordance between the inferred trees is the position of Embletonia pulchra. Extensive testing using Four-cluster Likelihood Mapping, Approximately Unbiased tests, and Quartet Scores revealed that its position is not due to any informative phylogenetic signal, but caused by confounding signal.ConclusionsOur data matrices and the inferred trees can serve as a solid foundation for future work on the taxonomy and evolutionary history of Cladobranchia. The placement of E. pulchra, however, proves challenging, even with large data sets and various optimization strategies. Moreover, quartet mapping results show that confounding signal present in the data is sufficient to explain the inferred position of E. pulchra, again leaving its phylogenetic position as an enigma.

New records of nudibranchs and a cephalaspid from Kuwait, northwestern Arabian Gulf (Mollusca, Heterobranchia)

In this study five new records and two probably undescribed species of heterobranch sea slugs placed in four genera, three families, and two orders are reported from Kuwait, northwestern Arabian / Persian Gulf with details and photographs. The present study increases the heterobranch diversity in Kuwaiti waters from 35 to 40 species. The range of habitats in Kuwait provides a vital opportunity for further investigation to understand the actual faunal diversity.