Sea Slug Species Research Articles

An integrative approach to the systematics of the Berthella californica species complex (Heterobranchia: Pleurobranchidae).

Berthella californica (W. H. Dall, 1900) is a widespread species of heterobranch sea slug distributed across the North Pacific Ocean, from Korea and Japan to the Galapagos Islands. Two distinct morphotypes are observed in B. californica, which differ in external coloration, egg-mass morphology and geographic distribution (with the exception of a small range overlap in Southern California). Molecular and morphological data obtained in this study reveals that these two morphotypes constitute distinct species. The name B. californica (type locality: San Pedro, California) is retained for the southern morphotype, whereas the name Berthella chacei (J. Q. Burch, 1944) (type locality: Crescent City, California) is resurrected for the northern morphotype. Moreover, molecular phylogenetic analyses recovered B. californica as sister to Berthellina, in a well-supported clade separate from Berthella, suggesting that the classification of B. californica may need additional revision.

Coping with Starvation: Contrasting Lipidomic Dynamics in the Cells of Two Sacoglossan Sea Slugs Incorporating Stolen Plastids from the Same Macroalga.

Several species of sacoglossan sea slugs are able to sequester chloroplasts from algae and incorporate them into their cells. However, the ability to maintain functional "stolen" plastids (kleptoplasts) can vary significantly within the Sacoglossa, giving species different capacities to withstand periods of food shortage. The present study provides an insight on the comparative shifts experienced by the lipidome of two sacoglossan sea slug species, Elysia viridis (long-term retention of functional chloroplasts) and Placida dendritica (retention of non-functional chloroplasts). A hydrophilic interaction liquid chromatography-mass spectrometry approach was employed to screen the lipidome of specimens from both species feeding on the macroalga Codium tomentosum and after 1-week of starvation. The lipidome of E. viridis was generally unaffected by the absence of food, while that of P. dendritica varied significantly. The retention of functional chloroplasts by E. viridis cells allows this species to endure periods of food shortage, while in P. dendritica a significant reduction in the amount of main lipids was the consequence of the consumption of its own mass to endure starvation. The large proportion of ether phospholipids (plasmalogens) in both sea slug species suggests that these compounds may play a key role in chloroplast incorporation in sea slug cells and/or be involved in the reduction of the oxidative stress resulting from the presence of kleptoplasts.

Molecular and morphological systematics of Bursatella leachii de Blainville, 1817 and Stylocheilus striatus Quoy & Gaimard, 1832 reveal cryptic diversity in pantropically distributed taxa (Mollusca : Gastropoda : Heterobranchia)

The ragged sea hare (Bursatella leachii) and the long-tailed sea hare (Stylocheilus striatus) are two widely distributed species of benthic heterobranch sea slugs. In this paper, integrative taxonomic analyses have been conducted to detect possible cryptic diversity. Our results revealed that both nominal species are actually species complexes, consisting of five genetically distinct taxa. Two of them belong to the genus Bursatella and three to the genus Stylocheilus. The name B. leachii is retained for a widely distributed species, present in the Atlantic, the Mediterranean, and parts of the Indo-Pacific region. The name B. ocelligera is resurrected for the other species, restricted to the Indo-Pacific and co-occurring with B. leachii in that area. With the present data, it is not possible to test whether B. leachii and B. ocelligera have evolved allopatrically in the Atlantic and Indo-Pacific or sympatrically in the latter. Bursatella leachii has been able to maintain gene flow between the Atlantic and the Indo-Pacific Oceans, possibly because of a combined effect of the Agulhas Leakage process and the ability to survive the colder waters of South Africa. On the contrary, the three species of Stylocheilus are allopatric; the name S. striatus is retained for an Indo-Pacific species, while the names S. polyomma and S. rickettsi are resurrected for species inhabiting the Western Atlantic and the Eastern Pacific respectively. Finally, the discovery of a museum specimen mistakenly identified as B. leachii, but bearing a shell in its adult form, led to the resurrection of the genus Phycophila, previously synonymised with Aplysia. Phycophila euchlora, the only species described to date, is distributed in the Central and Western Pacific Ocean.

Assessing cryptic marine fauna diversity as underwater macrophotography (UMP) objects in Sempu Strait, Indonesia

Cryptic marine fauna refers to organisms that live inside habitats that hidden from direct exposure to their outer environment. Its cryptic nature made these animals rarely observed, and hence understudied. Whereas, they are very popular among experienced divers alike as underwater macrophotography objects. The aim of this study is to assess the diversity of cryptic marine fauna on the proximity of coral reef area at Sempu Strait to bring up its underwater macrophotography tourism potential. While the definition of cryptic marine fauna itself could include any major group of marine organisms, we limit the extent of our study only into the four most popular animal groups in underwater macrophotography which are: fishes, sea slugs, arthropods, and flatworms. We conducted underwater surveys using roving diver technique spanning from October 2017 to June 2019 at eleven dive sites of Sempu Strait and yielded 84 species that consists of 45 species of sea slug, 29 Species of fish, 8 species of arthropods, and 2 species of flatworms. The overall fauna diversity shows that Sempu Strait has high diversity of sea slug and cryptic fishes, while the site-specific diversity shows that Stumbut dive site has the highest marine cryptic fauna diversity.

Diversity and Distribution of Sea Slugs (Gastropods: Heterobranchia) in Sempu Strait, Indonesia

The heterobranch sea slugs are one of the most under-studied marine lifeforms found around the Sempu Strait Area. Currently, the records of their occurrences around this area are only known from the underwater macrophotography enthusiast’s collection and have not been published on a scientific article. We conducted underwater surveys spanning from October 2017 to June 2019 at eleven dive sites of Sempu Strait and yielded 45 different species of heterobranch sea slugs, including 35 species of Nudibranchia, 6 Aplysiida (Anaspidea), 2 Cephalaspidea, and 2 Sacoglossa. The analysis of the sea slugs occurrence on Sempu Strait reveals that the areas around the Western Sempu Strait, including Rumah Apung, Kondang Buntung, Tiga Warna, and Stumbut have the most diverse sea slugs species, even though the majority of the species have a low sighting frequency. The analysis also revealed that roughly a third of the sea slugs encountered on the Sempu Strait areas are found on the coral rubble substrate. This study revealed that Sempu Strait has slightly lower sea slug species diversity than another nearby studied site. The records provided here hopefully could help to encourage macro-photography recreational dive activities to further develop the ecotourism sector around this area.

Eggs sunny-side up: A new species of Olea, an unusual oophagous sea slug (Gastropoda: Heterobranchia: Sacoglossa), from the western Atlantic.

Nearly all of the recognized species of sea slugs in clade Sacoglossa (about 300 taxa) are herbivorous, using a uniseriate radula in suctorial feeding. The only exceptions are a pair of monotypic genera in the ceratiform family Limapontiidae: Olea Agersborg, 1923 from the northeastern Pacific, and Calliopaea d'Orbigny, 1837 from the northeastern Atlantic coast of Europe and the Mediterranean. Both genera feed on the eggs of other heterobranchs, notably cephalaspideans, and lack cerata on the anterior dorsum. Major differences are that C. bellula d'Orbigny, 1837 has more cerata than O. hansineensis Agersborg, 1923, a more typical radula with ascending and descending rows of fully-formed teeth, and a much longer penial stylet. Here, we describe a new egg-eating sacoglossan species from the subtropical Gulf of Mexico coast of Florida, U.S.A. Phylogenetic relationships inferred from analyses of a four-gene dataset including 219 sacoglossan species indicated the new taxon (O. hensoni n. sp.) belongs to Olea. The generic placement of the new species is also supported by its highly reduced radula and comparatively short penial stylet. A full description of the reproductive, digestive, and nervous systems is also provided. Finding a new Olea species in the warm waters of the western Atlantic was surprising, given the genus was previously known only from the cold northern Pacific, and suggests further diversity in oophagous sacoglossans may await discovery.

Sea slugs (Gastropoda: Heterobranchia) from two remote reefs of the Southern Gulf of Mexico: Cayo Arenas and Cayo Arcas

Two field trips were made during 2017 to Cayo Arenas and Cayo Arcas, southern Gulf of Mexico. Direct and indirect sampling methods focused on shell-less marine heterobranchs were carried out. As a result, 30 species of sea slugs are reported for the first time from these 2 remote reefs off the Yucatan Peninsula. From these, 7 species hold new distribution records for the Gulf of Mexico: Sclerodoris worki, Platydoris angustipes, Polycera odhneri, Hexabranchus morsomus, Limenandra nodosa, Petalifera ramose, and Hermaea cruciata . Hexabranchus morsomus is a considerable west geographical range extension from the known distribution range, so far restricted to the Caribbean Sea. Nine specimens were identified up to genus level: Cuthona sp., Haminoea sp., Petalifera sp. and Elysia sp. With the present contribution, the sea slug richness in the Campeche Bank increases to 94 species.

Colour pattern measurements successfully differentiate two cryptic Onchidiidae Rafinesque, 1815 species

Cryptic species, by definition, appear very similar to each other. In the absence of obvious external morphological differences, quantitative measurements of fine-scale colour pattern differences may be used to distinguish between cryptic species. To demonstrate how this is accomplished, 30 specimens each of two cryptic onchidiid sea slug species in Singapore were collected and identified by sequencing a fragment of the mitochondrial cytochrome c oxidase subunit I gene. Sequences displayed a clear barcode gap: intraspecific distances (0–0.4%) and interspecific distances (4.8–5.5%) were distinct. To quantify colour patterns, eight pattern properties on the animals’ dorsal surface were measured using the PAT-GEOM software. Linear discriminant analysis and classification tree analysis were able to classify specimens with 80% and 81.7% accuracy respectively, and both identified proportion cover and randomness as the most important properties for differentiating the two species. Agreement between the genetic and pattern data is demonstrated by a significant correlation between the pairwise genetic and pattern distance matrices, as well as the significantly greater interspecific than intraspecific distances in both datasets. These results demonstrate that fine-scale pattern differences can be used to differentiate Peronia cryptic species. This approach has potential applications for a range of disciplines, including behaviour and ecology, and as an additional line of evidence for integrative taxonomy.

Characterization of the complete mitochondrial genome of Hermissenda emurai (Baba, 1937) (Nudibranchia, Facelinidae)

Hermissenda emurai is a species of sea slugs in the northwestern Pacific region. In this study, the complete mitochondrial genome of H. emurai (Mollusca: Facelinidae) collected from Korea was recorded. The assembled mitogenome of H. emurai was circular and 13,880 bp in length, including 27.1% A, 15.9% C, 20.5% G, and 36.5% T nucleotide distributions. The overall A–T composition was 63.6% while the G–C composition was 36.4%. Phylogenetic analysis according to 12 protein coding genes (atp8 gene excluded) showed that H. emurai clustered with Sakuraeolis japonica in the order Nudibranchia.

Lipidomics of solar-power animals: a tool to unravel the process of kleptoplasty

Lipidomics of solar-power animals: a tool to unravel the process of kleptoplasty

Distinct Bleaching Resilience of Photosynthetic Plastid-Bearing Mollusks Under Thermal Stress and High CO2 Conditions.

The impact of temperature on photo-symbiotic relationships has been highly studied in the tropical reef-forming corals but overlooked in less charismatic groups such as solar-powered sacoglossan sea slugs. These organisms display one of the most puzzling symbiotic features observed in the animal kingdom, i.e., their mollusk-plastid association, which enables them to retain photosynthetic active chloroplasts (i.e., kleptoplasts) retrieved from their algae feed sources. Here we analyze the impact of thermal stress (+4°C) and high pCO2 conditions (ΔpH = 0.4) in survival, photophysiology (i.e., bleaching, photosynthetic efficiency, and metabolism) and stress defense mechanisms (i.e., heat shock and antioxidant response) of solar-powered sacoglossan sea slugs, from tropical (Elysia crispata) and temperate (E. viridis) environments. High temperature was the main factor affecting the survival of both species, while pH only affected the survival of the temperate model. The photobiology of E. viridis remained stable under the combined scenario, while photoinhibition was observed for E. crispata under high temperature and high pCO2. In fact, bleaching was observed within all tropical specimens exposed to warming (but not in the temperate ones), which constitutes the first report where the incidence of bleaching in tropical animals hosting photosynthetic symbionts, other than corals, occurs. Yet, the expulsion of kleptoplasts by the tropical sea slug, allied with metabolic depression, constituted a physiological response that did not imply signs of vulnerability (i.e., mortality) in the host itself. Although the temperate species revealed greater heat shock and antioxidant enzyme response to environmental stress, we argue that the tropical (stenotherm) sea slug species may display a greater scope for acclimatization than the temperate (eurytherm) sea slug. E. crispata may exhibit increased capacity for phenotypic plasticity by increasing fitness in a much narrower thermal niche (minimizing maintenance costs), which ultimately may allow to face severe environmental conditions more effectively than its temperate generalist counterpart (E. viridis).

Cryptic speciation yields remarkable mimics: A new genus of sea slugs that masquerade as toxic algae (Caulerpa spp.)

Abstract“Cryptic” can refer to species that match their background through camouflage or disruptive colouration, or in taxonomy to externally similar but unrecognized congeners. In adaptive resemblance, organisms resemble parts of a larger host animal or plant on which the mimic is highly cryptic. Mimetic lineages that radiate onto superficially similar hosts may contain cryptic species in both senses: taxa that are difficult to detect, and challenging for taxonomists to distinguish. Here, we describe a new genus and four species of herbivorous sea slugs (Gastropoda, Heterobranchia, Sacoglossa), including remarkable mimics of toxic green algae (Caulerpa spp.) on which the slugs feed. The long‐recognized Stiliger smaragdinus Baba 1949 is highly mimetic of “sea grapes” (Caulerpa racemosa‐lentillifera), but phylogenetic analyses of four genes indicated Stiliger was polyphyletic: the name‐bearing species grouped within Placida, whereas Caulerpa‐mimetic lineages were phylogenetically distinct. We erect the genus Sacoproteus gen. n. for S. smaragdinus (Baba 1949), and describe four new species: S. nishae sp. n. from the Indo‐Pacific, which mimics Caulerpa chemnitzia; Sacoproteus yhiae sp. n. and Sacoproteus browni sp. n. from southern Australia, which mimic Caulerpa cactoides and Caulerpa gemminata; and Sacoproteus thomasleei sp. n., a non‐mimetic west Pacific species that shared key features. Stiliger s.s. and Placida species show crypsis and aposematism but not host mimicry, although Stiliger spp. feeding on undefended algae may be Batesian mimics. Investigating the ecology and biogeography of Sacoproteus gen. n. will yield insight into how selection generates such extraordinary examples of adaptive resemblance in the marine realm.

Beyond Capricornia: Tropical Sea Slugs (Gastropoda, Heterobranchia) Extend Their Distributions into the Tasman Sea

There is increasing evidence of poleward migration of a broad range of taxa under the influence of a warming ocean. However, patchy research effort, the lack of pre-existing baseline data, and taxonomic uncertainty for some taxa means that unambiguous interpretation of observations is often difficult. Here, we propose that heterobranch sea slugs provide a useful target group for monitoring shifts in distribution. As many sea slugs are highly colourful, popular with underwater photographers and rock-pool ramblers, and found in accessible habitats, they provide an ideal target for citizen scientist programs, such as the Sea Slug Census. This maximises our ability to rapidly gain usable diversity and distributional data. Here, we review records of recent range extensions by tropical species into the subtropical and temperate waters of eastern Australia and document, for the first time in Australian waters, observations of three tropical species of sea slug as well as range extensions for a further six to various locations in the Tasman Sea.

Kleptoplast photosynthesis is nutritionally relevant in the sea slug Elysia viridis

Several sacoglossan sea slug species feed on macroalgae and incorporate chloroplasts into tubular cells of their digestive diverticula. We investigated the role of the “stolen” chloroplasts (kleptoplasts) in the nutrition of the sea slug Elysia viridis and assessed how their abundance, distribution and photosynthetic activity were affected by light and starvation. Elysia viridis individuals feeding on the macroalga Codium tomentosum were compared with starved specimens kept in dark and low light conditions. A combination of variable Chl a fluorescence and hyperspectral imaging, and HPLC pigment analysis was used to evaluate the spatial and temporal variability of photopigments and of the photosynthetic capacity of kleptoplasts. We show increased loss of weight and body length in dark-starved E. viridis as compared to low light-starved sea slugs. A more pronounced decrease in kleptoplast abundance and lower photosynthetic electron transport rates were observed in dark-starved sea slugs than in low light-starved animals. This study presents strong evidence of the importance of kleptoplast photosynthesis for the nutrition of E. viridis in periods of food scarcity. Deprived of photosynthates, E. viridis could accelerate the breakdown of kleptoplasts in the dark to satisfy its’ energy requirements.

Embryonic Abnormalities of Two Seaslug Species from South Spain

The spawns and the embryonic development of the nudibranch species Polycera aurantiomarginata (Garcia and Bobo in Cah Biol Mar 25:361–373, 1984) and Polycera quadrilineata (Muller, 1776) were studied for two years. Throughout this study some abnormalities were detected in the embryonic and larval development of both species. First, the spawn seemed a pearl necklace because the eggs did not have intracapsular liquid and the capsular wall appeared very close to the egg. Second, embryos showed a normal development until the gastrula stage then a transparent sphere with two opposite cilia tuffs was developed instead the normal veliger larva. Third, aberrant veliger larvae were detected, in P. quadrilineata some of them showed a black zone. In P. aurantiomarginata the teratological events could be related to adult size and spawn number. Animals smaller than 15 mm never laid viable spawns while the egg masses of adults with 16–25 mm in size showed abnormalities in 80%. In the other hand, it is remarkable that animals bigger than 25 mm, which had already spawned several times, laid egg masses with abnormalities. The percentage of pearl necklace spawns was bigger in P. aurantiomarginata than in P. quadrilineata, while the percentage of spawns with aberrant veligers was bigger in the last one. However the values of egg masses with transparent ciliated spheres were similar in both species.

Molecular determination of kleptoplast origins from the sea slug Plakobranchus ocellatus (Sacoglossa, Gastropoda) reveals cryptic bryopsidalean (Chlorophyta) diversity in the Hawaiian Islands.

The sacoglossan sea slug species complex Plakobranchus ocellatus is a common algivore throughout the tropical Pacific, including the Hawaiian Islands. Plakobranchusocellatus is kleptoplastic-it sequesters and retains algal chloroplasts-a characteristic that can be exploited to molecularly characterize diminutive bryopsidalean algae that are typically difficult to locate, collect, and identify. Previous DNA barcode analyses of both P.ocellatus and its kleptoplasts have been conducted primarily in the western Pacific and have only minimally sampled the most eastern populations in the Hawaiian Islands. Using two chloroplast markers, rbcL and tufA, kleptoplast samples from an Oahu population of P.ocellatus were amplified and cloned to identify their algal sources. Plakobranchusocellatus sequester chloroplasts from up to 11 bryopsidalean algal species, all but one being diminutive in thallus size. Notably, eight of the detected algal species were new records to the Hawaiian Islands. A sequestration preference study demonstrated that the O'ahu population of P.ocellatus preferentially sequesters chloroplasts from diminutive, epilithic taxa. Using coxI barcoding of P.ocellatus, we showed the O'ahu population to be part of a clade that includes sequences from the neighboring island Maui, Australia, and the Philippines. The use of P.ocellatus as a novel sampling tool allows the exploration of the green algal community diversity and composition at a fine scale.

Shallow water sea slugs (Gastropoda: Heterobranchia) from the northwestern coast of the Sea of Japan, north of Peter the Great Bay, Russia.

The coast of northern Primorye region, north of Peter the Great Bay has been sparsely studied in regards to its molluscan fauna, with just a few works reviewing the distribution of local mollusks. This work presents a survey of the shallow water heterobranch sea slugs currently occurring around Kievka Bay to Oprichnik Bay, Russia. Thirty-nine species of sea slugs were found in this study and the new species Cadlina olgae sp. nov., described herein. Most (24) of the species occurring in the area have widespread ranges in the northern Pacific Ocean. The eight species are endemic for the Sea of Japan and adjacent part of the Sea of Okhotsk. Seven other occur also in northern Atlantic and Arctic waters. Thirteen found species are not known from Peter the Great Bay but known from adjacent northern Pacific waters. The finding of a previously undescribed species emphasizes the need of further surveys, particularly in subtidal and deeper waters, in order to improve the knowledge on this neglected fauna in Primorye.

Identification guide to the heterobranch sea slugs (Mollusca: Gastropoda) from Bocas del Toro, Panama

The Bocas del Toro Archipelago is located off the Caribbean coast of Panama. Until now, only 19 species of heterobranch sea slugs have been formally reported from this area; this number constitutes a fraction of total diversity in the Caribbean region. Based on newly conducted fieldwork, we increase the number of recorded heterobranch sea slug species in Bocas del Toro to 82. Descriptive information for each species is provided, including taxonomic and/or ecological notes for most taxa. The collecting effort is also described and compared with that of other field expeditions in the Caribbean and the tropical Eastern Pacific. This increase in known diversity strongly suggests that the distribution of species within the Caribbean is still poorly known and species ranges may need to be modified as more surveys are conducted.

Southern range extensions for twelve heterobranch sea slugs (Gastropoda: Heterobranchia) on the eastern coast of Australia

Port Stephens, on the central New South Wales coast, provides ideal oceanographic and benthic conditions for the settlement and growth of larvae of tropical species delivered from the north by the East Australian Current. The popularity of the bay for recreational and scientific diving has facilitated extensive documentation of the biota over several decades, confirming its high biodiversity. Of the 313 species of heterobranch sea slugs recorded from Port Stephens to date, 30 are not known to occur further south. Our observations increase the number of taxa with a southern distribution limit at Port Stephens by 12 species and add to a growing list of marine taxa that are progressively extending their southern range, potentially as a result of climate change.

Shallow water heterobranch sea slugs (Gastropoda: Heterobranchia) from the Región de Atacama, northern Chile.

The coast of northern Chile has been sparsely studied in regards to its invertebrate fauna, with just a few works reviewing the distribution of local mollusks. This work presents a survey of the shallow water heterobranch sea slugs currently occurring around the port of Caldera (27 °S), in the Región de Atacama, northern Chile. Eight species of sea slugs were found in this study: Aplysiopsis cf. brattstroemi (Marcus, 1959), Baptodoris peruviana (d’Orbigny, 1837), Diaulula variolata (d’Orbigny, 1837), Doris fontainii d’Orbigny, 1837, Onchidella marginata (Couthouy in Gould, 1852), Phidiana lottini (Lesson, 1831), Tyrinna delicata (Abraham, 1877) and the new species Berthella schroedli sp. nov., described herein. All of the species found in the area are endemic to South America, having distributions in the southeastern Pacific and South Atlantic Oceans, from Ancash, Perú to Peninsula Valdés, Argentina, and two of them represent species which are endemic to the Chilean coasts (Aplysiopsis cf. brattstroemi and Berthella schroedli). The finding of a previously undescribed species emphasizes the need of further surveys, particularly in subtidal and deeper waters, in order to improve the knowledge on this neglected fauna in Atacama.