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Article

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

by
Tauana J. Cunha
1,2,*,
Jose Fernández-Simón
3,
Macy Petrula
1,
Gonzalo Giribet
1 and
Juan Moles
1,3,*
1
Museum of Comparative Zoology, Department of Organismic & Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA
2
Field Museum of Natural History, 1400 S Lake Shore Drive, Chicago, IL 60605, USA
3
IRBio & Department of Evolutionary Biology, Ecology, and Environmental Sciences, Faculty of Biology, University of Barcelona, Av. Diagonal 643, 08028 Barcelona, Spain
*
Authors to whom correspondence should be addressed.
†
urn:lsid:zoobank.org:pub:0A8395D7-E73B-4018-84AD-5EB32CBB05BE.
Diversity 2023, 15(2), 219; https://doi.org/10.3390/d15020219
Submission received: 16 December 2022 / Revised: 13 January 2023 / Accepted: 18 January 2023 / Published: 3 February 2023
(This article belongs to the Special Issue Zoological Checklists: From Natural History Museums to Ecosystems)
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Abstract

:
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.

1. Introduction

The diversity of marine species shared between the southwest Pacific and the islands and coasts of the Indian Ocean has been the basis for the recognition of a common biogeographical realm [1], often referred to as the Indo-West Pacific. Nonetheless, the existence of cryptic species and species complexes has been increasingly recognized from taxa with such widespread distributions (e.g., [2,3]). To address both species delimitation and broad biogeographical patterns, it is crucial to have baseline data of species occurrences across areas, which is still lacking for many localities and invertebrate clades.
The Maldivian Archipelago comprises 26 atolls distributed in a chain stretching for over 820 km in the central Indian Ocean [4] (Figure 1). It is the seventh largest coral reef in the world [5], with 1190 islands sprinkled over approximately 90,000 km2 of ocean [4]. Two seasons characterized by strong winds in opposing directions (wet SW monsoon between May and September, dry NE monsoon between November and March [6]) have been suggested as a mechanism for larval transport from the western Indian Ocean and from Indonesia [7], which could contribute to the widespread species distributions of the Indo-Pacific.
Faunistic surveys in the Maldives date back to an expedition by J. Stanley Gardiner throughout the archipelago [8], which resulted in the first inventory of mollusks in the area [9], as well as a specific list of nudibranchs [10]. Three other broad expeditions have covered marine mollusks since then (reviewed in [11]), resulting in inventories of multiple atolls [12,13]. Additional work has produced mollusk or invertebrate lists from specific atolls [11,14,15] or particular clades (e.g., Costellariidae [7]; Rissoinidae [16]; Polyplacophora [17]). In this study, we focus on two of the six subclasses of gastropods: Heterobranchia, with a worldwide marine diversity of about 9000 species, and Vetigastropoda, with over 4000 extant species [18]. Heterobranch-specific studies from the Maldives include Eliot [10], Marcus and Marcus [19], Rudman [20], and Yonow [21,22], while no publication so far has specifically targeted groups of vetigastropods.
In addition to inventories still being sparse, comprehensive documentation of identified fauna is often lacking, including vouchers in museum collections. In this paper, we provide a checklist of the heterobranch and vetigastropod fauna from the Faafu Atoll with specimen vouchers, photographic evidence of live specimens, and genetic barcode data for most of the collected species, which collectively will allow future cross-verification of species identities and further work on the ecology and evolution of marine biodiversity. We also compiled literature from other parts of the archipelago to provide a comprehensive checklist of both gastropod clades for the Maldives.

2. Material and Methods

2.1. Sampling and Checklist

Gastropods were collected in April 2019 during 23 visits to 14 unique sites in the Faafu Atoll (also known as North Nilandhe Atoll) and one site in the capital Malé (North Malé Atoll), Maldives (Figure 1). The main targets of the campaign were heterobranchs, and most vetigastropods found during fieldwork were also sampled. Specimens were collected by hand in benthic environments on and under rocks, rubble, corals, algae, and seagrass meadows while scuba diving or snorkeling. Twelve day-dives of about an hour each were performed by two divers down to 35 m depth, and the material was processed at the Marine Research and High Education Center (MaRHE Center) at Magoodhoo Island. Heterobranchs and vetigastropods were preliminarily identified following Gosliner et al. [23] and Okutani [24], respectively. Live animals were photographed in the lab with a Canon 80D using the Canon MP-E 65 mm and Canon 100 mm macro lenses. Specimens were anesthetized with 7.5% MgCl2 and preserved in 95% ethanol, with selected individuals also preserved in RNAlater for future studies. All material was deposited in the Malacology Collection in the Museum of Comparative Zoology (MCZ, https://mczbase.mcz.harvard.edu), Harvard University (see Table S1 for voucher information). Identifications were refined with specialized literature [25,26,27,28,29,30,31,32]. COI sequence barcodes were also used for identification. Occurrence data for the entire Maldives were gathered from the Ocean Biodiversity Information System database (OBIS) [33] and literature records [9,10,11,12,13,14,15,19,21,22,23,26,27,34,35,36,37,38,39,40]. Maps and plots were built with the packages ggmap [41] and ggplot2 [42] in the R environment [43].

2.2. DNA Barcoding

DNA was extracted from either foot or mantle tissue of individual specimens using the Qiagen DNeasy Blood and Tissue Kit following the manufacturer’s protocol. For particularly small species, the entire organism was used for DNA extraction. The mitochondrial protein-coding gene cytochrome c oxidase subunit I (COI) was amplified using primer pairs LCO1490/HCO2198 [44] or jgLCO1490/jgHCO2198 [45]. Amplification reactions were carried out in a 25 μL-reaction volume using PuReTaq Ready-To-Go PCR Beads (GE Healthcare) with 1 μL of each primer, 2 μL of genomic DNA, and molecular-grade deionized water up to 25 μL. Amplification conditions included an initial denaturation step at 94 °C for 5 min, followed by 40 cycles of 94 °C for 15 s, 48 °C for 5 s, and 68 °C for 15 s, and a final extension at 72 °C for 7 min. Amplified products were purified using ExoSAP-IT (Affymetrix) and sequenced using Big-Dye Terminator in an ABI Prism 3730 XL Analyzer (Applied Biosystems). Forward and reverse sequences for each sample were assembled and edited in Geneious (v. 9.1.8) (https://geneious.com, accessed on 15 November 2022). Sequences were screened for contamination with BLAST [46] and a gene tree inferred with RAxML (v. 7.2.8) [47] based on an alignment from MAFFT (v. 7.309) [48] (Figure S1). Sequences were deposited in GenBank (accession numbers OQ206908–OQ207015; Table S1).

2.3. Genetic Delimitation of New Species

Phylogenetic trees were inferred for the new species being described here, together with publicly available sequences from related taxa retrieved from GenBank (https://www.ncbi.nlm.nih.gov/genbank, accessed on 15 November 2022) and BOLD Systems (https://boldsystems.org, accessed on 15 November 2022). Alignments were built in MAFFT using the G-INS-I algorithm implemented in Geneious. Phylogenetic analyses were performed on the CIPRES Science Gateway 3.3 (http://www.phylo.org, accessed on 15 November 2022), using maximum likelihood in IQ-TREE (v 2.1.2) [49] with the best substitution model selected in ModelFinder [50] accounting for codon positions. Branch support was estimated via ultrafast bootstrap with 1500 replicates [51]. Trees were visualized in FigTree (v. 1.4.4) (http://tree.bio.ed.ac.uk/software/figtree).
To further investigate the identity of the studied specimens, species delimitation tests were conducted. An Assemble Species by Automatic Partitioning (ASAP) [52] analysis was run using the web interface (https://bioinfo.mnhn.fr/abi/public/asap, accessed on 15 November 2022) with the Kimura (K80) distance model and default parameters (TS/TV = 2.0). Poisson Tree Processes (PTP) [53] was also run using the web interface (https://mptp.h-its.org, accessed on 15 November 2022).

3. Results

Marine heterobranchs and vetigastropods were collected in 14 sampling sites alongside the Faafu Atoll (mainly around Magoodhoo island) and one site in the capital Malé (Figure 1). In total, over 250 live specimens and 20 empty shells belonging to 104 species were collected, including 85 species of heterobranchs in 30 families and 19 species of vetigastropods in five families (Table 1). Over half of the species were collected in a single site (59%, Figure 2A), being mostly represented by a single specimen (58%, Figure 2B). Combined with previous occurrences from the literature, we compiled a checklist of 320 species for the Maldivian Archipelago (Table 1). About 64% of all species are only listed by one reference source (Figure 2C).
For heterobranchs, up to 46 species are reported for the first time in the Maldives (Table 1), thus increasing the country’s known heterobranch diversity by 26% and expanding their distribution ranges. Species of Acteonoidea, Pleurobranchida and Aplysiida (Figure 3), Cephalaspidea (Figure 4), Nudibranchia (Cladobranchia, Figure 5; Doridina, Figure 6), and Sacoglossa (Figure 7) were collected. The most collected order was Nudibranchia, with 52 species, followed by Cephalaspidea, with 15 species, and Sacoglossa, with 12. Barcodes were useful to identify most of the species, but in other cases, no identical sequences (below 95% BLAST identity) were found in GenBank (Figure 2D, Tables S2 and S3). From the 58 species of heterobranchs that were successfully barcoded, no identical sequences were available for 21 species of nudibranchs, two pleurobranchs, two cephalaspideans, and three sacoglossans. From those, cases of (pseudo)cryptic speciation are evident for Berthellina delicata (Figure 3b), Berthella martensi (Figure 3c), Colpodaspis thompsoni (Figure 4c), Philine orca (Figure 4m), Pteraeolidia aff. semperi (Figure 5p), and Elysia spp. (Figure 7b–e), with insufficient molecular or taxon sampling to further contribute to their taxonomic status. Nevertheless, six new species are described here based on molecular data and external morphological characters (see Systematics section below). Phylogenetic, species delimitation tests, and discrete external morphological characters aided in their discrimination and diagnosis and, therefore, are here officially described to provide taxonomic assistance to the species of the genera Limenandra, Eubranchus, Sakuraeolis, Moridilla, Tergiposacca, and Costasiella.
For vetigastropods, seven of the 19 collected species (37%) are new records for the Maldives, resulting in a list of 60 vetigastropod species now known from the archipelago (Table 1, Figure 8). One additional species of Trochus could not be confidently identified to species (Figure 8j), and possibly represents one of the species already recorded in the literature. New records represent 17% of the previously known diversity for the group, and at least two of these species are likely new to science (Emarginella sp. 1 [Figure 8d] and Stomatolina sp. 1 [Figure 8k]). All but two vetigastropod species were successfully barcoded, with most having relatively distant matches in GenBank (Figure 2D; 88.6% average identity to the best match, range 80.9–97.4%).
The gastropod subclass Neritimorpha was not targeted in this study, but one uncommon limpet-like species (Zacalantica tenuisculpta) was collected. It is included here to make this new occurrence for the Maldives available in the scientific literature, together with photos of the live specimen and barcoding data (Table 1, Figure 8o).
Systematics
Class Gastropoda Cuvier, 1795
Subclass Heterobranchia Burmeister, 1837
Order Nudibranchia Cuvier, 1817
Family Aeolidiidae Gray, 1827
Genus Limenandra Haefelfinger & Stamm, 1958
Limenandra evanescenti n. sp. Fernández-Simón & Moles, 2023 (Figure 5a)
ZooBank registration. urn:lsid:zoobank.org:act:48AAD3AC-062C-41AF-98CE-0C238789E0D0
Holotype. MCZ:Mala:393766 (1 spm: 95% ethanol). Magoodhoo, Faafu, Maldives (3°04′45.3” N 72°58′05.0” E), 1 m depth. Collected by snorkeling at night on 5 April 2019 by J. Moles. GenBank (COI: OQ207002). Singleton, 6.5 mm in length.
MCZ link. mczbase.mcz.harvard.edu/guid/MCZ:Mala:393766
Etymology. The species name refers to the vanishing appearance of the dorsal pigmented rings, typical of the species of the genus.
Diagnosis. Body elongate, slender, dirty white; vanished pink circles on head, after first and third ceratal clusters, surrounded by yellow dots; yellow dots also seen in between other ceratal clusters; laterals transparent with white blotches and brown zooxanthellae punctuation, as for oral and propodial tentacles. Rhinophores papillate; tip white; periocular area under rhinophores depigmented. Cerata papillate, cylindrical, white-tipped, directed posteriorly, arranged in 7 rows; innermost longer, up to 1.3 mm in length; outermost slightly curved.
Distribution. Only known from the type locality in the Maldives.
Ecology. Found under coral rubble.
Remarks. The overall morphology and coloration of L. evanescenti n. sp. are similar to the type species L. nodosa Haefelfinger & Stamm, 1958, found in the Mediterranean and Atlantic Ocean, and to L. confusa Carmona, Pola, Gosliner & Cervera, 2014 from the Pacific Ocean [54]. However, the new species presents an opaque white coloration, and the typical pink and yellow dorsal rings appear diffuse and fragmented. Molecular data of all accepted species of Limenandra are available and included in our phylogenetic analysis (Figure S2), where L. evanescenti n. sp. was found to be an independent lineage and its own taxonomic unit according to the species delimitation tests.
Family Eubranchidae Odhner, 1934
Genus Eubranchus Forbes, 1838
Eubranchusputnami n. sp. Fernández-Simón & Moles, 2023 (Figure 5d)
Eubranchus sp. 1, Debelius & Kuiter 2007 [55]: 346.
Eubranchus sp. 26, Gosliner et al. 2018 [23]: 281.
Eubranchus sp. (brown Eubranchus), Ryanskiy & Ivanov 2019 [56]: 87.
ZooBank registration. urn:lsid:zoobank.org:act:3FC8F783-2632-450A-A78B-983261B4F7E7
Material examined.Holotype MCZ:Mala:393748 (1 spm: 95% ethanol). Free-Climbing, Dharanboodhoo, Faafu, Maldives (3°03′53.9” N 72°55′16.5” E), 7 m depth. Collected using scuba on 4 April 2019 by J. Moles. GenBank (COI: OQ206999). Singleton, 7 mm in length.
MCZ link. mczbase.mcz.harvard.edu/guid/MCZ:Mala:393748
Etymology. This species is dedicated to George Putnam Jr. (1926–2019), a longtime supporter of the MCZ and founding donor of the Putnam Expeditionary Grant program that allowed this research.
Diagnosis. Body elongated, dark-brown. Head, rhinophores, dorsum, and laterals dark-brown; with two translucent bands on the upper laterals running from head (just below rhinophores) toward tail; digestive gland beige-whitish in color, seen by transparency. Rhinophores dark-brown, with white punctuation interspersed on the tips. Oral tentacles transparent. Cerata up to 1 mm in length, club-like, lateralized, up to 17 per side; transparent, digestive gland seen through, two crowns of white punctuation at base, tip swollen, milky white with subterminal orange ring.
Distribution. Indian (this study) and the Western Pacific Ocean [23].
Ecology. Found crawling on a plumularid hydroid, where it feeds upon.
Remarks. The morphology of E. putnami n. sp. is extremely characteristic with an elongated dark body and lateralized cerata, thus, resembling the hydroid colony it feeds on. To the best of our knowledge, no other species of Eubranchus has ever been described with this morphology. Somehow similar-looking morphotypes have been reported [23,55,56], and a molecular study of those throughout the distribution is required to further ascertain their status. A recent revision of Eubranchus found the genus divided into two clades [57], one formed by species recently emerged as Amphorina species, a genus containing species from the North Hemisphere. In our phylogenetic analysis, E. putnami n. sp. is almost the only tropical species and does not cluster with any sequenced species (Figure S3).
Family Facelinidae Bergh, 1889
Genus Sakuraeolis Baba, 1965
Sakuraeolis marhe n. sp. Fernández-Simón & Moles, 2023 (Figure 5n)
Facelina sp. 8, Gosliner et al. 2018 [23]: 303; Anderson 2018 [34]: 93.
ZooBank registration. urn:lsid:zoobank.org:act:4F708053-3E0E-4E4C-B8A0-4FA93FCB0B69
Material examined.Holotype MCZ:Mala:393879 (1 spm: 95% ethanol). Sunny Reef, Faafu, Maldives (3°08′34.6” N 73°00′43.4” E), 20 m depth. Collected using scuba on 12 April 2019 by J. Moles. GenBank (COI: OQ207003). Paratypes as holotype. Specimens up to 4 mm in length.
MCZ link. mczbase.mcz.harvard.edu/guid/MCZ:Mala:393879
Etymology. This species is named in apposition after the MaRHE Center and staff, for the logistics and their help assisting in the field.
Diagnosis. Body bright orange, or slightly paler; tail milky white. Upper half of oral tentacles and upper third of rhinophores and cerata milky white, opaque, or slightly translucent. Rhinophores and oral tentacles conical, smooth. Cerata in four horseshoe-shaped clusters, first one in front of pericardium, slightly separated from the rest; four per cluster side, innermost longer, with upper third white; sometimes elongated cnidosacs seen by transparency. Propodial tentacles conical, tentaculiform, directed posteriorly.
Distribution. Only known from the Maldives (this study) and the Philippines [23].
Ecology. The three specimens were found on top of an encrusting bryozoan in symbiosis with hydroids where it feeds.
Remarks.Sakuraeolis marhe n. sp. looks like Facelina sp. 8 [23], but our external morphological examination and molecular data suggest a relationship to Sakuraeolis (Figure S4). Diagnostic characters of the genus are present in our specimens, such as smooth rhinophores and horseshoe-shaped ceratal clusters [58]. Genetically, S. marhe n. sp. clustered with unidentified facelinids and S. arcana Ellis-Diamond, Picton, Tibiriçá & Sigwart, 2021, S. enosimensis (Baba, 1930), and S. japonica (Baba, 1937). These unidentified specimens encompass a ‘Facelina sp. 8’, two Favorinus sp. specimens likely belonging to another genus [59], and two Caloria sp. specimens with the typical orange coloration to its sister species, S. arcana [60]. Therefore, we believe these to be unidentified species belonging to Sakuraeolis, none of them being molecularly identical to S. marhe n. sp. according to the species delimitation tests (Figure S4). Chromatically, the most similar species of the genus is S. arcana, with a bright orange body and opaque white cerata, rhinophores, and oral tentacles. However, S. marhe n. sp. differs from S. arcana by having smooth rhinophores, shorter white coloration on the tip of the body appendages, and lacking a white stripe on the head.
Genus Moridilla Bergh, 1888
Moridilla maldivensis n. sp. Fernández-Simón & Moles, 2023 (Figure 5m)
Moridilla sp., Anderson 2018 [34]: 98.
ZooBank registration. urn:lsid:zoobank.org:act:C1B3DA53-526B-42C6-8E11-59EBCB262542
Holotype. MCZ:Mala:393739 (1 spm: 95% ethanol). Dharanboodhoo, Faafu, Maldives (3°03′30.5” N 72°55′29.6” E), 20 m depth. Collected using scuba on 4 April 2019 by T. J. Cunha. GenBank (COI: OQ207008). Singleton, 12 mm in length.
MCZ link. mczbase.mcz.harvard.edu/guid/MCZ:Mala:393739
Etymology. The species name derives from the type locality, so far, the only known distribution of the new species.
Diagnosis. Body elongated, slender; translucent gray, with lateral white bands on each ceratal cluster and dorsally on tail; tail pointy. Head coloration with a triangular pale orange marking frontally; oral tentacle coloration distally milky white, running laterally, converging behind rhinophores; bright orange band at each side. Rhinophores smooth anteriorly, papillate posteriorly; apically bright orange, stalk transparent. Foot slender, translucent; propodial tentacles triangular, pointy. Cerata arranged in seven clusters, progressively decreasing posteriorly; coloration pale orange with white punctuation, white subterminal tips; innermost longer, curled, upper half milky white.
Distribution. Only known from the type locality in the Maldives.
Ecology. Found under coral rubble, with nocturnal habits [34].
Remarks. Overall, Moridilla species are very similar looking, yet a distinctive head coloration in M. maldivensis n. sp. helps distinguish it from all described species so far [61,62]. Similar coloration is found on M. jobeli Schillo & Wägele, 2019, though this one presents the tip of the oral tentacles in orange (COI similarity up to 83.7%). Moridilla maldivensis n. sp. has also white lateral bands under each ceratal botch as a diagnostic feature. Molecular data of all accepted species of Moridilla plus an undescribed one is available and included in our phylogenetic analysis (Figure S5), where M. maldivensis n. sp. was found to be an independent lineage according to both the phylogeny and the species delimitation tests.
Family Fionidae Gray, 1857
Genus Tergiposacca Cella, Carmona, Ekimova, Chichvarkhin, Schepetov & Gosliner, 2016
Tergiposacca perspicua n. sp. Fernández-Simón & Moles, 2023 (Figure 5q)
Tergiposacca longicerata Cella, Carmona, Ekimova, Chichvarkhin, Schepetov & Gosliner, 2016 [63]: 22, Figure 5C.
ZooBank registration. urn:lsid:zoobank.org:act:59BFDE70-D9E6-4722-BE96-CB1D4CEBC9AA
Holotype. MCZ:Mala:393841 (1 spm: 95% ethanol). Pier, Magoodhoo, Faafu, Maldives (3°04′53.2” N 72°57′55.1” E), 1 m depth. Collected by snorkeling on 11 April 2019 by J. Moles. GenBank (COI: OQ207000). Singleton, 7 mm in length.
MCZ link. mczbase.mcz.harvard.edu/guid/MCZ:Mala:393841
Etymology. The specific epithet, perspicua, the feminine of perspicuus, is the Latin word for translucent because of the overall absence of body coloration.
Diagnosis. Body translucent, white viscera seen by transparency. Rhinophores and oral tentacles conical, smooth, transparent. Jaws white, seen by transparency. Cerata elongated, cylindrical, isodiametric; digestive gland granulose, beige, seen by transparency; subterminal ring transparent, terminal tips white. Propodium rounded.
Distribution. The Maldives (this study), the Philippines [63], Marshall Islands, and New Caledonia [64].
Ecology. Found under a rock.
Remarks. The only known species from the genus, T. longicerata Cella, Carmona, Ekimova, Chichvarkhin, Schepetov & Gosliner, 2016, was described based on several specimens from the Philippines with three different color morphotypes (see Figure 5 in Cella et al. [63]). However, only the specimen CASIZ177605, with orange pigmentation, was sequenced therein. This one showed a genetic divergence with T. perspicua n. sp. of 80%, rendering ours a new species. A burgundy color morphotype of T. longicerata was also found in the Maldives [34]. A broader molecular and systematic reevaluation of the latter and the brownish morphotypes found all over the Western Pacific [23,56] is needed to further ascertain the taxonomic status of all different color morphotypes. Nevertheless, T. perspicua n. sp. differs from the type species in the translucid whitish coloration that inspired its name.
Superorder Sacoglossa von Ihering, 1876
Family Costasiellidae K. B. Clark, 1984
Genus Costasiella Pruvot-Fol, 1951
Costasiella fridae n. sp. Fernández-Simón & Moles, 2023 (Figure 7f)
Costasiella sp. 1, Gosliner et al. 2018 [23]: 412.
Costasiella sp., Ryanskiy & Ivanov 2019 [56]: 130.
ZooBank registration. urn:lsid:zoobank.org:act:22BACF60-8C18-449F-A7AE-DE37C6352414
Examined material.Holotype MCZ:Mala:393874 (1 spm: 95% ethanol). Beyrufushi, Faafu, Maldives (3°06′46.1” N 73°01′15.9” E), 6 m depth. Collected using scuba on 11 April 2019 by J. Moles. GenBank (COI: OQ206988). Paratype as holotype. Specimens, 3 mm in length.
MCZ link. mczbase.mcz.harvard.edu/guid/MCZ:Mala:393874
Etymology. This species is named in honor of the Mexican artist Frida Kahlo for the resemblance of her iconic eyebrows to the distinct black, oval band behind the eyes of C. fridae n. sp.
Diagnosis. Body 3 mm in length; translucent white dorsum; snout milky white, converging into the middle of eyes; distinctive oval, black band behind eyes and rhinophores. Rhinophores cylindrical, bulbous when disturbed; upper two-thirds opaque white. Cerata moss green, innermost whiter; containing white, blue, and yellow iridescent dots, particularly on larger cerata; ceratal tips whitish.
Distribution. Tropical Indo-Pacific, cited in South Africa, the Maldives, Indonesia, Japan, Guam, and Hawaii [65].
Ecology. Two specimens found laying eggs on the green alga Avrainvillea sp.
Remarks. Specimens with similar coloration have been found all over the Indo-Pacific. The distinctive black, oval band behind the eyes is a diagnostic character of C. fridae n. sp., as is the white blotch in the snout area. Similar-looking specimens from Japanese waters have been identified as C. iridophora Ichikawa, 1993. Nevertheless, the overall head coloration of C. fridae n. sp. differs from Ichikawa’s [66] description as it lacks a pigmented area around the eyes and possesses a diagnostic black band. In our phylogeny, C. fridae n. sp. does not cluster with any sequenced species (Figure S6). Eight of the 17 currently accepted species and nine additional undescribed ones were recently sequenced and included in our phylogeny [67,68]. From those, C. fridae n. sp. is externally more similar to Costasiella sp. 2, cf. kuroshimae (Figure 8 in Jensen et al. [67]) and Costasiella sp. 1 (Figure 1E in Christa et al. [68]), although genetically they present great divergence (COI similarity up to 79%).

4. Discussion

Half of our collected heterobranch and vetigastropod species comprise new records for the Maldives (53 out of 104), highlighting how much diversity remains to be discovered in future surveys. This is further evidenced by the fact that the sampling campaign was limited to under two weeks of hand-picking live specimens by two people in a relatively small geographic area (mostly islands on the south of the Faafu Atoll). In an enormous effort to estimate the magnitude of mollusk richness in tropical marine environments, Bouchet et al. [69] encountered high spatial and habitat heterogeneity in New Caledonia, with about a third of species being collected in a single site. Despite the much lower sampling effort in the Maldives, we found that over half of our species were collected in only one site (Figure 2A), similar to a macroinvertebrate survey of the Baa Atoll [14], indicating that further work on the more than one thousand islands of the archipelago is expected to uncover increasing diversity levels. The final checklist (Table 1), which also includes all records we encountered in the literature for the Maldives, sums up to 320 species of the two gastropod subclasses, Heterobranchia (259) and Vetigastropoda (61), with our new records representing an increase of about 25% on the number of species known for the archipelago.
Notably, a high proportion of species (64%) in the checklist has only ever been found by a single source in the literature (Figure 2C, Table 1), which also reveals that several species recorded by previous authors were not found during our fieldwork. There are likely multiple reasons for that. Independent surveys in the Maldives show that a high proportion of taxa are collected in a single site and in low abundance, indicating ecological rarity (Figure 2A,B) [11,12,14]. This relates to the seasonality and habitat preferences of many species, resulting in the spatial heterogeneity found throughout marine environments [69]. Another related factor is the sampling methodology: besides time spent in the field and geographical breadth, most reported species in past mollusk surveys in the Maldives were only found as empty shells (e.g., [11,15]). Here we hand-picked live specimens during snorkeling and scuba diving to photograph live animals and obtain sequence data. More comprehensive sampling strategies, such as dredging, would likely produce a list with more overlap with previous studies (as discussed in Robertson [13]). Finally, habitat loss and climate change could also have had an important role in the turnover of species since past expeditions, such as the major event of coral mortality that heavily affected the Maldives in 1998 [5,70].
Yonow [21] stressed the significance of making new records of rare taxa available in the scientific literature, exemplifying with one sample of a sacoglossan from the Maldives [22], which turned out to be the only record for the entire Indian Ocean when the species was described a year later as having an Indo-West Pacific distribution [71]. Baseline biodiversity data, together with monitoring through time, are key resources for broader ecological and evolutionary studies, including evaluating the impact of environmental change. This is especially relevant in a place like the Maldives, where most islands are less than one meter above sea level and threatened by sea-level rise [4,72], which could hamper future studies in these habitats.
We note that a small part of the incongruence between literature records in our checklist could represent incorrect taxonomic identifications and, therefore, spurious occurrence data. We aimed to be as thorough as possible in the literature search so that our checklist reflects all heterobranchs and vetigastropods that, to our knowledge, have been recorded for the Maldives. However, many of these taxa lack systematic revisions and specialized resources for identification, which can potentially lead to the same species being identified with different names by different studies. Some examples are discussed in the sections below.

4.1. Heterobranchia in the Maldives: How Much Is to Be Learned?

Seven of the 14 known orders of heterobranchs inhabiting the Maldives waters were collected (Table 1). A single representative of the order Acteonimorpha was found and attributed to the species Pupa tessellata for its shell similarity. Regarding the order Pleurobranchida, Berthella martensi was already reported in the Maldives, yet DNA barcodes showed low similarity with other specimens of the same species, indicating that we may be dealing with a species complex (J. Moles unpubl. data). Our specimen of B. martensi likely fits with the original description (type locality: Mauritius [73]); thus, the other sequenced specimens should be reevaluated morphologically. Even though Berthellina citrina was previously recorded (e.g., [34]), our molecular evidence suggests this being B. delicata, which is, in turn, another complex of species to be further evaluated. Three species of the order Aplysiida were collected and barcoded, Dolabella auricularia, Dolabrifera dolabrifera, and Stylocheilus striatus. The latter two are the type species of genera recently found to contain species complexes with a wide distribution in the tropical Indo-Pacific [74,75].
Cephalaspidea is one of the major lineages of marine heterobranchs that reaches its highest diversity in tropical and subtropical waters of the Indo-Pacific [76]. To date, 26 species have been previously reported in the Maldives (Table 1), 10 being our new records. Within Haminoeidae, Phanerophthalmus batangas is reported here for the first time outside the Philippines [3] and in the Indian Ocean. Although P. olivaceus was previously recorded for the Maldives [19], we believe that specimen was likely a misidentified P. minikoiensis, a species also collected by us, given its color, jaws, and radular similarity. A likely third species, P. cf. cylindricus was identified here based on morphological data alone. Aliculastrum debile, Haloa aptei, and the two undescribed species of “mini and long-tail” haminoids in Oskars et al. [77] are also recorded in the region for the first time in this study. Additional new records for the Maldives include Acteocina sp. and Bulla vernicosa. Within the last genus, B. ampulla was already known to inhabit the Maldives [78] (Table 1), and here, B. vernicosa is reported for the region for the first time. Finally, in two cases, barcodes did not work to identify species, i.e., Colpodaspis thompsoni and Philine orca. Although sequences of both species were already available, barcodes were inconclusive in determining their identity (up to 91% of genetic divergence), which may indicate that we are dealing with species complexes that will require additional sampling.
Nudibranchs are one of the most diverse orders of heterobranchs, including Cladobranchia, with more than a thousand species [79]. A total of 35 species were previously reported for the Maldives, now supplemented with the 15 reported here for the first time, including the five new species described. Our barcodes demonstrated the existence of species complexes in some genera, hampering species identification. This is the case of Cratena [80], with 11 recognized species [18] but with many morphotypes to be described [23]. Here, three species of the genus were found, and only Cratena sp. 5 (sensu Gosliner et al. [23]) could be recognized and reported as widespread in the Indo-Pacific. Based on barcoding data, both our Cratena sp. 5 and Cratena sp. A were recovered in distant phylogenetic positions regarding the type species C. peregrina (Gmelin, 1791) and other represented species (Figure S4). Likewise, Eubranchus is a diverse genus with 46 species [18] and several more awaiting formal description [23]. However, the two undescribed species reported here become the first genus records for the Maldives. The only species successfully barcoded is described as E. putnami n. sp. (Eubranchus sp. 26 in Gosliner et al. [23]) based on its unique morphology and molecular identity. In addition, Sakuraeolis marhe n. sp. (Facelina sp. 8 in Gosliner et al. [23]) is described here based on its distinctive body coloration and reported for the first time outside the Philippines. Furthermore, the new species Limenandra evanescenti n. sp. is the first representative of the genus found in the Maldives, with a COI divergence of 83.7% from all other described species to date [54]. Moreover, Tergiposacca perspicua n. sp. is described here as the second recognized species of the genus. This species was thought to be a color morphotype of T. longicerata [63], meaning additional molecular data could still reveal new species within the different color variations. Finally, the new species Moridilla maldivensis n. sp. becomes the second species of the genus reported for the Maldives, after M. brockii Bergh, 1888 [34]. All the previous species of the genus have been sequenced [61,62], and ours was recovered as genetically distinct (it was also different morphologically). In addition, we provide a glimpse of other possible cryptic species, such as Godiva sp. 1, reported for the Maldives for the first time, and Pteraeolidia aff. semperi, genetically dissimilar to any other species known and sequenced [81]. In addition, Phestilla lugubris, a Porites coral-feeding species, became the second reported species of the genus for the Maldives after P. melanobrachia. Lastly, non-aeolid cladobranchs such as Doto and Embletonia were first reported for the region, but only E. gracilis could be identified at the species level.
The barcodes of Doridina were better matching with existing species. Eleven of them were identified at the species level through BLAST, while 10 had no matches on GenBank. The family Actinocyclidae is reported for the first time in the Maldives, with the species Hallaxa fuscescens and H. indecora. In addition, the first records for the region were found for the species Verconia simplex and for the genus Goniodoridella with a likely new species to be described (Paz-Sedano pers. comm.). Two species of the family Discodorididae were also reported and barcoded here for the first time, Thordisa cf. oliva and Rostanga sp. 2 (sensu Gosliner et al. [23]). Regarding Chromodorididae, we collected five species of Goniobranchus. G. albonares was first reported and, together with G. setoensis, was barcoded for the first time. In addition, representatives of two species of Gymnodoris were found, a genus where still dozens of species await formal description [82], including our undescribed species. Despite being very abundant in Indo-Pacific reefs, Phyllidiidae taxonomy remains problematic because of its conservative morphology and color patterns, with several cases of cryptic speciation [83]. Here we found nine species belonging to Phyllidia, Phyllidiella, and Phyllidiopsis, with one unidentified species per genus. We provide molecular data for the endemic Phyllidia koehleri and evidence that Phyllidiella rosans, with different morphotypes across the Pacific [55], may also represent a species complex. Overall, despite their conspicuous abundance, several geographical and chromatic morphotypes of Phyllidiidae need to be sequenced to better comprehend their diversity [21].
Regarding Sacoglossa, the most species-rich genus Elysia (Plakobranchidae) currently contains more than 100 recognized species [18]. Thus, it is assumed that many of the species are poorly known or have complex taxonomic histories [84]. Here, five species were reported, and four of them were barcoded, although only two could be attributed to the non-described species Elysia sp. 6 (sensu Gosliner et al. [23]) and E. cf. marginata sp. 2 (sensu Krug et al. [84]), the latter recently unraveled from the species complex belonging to E. ornata [85]. Elysia sp. 44 (sensu Gosliner et al. [23]) and E. pusilla were identified by external morphology and both seem to have been sequenced here for the first time. The latter is almost 92% identical to E. pusilla Guam_19 from Vendetti et al. [86]; thus, we seem to have found here a new case of cryptic speciation of this sacoglossan species. Still, within Plakobranchidae, three species of Thuridilla were attributed to T. livida, T. vataae, and Thuridilla sp. 6, an undescribed species unraveled from the species complex of T. gracilis by Martín-Hervás et al. [87]. Polybranchia jensenae and Cyerce elegans were recorded for the first time in the Maldives, as well as the new species Costasiella fridae n. sp. and Stiliger sp. 1 (description in progress).

4.2. The Underestimated Diversity of Vetigastropoda

Trochidae, Fissurellidae, and Turbinidae, some of the most diverse families of vetigastropods in general, were accordingly the most diverse in our collections, as well as in the overall checklist compiled from the literature for the Maldives. At least two of the species collected here are likely new to science, the fissurellid Emarginella sp. 1 (Figure 8d) and the trochid Stomatolina sp. 1 (Figure 8k), both groups whose known diversity is still largely underestimated [88,89].
While COI barcoding data are often used to identify species of various animals through high-identity BLAST matches in GenBank, our results reveal how vetigastropods are underrepresented in such databases. For example, even the widely distributed and large-bodied Turbo argyrostomus was only represented by one specimen with COI data in GenBank so far. Interestingly, this was one of the species with the highest match, with our Maldivian specimens sharing 97% identity to the single public sequence from Japan. Another of the closest matches was for the turbinid Astralium rhodostomum, with 95% identity to public data from Thailand. For this species, sequence identity lowered to 88% relative to GenBank specimens identified as A. rhodostomum from the Philippines and Papua New Guinea. Matches with such low percent identity were relatively frequent for our vetigastropod species (Figure 2D). This could either indicate that mitochondrial divergence within species might be larger than expected for these groups, or that many of these lineages represent cryptic species that need further molecular investigation from a broader geographic range.
Another interesting case is that of the trochid Calliotrochus marmoreus (Figure 8g), for which our specimens shared a high identity of about 97% with specimens from the Red Sea (listed as Gastropoda sp. in GenBank but identified as C. marmoreus by us from a photo shared by the authors [90]). Sequence identity with specimens from the Philippines and Hawaii was 84–86%, suggesting that fauna from the Maldives might be more similar to the fauna of the Red Sea than to that of the Pacific. Morphologically recognized as the same species across oceans [31], genomic data could help clarify possible cryptic species and biogeographical patterns of divergence.
Our checklist of vetigastropods from the Maldives also alerts us to possible erroneous taxonomic identifications and, therefore, occurrences. For example, Clanculus denticulatus was only listed in the OBIS database, and it is morphologically very similar to C. samoensis, recorded by several sources. While we can assign our Maldivian specimens to C. samoensis (Figure 8f) based on systematic work for the genus [32], online resources seem to be wrongly attributing photos of C. samoensis to C. denticulatus, helping to perpetuate erroneous identifications. Similarly, C. pharaonius and C. puniceus are another pair of morphologically similar species recorded for the Maldives by a single author each [12,38] that could represent specimens of just one of these species.
Another example of possible misidentification is Trochus flammulatus, only recorded in the Maldives by one literature source [39], and otherwise only known from islands in the western Indian Ocean such as Aldabra, Mauritius, and Réunion [18]. Kohn [39] explicitly stated that his mollusk fauna was identified based on the collection of one natural history museum and that no further attempt had been made to verify the names used. Given that Trochus is a diverse genus often hard to identify at the species level, and that several other morphologically similar species have been recorded for the Maldives multiple times, T. flammulatus might represent a misidentification. For our specimens of Trochus spp., several of which are juveniles (Figure 8h–j), even COI barcoding helped little in confirming species identity: while sequences allowed to sort samples to different species (Figure S1), the best BLAST matches were in the range of 86–88% to various Trochus species represented in GenBank.
The cases discussed above exemplify and reflect the paucity of systematic revisions for diverse vetigastropod groups, the little photographic evidence of live animals, and the lack of synthetic literature for their identification. Some additional groups that we note as in need of revisionary work include the trochid subfamily Stomatellinae and several genera of Fissurellidae, including Emarginella spp. All our specimens were photographed alive, almost all were barcoded, and we hope these will be useful resources for future studies in the group.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/d15020219/s1, Table S1. Voucher information and GenBank accession codes for collected specimens. Table S2. BLAST results from GenBank: the top 100 hits for each queried specimen. Table S3. BLAST results from GenBank: the best hit for each queried specimen. Figures S1–S6. COI gene tree for all barcoded specimens, and phylogenetic trees and species delimitation tests for the six newly described species [61,67,91,92,93].

Author Contributions

Conceptualization: J.M.; Fieldwork: J.M. and T.J.C.; Photography: T.J.C.; Plates: J.F.-S.; Barcoding: M.P., J.M. and T.J.C.; Species descriptions: J.F.-S. and J.M.; Checklist: T.J.C., J.F.-S. and J.M.; Analyses and interpretation: T.J.C., J.F.-S. and J.M.; Writing—Original Draft: T.J.C., J.F.-S. and J.M.; Writing—Review and Editing: all authors; Supervision: J.M. and T.J.C.; Funding Acquisition: J.M. and G.G. All authors have read and agreed to the published version of the manuscript.

Funding

Fieldwork was funded by a Putnam Expedition Grant from the Museum of Comparative Zoology to JM. Lab work was supported by internal funds from the Faculty of Arts and Sciences, Harvard University, to GG. Additional lab work was conducted in the Pritzker Laboratory at the Field Museum. MP was supported by NSF REU Award 1,757,780 and Harvard University, GSAS Office of Diversity and Minority Affairs. TJC was supported by a Faculty for the Future Fellowship from the Schlumberger Foundation, and a Field Museum Women’s Board Postdoctoral Fellowship. JM postdoctoral fellowships were supported by the Ramón Areces (Spain) and the Alexander von Humboldt (Germany) Foundations. JFS contract was supported by the Spanish Government through the HETGEN1000 project (PID2021-127037NA-I00/MCIN/AEI/10.13039/501100011033/y por FEDER una manera de hacer Europa).

Data Availability Statement

Voucher information is fully available in MCZbase (https://mczbase.mcz.harvard.edu) and summarized in Table S1. COI sequences can be retrieved from GenBank (accession OQ206908–OQ207015).

Acknowledgments

We are indebted to the MaRHE Center staff for their help while collecting in the Maldives and for providing some photographs of live specimens. We thank David Herbert, Yasunori Kano, and Daniel Geiger for discussions that helped in identifying some specimens. We appreciate Jennifer Trimble’s assistance with specimens and databasing the material deposited in the MCZ, and Paul Callomon’s help in getting access to unpublished literature deposited in the Academy of Natural Sciences of Drexel University. We thank the reviewers who provided comments on this manuscript.

Conflicts of Interest

The authors have no conflict of interest to declare.

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Figure 1. Maldivian Archipelago (left), highlighting the capital Malé (circle) and the Faafu Atoll (square), where most collecting sites are located (right). Scuba diving sites are labeled according to names used by staff at the MaRHE Center, based at Magoodhoo Island.
Figure 1. Maldivian Archipelago (left), highlighting the capital Malé (circle) and the Faafu Atoll (square), where most collecting sites are located (right). Scuba diving sites are labeled according to names used by staff at the MaRHE Center, based at Magoodhoo Island.
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Figure 2. Distribution of species of Heterobranchia (purple) and Vetigastropoda (yellow) by (A) the number of sites where they were collected, (B) the number of specimens, and (C) the number of literature sources where the species is recorded. (D) Percent identity of the best BLAST hit for all barcoded specimens.
Figure 2. Distribution of species of Heterobranchia (purple) and Vetigastropoda (yellow) by (A) the number of sites where they were collected, (B) the number of specimens, and (C) the number of literature sources where the species is recorded. (D) Percent identity of the best BLAST hit for all barcoded specimens.
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Figure 3. Acteonoidea: (a) Pupa tessellata (MCZ:Mala:393822), dorsal and ventral view; Pleurobranchida: (b) Berthellina delicata (MCZ:Mala:393775); (c) Berthella martensi (MCZ:Mala:393762); Aplysiida: (d) Dolabella auricularia (MCZ:Mala:393823); (e) Dolabrifera dolabrifera (MCZ:Mala:393776), two color morphotypes; (f) Stylocheilus striatus (MCZ:Mala:393764). Photos by T. J. Cunha.
Figure 3. Acteonoidea: (a) Pupa tessellata (MCZ:Mala:393822), dorsal and ventral view; Pleurobranchida: (b) Berthellina delicata (MCZ:Mala:393775); (c) Berthella martensi (MCZ:Mala:393762); Aplysiida: (d) Dolabella auricularia (MCZ:Mala:393823); (e) Dolabrifera dolabrifera (MCZ:Mala:393776), two color morphotypes; (f) Stylocheilus striatus (MCZ:Mala:393764). Photos by T. J. Cunha.
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Figure 4. Cephalaspidea: (a) Acteocina sp. (MCZ:Mala:393847), dorsal and ventral view; (b) Bulla vernicosa (MCZ:Mala:393799); (c) Colpodaspis thompsoni (MCZ:Mala:393765); (d) Haloa aptei (MCZ:Mala:393843); (e) Lamprohaminoea cymbalum (MCZ:Mala:393734); (f) ‘Long tail haminoid’ (MCZ:Mala:393732); (g) ‘Mini haminoid’ (MCZ:Mala:393728); (h) Phanerophthalmus batangas (MCZ:Mala:393707); (i) Phanerophthalmus cf. cylindricus (MCZ:Mala:393777); (j) Phanerophthalmus minikoiensis (MCZ:Mala:393706); (k) Vellicolla muscaria (MCZ:Mala:393871); (l) Aliculastrum debile (MCZ:Mala:393820); (m) Philine orca (MCZ:Mala:393750); (n) Chelidonura varians. Photos by T. J. Cunha; image of (n) courtesy of Davide Seveso.
Figure 4. Cephalaspidea: (a) Acteocina sp. (MCZ:Mala:393847), dorsal and ventral view; (b) Bulla vernicosa (MCZ:Mala:393799); (c) Colpodaspis thompsoni (MCZ:Mala:393765); (d) Haloa aptei (MCZ:Mala:393843); (e) Lamprohaminoea cymbalum (MCZ:Mala:393734); (f) ‘Long tail haminoid’ (MCZ:Mala:393732); (g) ‘Mini haminoid’ (MCZ:Mala:393728); (h) Phanerophthalmus batangas (MCZ:Mala:393707); (i) Phanerophthalmus cf. cylindricus (MCZ:Mala:393777); (j) Phanerophthalmus minikoiensis (MCZ:Mala:393706); (k) Vellicolla muscaria (MCZ:Mala:393871); (l) Aliculastrum debile (MCZ:Mala:393820); (m) Philine orca (MCZ:Mala:393750); (n) Chelidonura varians. Photos by T. J. Cunha; image of (n) courtesy of Davide Seveso.
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Figure 5. Nudibranchia, Cladobranchia: (a) Limenandra evanescenti n. sp. (MCZ:Mala:393766); (b) Doto sp. (MCZ:Mala:393816); (c) Embletonia gracilis (MCZ:Mala:393844); (d) Eubranchus putnami n. sp. (MCZ:Mala:393748); (e) Eubranchus sp. (MCZ:Mala:393798); (f) Herviella albida (MCZ:Mala:393849); (g) Caloria indica (MCZ:Mala:393881); (h) Cratena sp. A (MCZ:Mala:393850); (i) Cratena sp. 5 (MCZ:Mala:393846); (j) Cratena sp. B (MCZ:Mala:393872); (k) Favorinus mirabilis (MCZ:Mala:393795); (l) Favorinus japonicus (MCZ:Mala:393840); (m) Moridilla maldivensis n. sp. (MCZ:Mala:393739); (n) Sakuraeolis marhe n. sp. (MCZ:Mala:393879); (o) Noumeaella sp. (MCZ:Mala:393817); (p) Pteraeolidia aff. semperi (MCZ:Mala:393738); (q) Tergiposacca perspicua n. sp. (MCZ:Mala:393841), ventral view; (r) Godiva sp. (MCZ:Mala:393845); (s) Samla riwo (MCZ:Mala:393744); (t) Samla bicolor (MCZ:Mala:393873); (u) Phestilla lugubris (MCZ:Mala:393735). Photos by T. J. Cunha.
Figure 5. Nudibranchia, Cladobranchia: (a) Limenandra evanescenti n. sp. (MCZ:Mala:393766); (b) Doto sp. (MCZ:Mala:393816); (c) Embletonia gracilis (MCZ:Mala:393844); (d) Eubranchus putnami n. sp. (MCZ:Mala:393748); (e) Eubranchus sp. (MCZ:Mala:393798); (f) Herviella albida (MCZ:Mala:393849); (g) Caloria indica (MCZ:Mala:393881); (h) Cratena sp. A (MCZ:Mala:393850); (i) Cratena sp. 5 (MCZ:Mala:393846); (j) Cratena sp. B (MCZ:Mala:393872); (k) Favorinus mirabilis (MCZ:Mala:393795); (l) Favorinus japonicus (MCZ:Mala:393840); (m) Moridilla maldivensis n. sp. (MCZ:Mala:393739); (n) Sakuraeolis marhe n. sp. (MCZ:Mala:393879); (o) Noumeaella sp. (MCZ:Mala:393817); (p) Pteraeolidia aff. semperi (MCZ:Mala:393738); (q) Tergiposacca perspicua n. sp. (MCZ:Mala:393841), ventral view; (r) Godiva sp. (MCZ:Mala:393845); (s) Samla riwo (MCZ:Mala:393744); (t) Samla bicolor (MCZ:Mala:393873); (u) Phestilla lugubris (MCZ:Mala:393735). Photos by T. J. Cunha.
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Figure 6. Nudibranchia, Doridina: (a) Hallaxa indecora (MCZ:Mala:393835); (b) Hallaxa fuscescens (MCZ:Mala:393778); (c) Glossodoris acosti (MCZ:Mala:393870); (d) Goniobranchus glenei; (e) Goniobranchus setoensis (MCZ:Mala:393833); (f) Goniobranchus conchyliatus (MCZ:Mala:393705); (g) Goniobranchus fidelis (MCZ:Mala:393721); (h) Goniobranchus albonares (MCZ:Mala:393832); (i) Verconia simplex (MCZ:Mala:393831); (j) Dendrodoris nigra (MCZ:Mala:393710); (k) Rostanga sp. 2 (MCZ:Mala:393742); (l) Mexichromis similaris (MCZ:Mala:393877); (m) Hypselodoris maculosa (MCZ:Mala:393783); (n) Hypselodoris nigrostriata; (o) Thordisa cf. oliva (MCZ:Mala:393780); (p) Goniodoridella sp. (MCZ:Mala:393815); (q) Roboastra gracilis (MCZ:Mala:393829); (r) Gymnodoris ceylonica; (s) Gymnodoris sp. (MCZ:Mala:393743); (t) Phyllidia sp. (MCZ:Mala:393878); (u) Phyllidiella sp. (MCZ:Mala:393785); (v) Phyllidia koehleri (MCZ:Mala:393746); (w) Phyllidia rosans (MCZ:Mala:393796); (x) Phyllidia alyta (MCZ:Mala:393788); (y) Phyllidia picta (MCZ:Mala:393774); (z) Phyllidia varicosa (MCZ:Mala:393757); (aa) Phyllidiella sp. 1 (MCZ:Mala:393736); (ab) Phyllidiella zeylanica; (ac) Phyllidiella striata (MCZ:Mala:393808); (ad) Phyllidiopsis sp. (MCZ:Mala:393747); (ae) Phyllidiopsis xishaensis (MCZ:Mala:393740). Photos by T. J. Cunha; images of (d,r,ab) courtesy of Davide Seveso; images of (j,m,n) courtesy of Davide Maggioni.
Figure 6. Nudibranchia, Doridina: (a) Hallaxa indecora (MCZ:Mala:393835); (b) Hallaxa fuscescens (MCZ:Mala:393778); (c) Glossodoris acosti (MCZ:Mala:393870); (d) Goniobranchus glenei; (e) Goniobranchus setoensis (MCZ:Mala:393833); (f) Goniobranchus conchyliatus (MCZ:Mala:393705); (g) Goniobranchus fidelis (MCZ:Mala:393721); (h) Goniobranchus albonares (MCZ:Mala:393832); (i) Verconia simplex (MCZ:Mala:393831); (j) Dendrodoris nigra (MCZ:Mala:393710); (k) Rostanga sp. 2 (MCZ:Mala:393742); (l) Mexichromis similaris (MCZ:Mala:393877); (m) Hypselodoris maculosa (MCZ:Mala:393783); (n) Hypselodoris nigrostriata; (o) Thordisa cf. oliva (MCZ:Mala:393780); (p) Goniodoridella sp. (MCZ:Mala:393815); (q) Roboastra gracilis (MCZ:Mala:393829); (r) Gymnodoris ceylonica; (s) Gymnodoris sp. (MCZ:Mala:393743); (t) Phyllidia sp. (MCZ:Mala:393878); (u) Phyllidiella sp. (MCZ:Mala:393785); (v) Phyllidia koehleri (MCZ:Mala:393746); (w) Phyllidia rosans (MCZ:Mala:393796); (x) Phyllidia alyta (MCZ:Mala:393788); (y) Phyllidia picta (MCZ:Mala:393774); (z) Phyllidia varicosa (MCZ:Mala:393757); (aa) Phyllidiella sp. 1 (MCZ:Mala:393736); (ab) Phyllidiella zeylanica; (ac) Phyllidiella striata (MCZ:Mala:393808); (ad) Phyllidiopsis sp. (MCZ:Mala:393747); (ae) Phyllidiopsis xishaensis (MCZ:Mala:393740). Photos by T. J. Cunha; images of (d,r,ab) courtesy of Davide Seveso; images of (j,m,n) courtesy of Davide Maggioni.
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Figure 7. Sacoglossa: (a) Cyerce elegans (MCZ:Mala:393754); (b) Elysia pusilla (MCZ:Mala:393737); (c) Elysia cf. marginata (MCZ:Mala:393708); (d) Elysia sp. 11 (MCZ:Mala:393722); (e) Elysia sp. 44 (MCZ:Mala:393711); (f) Costasiella fridae n. sp. (MCZ:Mala:393874); (g) Stiliger sp. 1 (MCZ:Mala:393830); (h) Thuridilla sp. 6 (T. gracilis species-complex) (MCZ:Mala:393741); (i) Thuridilla vataae (MCZ:Mala:393868); (j) Thuridilla livida (MCZ:Mala:393767); (k) Polybranchia jensenae (MCZ:Mala:393800). Photos by T. J. Cunha.
Figure 7. Sacoglossa: (a) Cyerce elegans (MCZ:Mala:393754); (b) Elysia pusilla (MCZ:Mala:393737); (c) Elysia cf. marginata (MCZ:Mala:393708); (d) Elysia sp. 11 (MCZ:Mala:393722); (e) Elysia sp. 44 (MCZ:Mala:393711); (f) Costasiella fridae n. sp. (MCZ:Mala:393874); (g) Stiliger sp. 1 (MCZ:Mala:393830); (h) Thuridilla sp. 6 (T. gracilis species-complex) (MCZ:Mala:393741); (i) Thuridilla vataae (MCZ:Mala:393868); (j) Thuridilla livida (MCZ:Mala:393767); (k) Polybranchia jensenae (MCZ:Mala:393800). Photos by T. J. Cunha.
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Figure 8. Vetigastropoda: (a) Hemimarginula cf. biangulata (dorsal: MCZ:Mala:393769, ventral: MCZ:Mala:393856); (b) Diodora singaporensis (MCZ:Mala:393718); (c) Emarginella nigromaculata (MCZ:Mala:393851); (d) Emarginella sp. 1 (live: MCZ:Mala:393792, shell: MCZ:Mala:393791); (e) Haliotis ovina (MCZ:Mala:393717); (f) Clanculus samoensis (MCZ:Mala:393713); (g) Calliotrochus marmoreus, with color variation (left: MCZ:Mala:393753, right: MCZ:Mala:393857); (h) juvenile of Trochus maculatus (MCZ:Mala:393804); (i) juvenile of Trochus cf. stellatus (MCZ:Mala:393864); (j) Trochus sp. 1 (adult: MCZ:Mala:393790, juvenile: MCZ:Mala:393863); (k) Stomatolina sp. 1 (MCZ:Mala:393763); (l) Stomatolina rubra (MCZ:Mala:393860); (m) juvenile of Turbo petholatus (MCZ:Mala:393786); (n) Stomatella varia, with color variation (top-left: MCZ:Mala:393752, top-right: MCZ:Mala:393811, bottom-left: MCZ:Mala:393797, bottom-right: MCZ:Mala:393859). Neritimorpha: (o) Zacalantica tenuisculpta (MCZ:Mala:393858). Photos by T. J. Cunha.
Figure 8. Vetigastropoda: (a) Hemimarginula cf. biangulata (dorsal: MCZ:Mala:393769, ventral: MCZ:Mala:393856); (b) Diodora singaporensis (MCZ:Mala:393718); (c) Emarginella nigromaculata (MCZ:Mala:393851); (d) Emarginella sp. 1 (live: MCZ:Mala:393792, shell: MCZ:Mala:393791); (e) Haliotis ovina (MCZ:Mala:393717); (f) Clanculus samoensis (MCZ:Mala:393713); (g) Calliotrochus marmoreus, with color variation (left: MCZ:Mala:393753, right: MCZ:Mala:393857); (h) juvenile of Trochus maculatus (MCZ:Mala:393804); (i) juvenile of Trochus cf. stellatus (MCZ:Mala:393864); (j) Trochus sp. 1 (adult: MCZ:Mala:393790, juvenile: MCZ:Mala:393863); (k) Stomatolina sp. 1 (MCZ:Mala:393763); (l) Stomatolina rubra (MCZ:Mala:393860); (m) juvenile of Turbo petholatus (MCZ:Mala:393786); (n) Stomatella varia, with color variation (top-left: MCZ:Mala:393752, top-right: MCZ:Mala:393811, bottom-left: MCZ:Mala:393797, bottom-right: MCZ:Mala:393859). Neritimorpha: (o) Zacalantica tenuisculpta (MCZ:Mala:393858). Photos by T. J. Cunha.
Diversity 15 00219 g008
Table
Table 1. Checklist of heterobranch and vetigastropod species found in the Maldives, including new species and undetermined species (sensu Gosliner et al. [23] for heterobranchs). Species collected in this study are highlighted in bold, figure citations are included. Species names recorded from the literature were updated according to WoRMS [18] unless explicitly discussed in the source reference. From the OBIS database [33], only records with ‘preserved specimens’ were considered.
Table 1. Checklist of heterobranch and vetigastropod species found in the Maldives, including new species and undetermined species (sensu Gosliner et al. [23] for heterobranchs). Species collected in this study are highlighted in bold, figure citations are included. Species names recorded from the literature were updated according to WoRMS [18] unless explicitly discussed in the source reference. From the OBIS database [33], only records with ‘preserved specimens’ were considered.
FamilySpeciesAuthorityFigureReference
HETEROBRANCHIA
ACOCHLIDIIMORPHA
ParhedylidaeMicrohedyle gerlachiEr. Marcus & Ev. Marcus, 1960 [19]
ACTEONIMORPHA
ActeonidaeJaponacteon suturalis(A. Adams, 1855) [13]
ActeonidaePupa affinis(A. Adams, 1855) [13]
ActeonidaePupa alveola(Souverbie, 1863) [38]
ActeonidaePupa nitidula(Lamarck, 1816) [12,40]
ActeonidaePupa solidula(Linnaeus, 1758) [12,40]
ActeonidaePupa sulcata(Gmelin, 1791) [38]
ActeonidaePupa tessellata(Reeve, 1842)3a[40], This study
AplustridaeAplustrum amplustre(Linnaeus, 1758) [13,38]
APLYSIIDA
AplysiidaeAplysia cf. nigrocinctaMartens, 1880 [21,22,34]
AplysiidaeAplysia parvulaGuilding in Mörch, 1863 [21]
AplysiidaeDolabella auricularia(Lightfoot, 1786)3d[13,19,21,22,34], This study
AplysiidaeDolabrifera dolabrifera(Rang, 1828)3e[21,34], This study
AplysiidaeStylocheilus longicauda(Quoy & Gaimard, 1825) [21]
AplysiidaeStylocheilus striatus(Quoy & Gaimard, 1832)3fThis study
ARCHITECTONICOIDEA
ArchitectonicidaeArchitectonica modesta(Philippi, 1849) [40]
ArchitectonicidaeHeliacus infundibuliformis(Gmelin, 1791) [33]
ArchitectonicidaeHeliacus trochoides(Deshayes, 1830) [33]
ArchitectonicidaePsilaxis radiatus(Röding, 1798) [9,12,38,40]
CEPHALASPIDEA
AglajidaeBiuve fulvipunctata(Baba, 1938) [34]
AglajidaeChelidonura castaneaYonow, 1994 [22]
AglajidaeChelidonura electraRudman, 1970 [21,34]
AglajidaeChelidonura hirundinina(Quoy & Gaimard, 1833) [21,34]
AglajidaeChelidonura punctataEliot, 1903 [21,33]
AglajidaeChelidonura sp. [34]
AglajidaeChelidonura variansEliot, 19034n[21,22,33], This study
AglajidaeMariaglaja sandrana(Rudman, 1973) [21,22,34]
AglajidaeMariaglaja tsurugensis(Baba & Abe, 1959) [33]
AglajidaeNakamigawaia spiralisKuroda & Habe, 1961 [34]
AglajidaeOdontoglaja guamensisRudman, 1978 [34]
AglajidaePhilinopsis speciosaPease, 1860 [22,33,34]
AglajidaeTubulophilinopsis gardineri(Eliot, 1903) [34]
AglajidaeTubulophilinopsis pilsbryi [19]
BullidaeBulla ampullaLinnaeus, 1758 [9,12,13,15,38]
BullidaeBulla vernicosaGould, 18594bThis study
ColpodaspiddidaeColpodaspis thompsoniG. H. Brown, 19794c[34], This study
GastropteridaeSagaminopteron psychedelicumCarlson & Hoff, 1974 [34]
Haminoeidae“Atys” xarifae (cf. Weinkauffia)Er. Marcus & Ev. Marcus, 1960 [19]
HaminoeidaeAliculastrum cylindricum(Helbling, 1779) [40]
HaminoeidaeAliculatrum debile(Pease, 1860)4lThis study
HaminoeidaeAtys naucum(Linnaeus, 1758) [40]
HaminoeidaeAtys sp. 1 [11]
HaminoeidaeAtys sp. 2 [11]
HaminoeidaeHaloa aptei(Bharate, Oskars, Narayana, Ravinesh, Biju Kumar & Malaquias, 2018)4dThis study
HaminoeidaeLamprohaminoea cymbalum(Quoy & Gaimard, 1833)4e[21], This study
HaminoeidaeLong tail haminoid 4fThis study
HaminoeidaeMini haminoid 4gThis study
HaminoeidaePhanerophthalmus batangasAustin, Gosliner & Malaquias, 20184hThis study
HaminoeidaePhanerophthalmus cf. cylindricus(Pease, 1861)4iThis study
HaminoeidaePhanerophthalmus cf. olivaceus [19]
HaminoeidaePhanerophthalmus minikoiensis(E. A. Smith, 1903)4jThis study
HaminoeidaeVellicolla cf. muscaria(Gould, 1859)4kThis study
PhilinidaePhiline orcaGosliner, 19884m[19], This study
TornatinidaeActeocina sp. 4aThis study
NUDIBRANCHIA
ActinocyclidaeHallaxa fuscescens(Pease, 1871)6bThis study
ActinocyclidaeHallaxa indecora(Bergh, 1905)6aThis study
AegiridaeAegires sp. [34]
AegiridaeNotodoris citrinaBergh, 1875 [34]
AegiridaeNotodoris gardineriEliot, 1903 [10,21,22,33,34]
AeolidiidaeBaeolidia dela(Er. Marcus & Ev. Marcus, 1960)[19]
AeolidiidaeBaeolidia variabilisCarmona, Pola, Gosliner & Cervera, 2014[34]
AeolidiidaeLimenandra evanescenti n. sp.Fernández-Simón & Moles, 20235aThis study
ArminidaeDermatobranchus striatusvan Hasselt, 1824 [10,33]
ArminidaePleurophyllidia gracilisBergh, 1874 [10]
BornellidaeBornella anguillaS. Johnson, 1984 [34]
ChromodorididaeCeratosoma gracillimumSemper in Bergh, 1876 [10,34]
ChromodorididaeCeratosoma trilobatum(J. E. Gray, 1827) [10,33,34]
ChromodorididaeChromodoris elisabethinaBergh, 1877 [10,19,34]
ChromodorididaeChromodoris lochiRudman, 1982 [21,22,34]
ChromodorididaeChromodoris pustulansBergh, 1877 [10]
ChromodorididaeDoriprismatica atromarginata(Cuvier, 1804) [19]
ChromodorididaeGlossodoris acostiMatsuda & Gosliner, 20186c[21,22,33,34], This study
ChromodorididaeGlossodoris hikuerensis(Pruvot-Fol, 1954) [22,34]
ChromodorididaeGlossodoris pallida(Rüppell & Leuckart, 1830) [21,34]
ChromodorididaeGoniobranchus albonares(Rudman, 1990)6hThis study
ChromodorididaeGoniobranchus cavae(Eliot, 1904) [34]
ChromodorididaeGoniobranchus coi(Risbec, 1956) [33]
ChromodorididaeGoniobranchus conchyliatus(Yonow, 1984)6f[34], This study
ChromodorididaeGoniobranchus decorus(Pease, 1860) [21]
ChromodorididaeGoniobranchus fidelis(Kelaart, 1858)6g[22,33,34], This study
ChromodorididaeGoniobranchus geminusRudman, 1987 [33,34]
ChromodorididaeGoniobranchus geometricus(Risbec, 1928) [21,22,33,34]
ChromodorididaeGoniobranchus gleniei(Kelaart, 1858)6d[21,22,33,34], This study
ChromodorididaeGoniobranchus setoensis(Baba, 1938)6e[34], This study
ChromodorididaeGoniobranchus tritos(Yonow, 1994) [22,34]
ChromodorididaeHypselodoris bullockii(Collingwood, 1881) [33]
ChromodorididaeHypselodoris emmaRudman, 1977 [22,33,34]
ChromodorididaeHypselodoris infucata(Rüppell & Leuckart, 1830) [33]
ChromodorididaeHypselodoris krakatoaGosliner & Johnson, 1999 [34]
ChromodorididaeHypselodoris maculosa(Pease, 1871)6m[21,33,34], This study
ChromodorididaeHypselodoris maridadilusRudman, 1977 [34]
ChromodorididaeHypselodoris nigrostriata(Eliot, 1904)6nThis study
ChromodorididaeHypselodoris rosans(Bergh, 1889) [10]
ChromodorididaeHypselodoris rudmaniGosliner & Johnson, 1999 [34]
ChromodorididaeHypselodoris sp. 16 [34]
ChromodorididaeHypselodoris whitei(Adams & Reeve, 1850) [22,33,34]
ChromodorididaeMexichromis pusilla(Bergh, 1874) [22]
ChromodorididaeMexichromis similaris(Rudman, 1986)6l[34], This study
ChromodorididaeMiamira magnifica(Eliot, 1910) [22,33,34]
ChromodorididaeMiamira miamirana(Bergh, 1875) [21]
ChromodorididaeMiamira sinuata(van Hasselt, 1824) [34]
ChromodorididaeThorunna sp. [19]
ChromodorididaeVerconia simplex(Pease, 1871)6iThis study
ChromodorididaeVerconia varians(Pease, 1871) [22,33]
DendrodorididaeDendrodoris nigra(Stimpson, 1855)6j[10,21,33,34], This study
DiscodorididaeAsteronotus cespitosus(van Hasselt, 1824) [34]
DiscodorididaeAtagema intecta(Kelaart, 1859) [10]
DiscodorididaeDictyodoris maculataEliot, 1903 [10,33]
DiscodorididaeDiscodoris boholiensisBergh, 1877 [10,33,34]
DiscodorididaeDiscodoris concinna(Alder & Hancock, 1864) [10]
DiscodorididaeDiscodoris pardalis(Alder & Hancock, 1864) [10]
DiscodorididaeHalgerda iotaYonow, 1994 [22]
DiscodorididaeHalgerda tessellata(Bergh, 1880) [21,34]
DiscodorididaeJorunna funebris(Kelaart, 1858) [34]
DiscodorididaeJorunna rubescens(Bergh, 1876) [34]
DiscodorididaePeltodoris murrea(Abraham, 1877) [34]
DiscodorididaePlatydoris cruenta(Quoy & Gaimard, 1832) [33]
DiscodorididaePlatydoris scabra(Cuvier, 1804) [10,33]
DiscodorididaePlatydoris sp. [22]
DiscodorididaeRostanga sp. 2 6kThis study
DiscodorididaeSebadoris nubilosa(Pease, 1871) [19]
DiscodorididaeThordisa cf. olivaChan & Gosliner, 20076oThis study
DorididaeDoriopsis apicalisBergh, 1890 [33]
DorididaeDoriopsis pecten(Collingwood, 1881) [34]
DoridomorphidaeDoridomorpha gardineriEliot, 1903 [10,19,33]
DotidaeDoto sp. 5bThis study
EmbletoniidaeEmbletonia gracilisRisbec, 19285cThis study
EubranchidaeEubranchus putnami n. sp.Fernández-Simón & Moles, 20235dThis study
EubranchidaeEubranchus sp. 5eThis study
FacelinidaeCaloria indica(Bergh, 1896)5g[22,33,34], This study
FacelinidaeCratena phyllodaEr. Marcus & Ev. Marcus, 1960 [19]
FacelinidaeCratena simbaEdmunds, 1970 [34]
FacelinidaeCratena sp. 5 5i[34], This study
FacelinidaeCratena sp. A 5hThis study
FacelinidaeCratena sp. B 5jThis study
FacelinidaeSakuraeolis marhe n. sp.Fernández-Simón & Moles, 20235n[34], This study
FacelinidaeFavorinus japonicusBaba, 19495l[34], This study
FacelinidaeFavorinus mirabilisBaba, 19555kThis study
FacelinidaeFavorinus tsuruganusBaba & Abe, 1964 [34]
FacelinidaeHerviella albidaBaba, 19665fThis study
FacelinidaeHerviella yatsui(Baba, 1930) [33]
FacelinidaeMoridilla brockiiBergh, 1888 [22,33,34]
FacelinidaeMoridilla maldivensis n. sp.Fernández-Simón & Moles, 20235mThis study
FacelinidaeMoridilla sp. [34]
FacelinidaeNoumeaella sp. 5oThis study
FacelinidaeNoumeaella sp. C [34]
FacelinidaePhidiana unilineata(Alder & Hancock, 1864) [33]
FacelinidaePteraeolidia aff. semperi(Bergh, 1870)5p[19,22,33,34], This study
FionidaeFiona sp. [33]
FionidaeTergiposacca longicerataCella, Carmona, Ekimova, Chichvarkhin, Schepetov & Gosliner, 2016[34]
FionidaeTergiposacca perspicua n. sp.Fernández-Simón & Moles, 20235qThis study
FlabellinidaeCoryphellina exoptata(Gosliner & Willan, 1991) [34]
FlabellinidaeFlabellina sp. [34]
GoniodorididaeGoniodoridella sp. 6pThis study
GoniodorididaeTrapania euryeiaGosliner & Fahey, 2008 [34]
GoniodorididaeTrapania naevaGosliner & Fahey, 2008 [37]
HexabranchidaeHexabranchus sanguineus(Rüppell & Leuckart, 1830)-[10,21,33,34], This study
LomanotidaeLomanotus vermiformisEliot, 1908 [34]
MadrellidaeMadrella ferruginosaAlder & Hancock, 1864 [10,33]
MyrrhinidaeGodiva sp. 5rThis study
PhyllidiidaePhyllidia alytaYonow, 19966x[10,21,33,34], This study
PhyllidiidaePhyllidia coelestisBergh, 1905 [34]
PhyllidiidaePhyllidia elegansBergh, 1869 [33]
PhyllidiidaePhyllidia exquisitaBrunckhorst, 1993 [21,34]
PhyllidiidaePhyllidia koehleriPerrone, 20006v[21,33,34], This study
PhyllidiidaePhyllidia marindica(Yonow & Hayward, 1991) [21,33,34]
PhyllidiidaePhyllidia multituberculataC. R. Boettger, 1918 [21]
PhyllidiidaePhyllidia ocellataCuvier, 1804 [34]
PhyllidiidaePhyllidia pictaPruvot-Fol, 19576yThis study
PhyllidiidaePhyllidia rueppelii(Bergh, 1869) [10]
PhyllidiidaePhyllidia sp. 6tThis study
PhyllidiidaePhyllidia varicosaLamarck, 18016z[10,14,19,33,34], This study
PhyllidiidaePhyllidiella meandrina(Pruvot-Fol, 1957) [33]
PhyllidiidaePhyllidiella rosans(Bergh, 1873)6w[14,21,33,34], This study
PhyllidiidaePhyllidiella rudmaniBrunckhorst, 1993 [14,21,33,34]
PhyllidiidaePhyllidiella sp. 6uThis study
PhyllidiidaePhyllidiella sp. 1 6aaThis study
PhyllidiidaePhyllidiella striata(Bergh, 1889)6ac[10,21,33,34], This study
PhyllidiidaePhyllidiella zeylanica(Kelaart, 1859)6ab[21,33,34], This study
PhyllidiidaePhyllidiopsis annaeBrunckhorst, 1993 [33,34]
PhyllidiidaePhyllidiopsis cardinalisBergh, 1876 [34]
PhyllidiidaePhyllidiopsis gemmataPruvot-Fol, 1957 [21,34]
PhyllidiidaePhyllidiopsis krempfiPruvot-Fol, 1957 [21]
PhyllidiidaePhyllidiopsis shireenaeBrunckhorst, 1990 [21,34]
PhyllidiidaePhyllidiopsis sp. 6adThis study
PhyllidiidaePhyllidiopsis sp. 5 [34]
PhyllidiidaePhyllidiopsis sphingisBrunckhorst, 1993 [21,34]
PhyllidiidaePhyllidiopsis xishaensis(Lin, 1983)6ae[21,33,34], This study
PinufiidaePinufius rebusEr. Marcus & Ev. Marcus, 1960 [19]
PolyceridaeGymnodoris ceylonica(Kelaart, 1858)6r[34], This study
PolyceridaeGymnodoris crocea(Bergh, 1889) [10,33]
PolyceridaeGymnodoris sp. 6sThis study
PolyceridaeMartadoris amakusana(Baba, 1987) [21,34]
PolyceridaeNembrotha cristataBergh, 1877 [22,33,34]
PolyceridaeNembrotha guttataYonow, 1994 [21,22,33,34]
PolyceridaeNembrotha kubaryanaBergh, 1877 [10,33]
PolyceridaeNembrotha lineolataBergh, 1905 [34]
PolyceridaeNembrotha megaloceraYonow, 1990 [14]
PolyceridaePolycera sp. 5 [34]
PolyceridaeRoboastra gracilis(Bergh, 1877)6q[21,22,33,34], This study
PolyceridaeTambja affinis(Eliot, 1904) [34]
PolyceridaeTambja morosa(Bergh, 1877) [34]
PolyceridaeTambja olivariaYonow, 1994 [22,34]
PolyceridaeThecacera vittataYonow, 1994 [22,34]
PolyceridaeTyrannodoris nikolasi(Pola, Padula, Gosliner & Cervera, 2014)[34]
SamlidaeSamla bicolor(Kelaart, 1858)5t[34], This study
SamlidaeSamla riwo(Gosliner & Willan, 1991)5s[34], This study
SamlidaeSamla rubropurpurata(Gosliner & Willan, 1991) [34]
SamlidaeSamla sp. 2 [34]
TrinchesiidaeCuthona netsica(Er. Marcus & Ev. Marcus, 1960)[19]
TrinchesiidaePhestilla lugubris(Bergh, 1870)5uThis study
TrinchesiidaePhestilla melanobrachiaBergh, 1874 [22,33,34]
TrinchesiidaePhestilla minorRudman, 1981 [34]
TrinchesiidaeTrinchesia sibogae(Bergh, 1905) [34]
TritoniidaeMarionia arborescensBergh, 1890 [10,34]
PLEUROBRANCHIDA
PleurobranchidaeBerthella martensi(Pilsbry, 1896)3c[22,33,34], This study
PleurobranchidaeBerthellina delicata(Rüppell & Leuckart, 1828)3b[22,33], This study
PleurobranchidaePleurobranchus forskaliiRüppell & Leuckart, 1828 [34]
PleurobranchidaePleurobranchus grandisPease, 1868 [34]
PTEROPODA
CavoliniidaeCavolinia globulosaGray, 1850 [35]
CavoliniidaeCavolinia sp. [35]
CavoliniidaeCavolinia unicinata(d’Orbigny, 1835) [13]
CliidaeClio convexa(Boas, 1886) [35]
CliidaeClio cuspidata(Bosc, 1801) [35]
CreseidaeBoasia chierchiae(Boas, 1886) [35]
CreseidaeCreseis virgula(Rang, 1828) [35]
CymbuliidaeCymbulia sp. [35]
PeraclidaePeracle reticulata(d’Orbigny, 1835) [35]
PYLOPULMONATA
PyramidellidaeLongchaeus acus(Gmelin, 1791) [12,15]
PyramidellidaeLongchaeus insularum(Pilsbry, 1922) [13]
PyramidellidaeLongchaeus maculosus(Lamarck, 1822) [12]
PyramidellidaeObeliscus monilisA. Adams, 1854 [40]
PyramidellidaeOtopleura auriscati(Holten, 1802) [12]
PyramidellidaeOtopleura mitralis(A. Adams, 1854) [13]
PyramidellidaeOtopleura nodicincta(A. Adams, 1854) [12,40]
PyramidellidaePyramidella dolabrata(Linnaeus, 1758) [12,40]
PyramidellidaePyramidella sp. [11]
SACOGLOSSA
CostasiellidaeCostasiella fridae n. sp.Fernández-Simón & Moles, 20237fThis study
HermaeidaeCyerce elegansBergh, 18707aThis study
HermaeidaeCyerce nigraBergh, 1871 [10]
HermaeidaeHermaea minorBergh, 1888 [10]
HermaeidaePolybranchia jensenaeMedrano, Krug, Gosliner, Biju Kumar & Valdés, 20187kThis study
LimapontiidaeStiliger sp. 1 7gThis study
PlakobranchidaeElysia cf. marginata(Pease, 1871)7c[34], This study
PlakobranchidaeElysia obtusaBaba, 1938-This study
PlakobranchidaeElysia pusilla(Bergh, 1871)7b[36], This study
PlakobranchidaeElysia sp. 11 7dThis study
PlakobranchidaeElysia sp. 17 [34]
PlakobranchidaeElysia sp. 44 7eThis study
PlakobranchidaePlakobranchus ocellatusvan Hasselt, 1824 [21,34]
PlakobranchidaeThuridilla coerulea(Kelaart, 1857) [22]
PlakobranchidaeThuridilla gracilis(Risbec, 1928)7h[21,22,33,34], This study
PlakobranchidaeThuridilla livida(Baba, 1955)7j[34], This study
PlakobranchidaeThuridilla sp. 1 [34]
PlakobranchidaeThuridilla vataae(Risbec, 1928)7i[21,34], This study
SIPHONARIIDA
SiphonarioideaSiphonaria cf. normalisA. Gould, 1846 [11,13]
SYSTELLOMMATOPHORA
OnchidiidaePeronia peronii(Cuvier, 1804) [19]
OnchidiidaePeronia verruculatum(Cuvier, 1830) [13]
UMBRACULIDA
UmbraculidaeUmbraculum umbraculum(Lightfoot, 1786) [11]
VETIGASTROPODA
FISSURELLIDA
FissurellidaeDiodora singaporensis(Reeve, 1850)8b[9,13], This study
FissurellidaeDiodora cf. ticaonica(Reeve, 1850) [13]
FissurellidaeEmarginella incisura(A. Adams, 1852) [9,13]
FissurellidaeEmarginella nigromaculata(Thiele, 1915)8cThis study
FissurellidaeEmarginella planulata(A. Adams, 1852) [9]
FissurellidaeEmarginella sp. 1 8dThis study
FissurellidaeEmarginula dilectaA. Adams, 1852 [13]
FissurellidaeEmarginula souverbianaPilsbry, 1891 [13]
FissurellidaeEmarginula sp. -This study
FissurellidaeHemimarginula cf. biangulata(G. B. Sowerby III, 1901)8aThis study
HALIOTIDA
HaliotidaeHaliotis clathrataReeve, 1846 [12,26]
HaliotidaeHaliotis ovinaGmelin, 17918e[9,11,13,15,26,33,38], This study
LEPETELLIDA
ScissurellidaeScissurella quadrataGeiger & Jansen, 2004 [27]
ScissurellidaeScissurella rotaYaron, 1983-[27], This study
ScissurellidaeSukashitrochus estotiensisLozouet, 1999 [27]
SEGUENZIIDA
ChilodontaidaePerrinia angulifera(A. Adams, 1853) [9]
TROCHIDA
AngariidaeAngaria delphinus(Linnaeus, 1758) [13,38]
AngariidaeAngaria sp. [11]
ColloniidaeCollonista solida(Preston, 1908) [13]
LiotiidaeLiotia squamicostataE. A. Smith, 1903 [13]
LiotiidaeLiotina sp. [13]
PhasianellidaeHiloa variabilis(Pease, 1861) [13]
TrochidaeCalliotrochus marmoreus(Pease, 1861)8g[13,31], This study
TrochidaeClanculus denticulatus(Gray, 1826) [33]
TrochidaeClanculus pharaonius(Linnaeus, 1758) [38]
TrochidaeClanculus puniceus(Philippi, 1846) [12]
TrochidaeClanculus samoensis(Hombron & Jacquinot, 1848)8f[9,11,12,13], This study
TrochidaeEthalia striolata(A. Adams, 1855) [13]
TrochidaeEthaliella rhodomphala(E. A. Smith, 1903) [9,13]
TrochidaeJujubinus maldivensis(E. A. Smith, 1903) [9,13]
TrochidaeMonilea calyculus(W. Wood, 1828) [9]
TrochidaeMonilea simulansE. A. Smith, 1899 [9]
TrochidaeRossiteria nucleus(Philippi, 1850) [13]
TrochidaeRubritrochus pulcherrimus(A. Adams, 1855) [9,13]
TrochidaeStomatella auriculaLamarck, 1816 [9,11,12,13]
TrochidaeStomatella nigraQuoy & Gaimard, 1834 [12]
TrochidaeStomatella varia(A. Adams, 1850)8nThis study
TrochidaeStomatia phymotisHelbling, 1779 [11,12,13]
TrochidaeStomatolina cf. irisata(Dufo, 1840) [11]
TrochidaeStomatolina rubra(Lamarck, 1822)8lThis study
TrochidaeStomatolina sp. 1 8kThis study
TrochidaeSynaptocochlea sp. [13]
TrochidaeTrochus cf. intextusKiener, 1850 [11]
TrochidaeTrochus flammulatusLamarck, 1822 [39]
TrochidaeTrochus maculatusLinnaeus, 17588h[9,11,12,13,14,15,38], This study
TrochidaeTrochus ochroleucusGmelin, 1791 [13]
TrochidaeTrochus radiatusGmelin, 1791 [9,12,38]
TrochidaeTrochus sacellumPhilippi, 1855 [33]
TrochidaeTrochus cf. stellatusGmelin, 17918i[9], This study
TrochidaeTrochus sp. 8jThis study
TrochidaeTrochus tubiferusKiener, 1850 [9,13]
TurbinidaeAstralium haematragum(Menke, 1829) [33]
TurbinidaeAstralium cf. helicinum(Gmelin, 1791) [13]
TurbinidaeAstralium rhodostomum(Lamarck, 1822)-[11,12,33], This study
TurbinidaeRochia conus(Gmelin, 1791) [15]
TurbinidaeTectus fenestratus(Gmelin, 1791) [12,33]
TurbinidaeTectus pyramis(Born, 1778)-[12,13,14,33], This study
TurbinidaeTurbo argyrostomusLinnaeus, 1758-[9,11,12,13,38,39], This study
TurbinidaeTurbo chrysostomusLinnaeus, 1758 [33]
TurbinidaeTurbo intercostalisMenke, 1846 [15]
TurbinidaeTurbo petholatusLinnaeus, 17588m[11,12,15,38], This study
NERITIMORPHA
CYCLONERITIDA
PhenacolepadidaeZacalantica tenuisculpta(Thiele, 1909)8oThis study
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MDPI and ACS Style

Cunha, T.J.; Fernández-Simón, J.; Petrula, M.; Giribet, G.; Moles, J. Photographic Checklist, DNA Barcoding, and New Species of Sea Slugs and Snails from the Faafu Atoll, Maldives (Gastropoda: Heterobranchia and Vetigastropoda). Diversity 2023, 15, 219. https://doi.org/10.3390/d15020219

AMA Style

Cunha TJ, Fernández-Simón J, Petrula M, Giribet G, Moles J. Photographic Checklist, DNA Barcoding, and New Species of Sea Slugs and Snails from the Faafu Atoll, Maldives (Gastropoda: Heterobranchia and Vetigastropoda). Diversity. 2023; 15(2):219. https://doi.org/10.3390/d15020219

Chicago/Turabian Style

Cunha, Tauana J., Jose Fernández-Simón, Macy Petrula, Gonzalo Giribet, and Juan Moles. 2023. "Photographic Checklist, DNA Barcoding, and New Species of Sea Slugs and Snails from the Faafu Atoll, Maldives (Gastropoda: Heterobranchia and Vetigastropoda)" Diversity 15, no. 2: 219. https://doi.org/10.3390/d15020219

APA Style

Cunha, T. J., Fernández-Simón, J., Petrula, M., Giribet, G., & Moles, J. (2023). Photographic Checklist, DNA Barcoding, and New Species of Sea Slugs and Snails from the Faafu Atoll, Maldives (Gastropoda: Heterobranchia and Vetigastropoda). Diversity, 15(2), 219. https://doi.org/10.3390/d15020219

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