ArticlePDF Available

Systematic revision of the Indo-West Pacific colourful bubble-snails of the genus Lamprohaminoea Habe, 1952 (Cephalaspidea : Haminoeidae)

Authors:
Trond Roger Oskars at Møreforsking
Trond Roger Oskars
Manuel Malaquias at University of Bergen
Manuel Malaquias
Download full-text PDF
Read full-text
Download citation

Abstract

The genus Lamprohaminoea includes species of colourful haminoeid snails associated with coral reefs and rocky shores in the tropical Indo-West Pacific. In this work, we revise the diversity and systematics of Lamprohaminoea species based on a phylogenetic hypothesis and on a detailed morphological analysis of specimens. Shells, external features of the animals and anatomical characters from the jaws, radula, gizzard plates, and male reproductive system were studied by optical and scanning electron microscopy. Additionally, a molecular species delimitation analysis based on the Automatic Barcode Gap Discovery method using DNA sequences of the cytochrome c oxidase subunit I was implemented. Five species were recognised, three of them new to science, namely L. cymbalum, L. ovalis, L. vamiziensis sp. nov., L. evelinae sp. nov., and L. mikkelsenae sp. nov. Morphologically, these species can be separated by subtle differences of their external colouration and by features of the male reproductive system. Lamprohaminoea vamiziensis sp. nov. is known only from the western Indian Ocean and L. evelinae sp. nov., from the west Pacific, whereas the other three occur across the Indo-West Pacific realm.
Content uploaded by Manuel Malaquias
Author content
All content in this area was uploaded by Manuel Malaquias on Sep 08, 2020
Content may be subject to copyright.
Systematic revision of the Indo-West Pacific colourful
bubble-snails of the genus Lamprohaminoea Habe, 1952
(Cephalaspidea : Haminoeidae)
Trond R. Oskars
A,B
and Manuel António E. Malaquias
A,C
A
Section of Taxonomy and Evolution, Department of Natural History, University Museum of Bergen,
University of Bergen, PB7800, NO-5020 Bergen, Norway.
B
Department of Environmental Protection, Fylkesmannen i Møre og Romsdal (County Governor’soffice),
PO2520, NO-6404 Molde, Norway.
C
Corresponding author. Email: manuel.malaquias@uib.no
Abstract. The genus Lamprohaminoea includes species of colourful haminoeid snails associated with coral reefs and
rocky shores in the tropical Indo-West Pacific. In this work, we revise the diversity and systematics of Lamprohaminoea
species based on a phylogenetic hypothesis and on a detailed morphological analysis of specimens. Shells, external
features of the animals and anatomical characters from the jaws, radula, gizzard plates, and male reproductive system
were studied by optical and scanning electron microscopy. Additionally, a molecular species delimitation analysis
based on the Automatic Barcode Gap Discovery method using DNA sequences of the cytochrome coxidase subunit
I was implemented. Five species were recognised, three of them new to science, namely L. cymbalum,L. ovalis,
L. vamiziensis sp. nov., L. evelinae sp. nov., and L. mikkelsenae sp. nov. Morphologically, these species can be
separated by subtle differences of their external colouration and by features of the male reproductive system.
Lamprohaminoea vamiziensis sp. nov. is known only from the western Indian Ocean and L. evelinae sp. nov.,
from the west Pacific, whereas the other three occur across the Indo-West Pacific realm.
Keywords: biodiversity, haminoeid snails, Heterobranchia, Mollusca, morphology, phylogeny.
Received 6 April 2020, accepted 27 May 2020, published online 8 September 2020
Introduction
Oskars and Malaquias (2019) have shown that the Indo-West
Pacific (IWP) genus Haloa Pilsbry, 1921 (sensu Oskars et al.
2019) comprises a paraphyletic group of four distinct genera
(Fig. 1). One of them is Lamprohaminoea Habe, 1952, which
includes only colourful species with patterns of green, red,
orange, white, yellow, and purple dots or blotches (Fig. 2,3)
distributed across subtropical and tropical latitudes of the IWP
realm, where they inhabit tidal and shallow rocky and coral
reef systems (Gosliner et al.2008,2015; Apte and Desai 2017;
Tibiri¸cá and Malaquias 2017). It has been suggested that the
occurrence of bright colours in these snails signals the
presence of distasteful secondary metabolites with a
deterrent role in defence (Poiner et al.1989; Fontana et al.
2001; Mollo et al.2008). Like other haminoeids,
Lamprohaminoea are herbivores feeding apparently on
cyanobacteria (Cruz-Rivera and Paul 2006).
In recent literature three species of colourful haminoeids
are often recognised, namely the widespread Lamprohaminoea
cymbalum (Quoy & Gaimard, 1833), with a whitish-greenish
background, and the presence of large orange blotches
surrounded by a white rim, Lamprohaminoea ovalis (Pease,
1868), also widespread in the IWP with a greenish background
pattern, dotted by dark purple spots and with rounded orange
blotches surrounded by a white rim, and Lamprohaminoea
cyanomarginata (Heller & Thompson, 1983), native to the Red
Sea with a white background, scarce purple blotches and lobes
lined by purple colour (Heller and Thompson 1983; Debelius
1996;Rudman1999a,1999b,2003; Hori 2017; Gosliner et al.
2008,2015; Nimbs and Smith 2016; Apte and Desai 2017;
Pittman and Fiene 2018a,2018b).
The species L. cymbalum (Quoy & Gaimard, 1833)
(originally named Bulla cymbalum) was described on the
basis of shells from Guam, and L. ovalis (Pease, 1868)
(originally described as Haminea ovalis), was based on
shells and colour patterns of specimens from Tahiti
(Fig. 2A). Heller and Thompson (1983) described
L. cyanomarginata (original name Haminea cyanomarginata)
from the Sudanese Red Sea based on the shell, colour pattern,
radula and male reproductive system. There are now several
records of this latter species in the Mediterranean Sea where it
seems to be established and thriving (Zenetos et al.2004,2008,
Journal compilation CSIRO 2020 www.publish.csiro.au/journals/is
CSIRO PUBLISHING
Invertebrate Systematics, 2020, 34, 727–756
https://doi.org/10.1071/IS20026
... Recently, OSkaRS and MalaquIaS (2019) have resurrected the generic name Lamprohaminoea to include some previously Indo-Pacific Haminoea species characterized by colourful patterns, including H. cyanomarginata. Subsequently, these authors (OSkaRS & MalaquIaS, 2020) have considered this species as a junior synonym of Lamprohaminoea ovalis in their systematic revision of the genus. These authors documented a remarkable genetic homogeneity throughout its wide distribution area, including samples from the Red Sea and Mediterranean, despite the variability of its colour pattern which they considered as intraspecific variation. ...
... These authors documented a remarkable genetic homogeneity throughout its wide distribution area, including samples from the Red Sea and Mediterranean, despite the variability of its colour pattern which they considered as intraspecific variation. Thus, these authors called the "purple morph" of L. ovalis the taxon previously described in the Red Sea as H. cyanomarginata (OSkaRS & MalaquIaS, 2020). ...
... all the specimens observed in the study area belong to the so called 'purple morph' of L. ovalis (OSkaRS & MalaquIaS, 2020), characterized by white background with solid purple lines along edges of cephalic shield, parapodial and pallial lobes, and scattered yellow round blotches (Fig. 2). The shell is globose, translucent, with a smooth surface and almost imperceptible growth lines (Fig. 4a). ...
Fast recent southwestward expansion of the alien species Lamprohaminoea ovalis (Gastropoda, Heterobranchia) along the Mediterranean coasts of the Iberian Peninsula
Article
Full-text available
  • Jul 2024
Monitoring and updating the geographic spread of non-native species is of chief importance for conservation. Here we report on the range expansion of the Red Sea alien heterobranch gastropod Lamprohaminoea ovalis in southeast Spain, which reached the Alboran Sea (coast of the Granada province) in autumn 2023. This record represents the westernmost of the species in the Mediterranean Sea. The species is established in the studied area with a seasonal presence. It appears in summer, reaches reaches population peak in autumn, and disappears during winter. The importance of "citizen scientists" for information about the distribution of species and monitoring the status on invasive populations is stressed.
View
... During the work on the phylogeny and systematics of Haloa sensu lato , one whole specimen was photographed and DNA sequencing was attempted. The genetic markers from the two specimens on which sequencing was attempted were cytochrome oxidase 1(COI), 16S ribosomal ribonucleic acid(rRNA), 12S rRNA, 28S rRNA and Histone 3 (see Oskars and Malaquias 2020a). However, none of these genetic markers amplified successfully. ...
... Due to this, the whole specimen was extracted for DNA. However, as the gene amplifications all failed, the remaining specimens were set aside for more thorough anatomical study in the systematic revision of Lamprohaminoea (Oskars and Malaquias, 2020a), as it was assumed to be a juvenile Lamprohaminoea. The large shell-less specimen was dissected, but when it became apparent that it was likely a unique species within Haminoeidae, gene amplification and sequencing was attempted. ...
... It also differs from A. naucum in that the aperture is wider anteriorly and tapers more apically. The external colouration of this genus is reminiscent of Lamprohaminoea, but the colourful markings are restricted to the mantle, whereas in Lamprohaminoea the cephalic shield and parapodia also have scattered colourful dots (Oskars and Malaquias 2020a). It is also distinguished from Lamprohaminoea by internal anatomy (see below). ...
Release the confetti! A new genus and species of Indo-West Pacific bubble snails (Cephalaspidea: Haminoeidae)
Article
Full-text available
  • Feb 2024
The bubble snail family Haminoeidae has traditionally been the richest in genera within Cephalaspidea; however, most of these genera were erected based on only the characteristics of the shell or external morphology. The family was recently revised through a combined analysis of DNA, internal anatomy, and external body and shell morphology, leading to major taxonomic rearrangements and a drastic reduction in the number of genera. However, these analyses also show that there may still be undefined genera and certainly several undescribed species waiting to be discovered. In this work, a new genus and species is described in light of recent revisions within Haminoeidae and the phylogenetic hypothesis generated by Oskars and colleagues. Due to its colourful external anatomy, the new species was initially assumed to belong to Lamprohaminoea, but the specimens failed to produce DNA sequences that could confirm this hypothesis. During further anatomical study of species of Lamprohaminoea and further examination of these specimens, it became clear that the morpho-anatomical features of Confettiella malaquiasi gen. n. and sp. n. distinguish it from this genus and all other genera and species of the Haminoeidae. To illustrate this, shells, external features of the animals, and anatomical characters of the jaws, radula, gizzard plates, and female and male reproductive system were studied by optical and scanning electron microscopy, and these studies are reported here.
View
... Following a taxonomic revision of the Order Cephalaspidea, Haminoea cyanomarginata Heller & Thompson, 1983 was described from individuals of the Red Sea (Heller & Thompson, 1983;Dekker & Orlin, 2000) and initially considered junior synonym of Lamprohaminoea cyanomarginata (Oskars & Malaquias, 2019). Further taxonomic studies demonstrated that both H. cyanomarginata and L. cyanomarginata are junior synonyms of Lamprohaminoea ovalis (Pease, 1868; Oskars & Malaquias, 2020). This heterobranch, characterized by highly variable body colour pattern, was first described from Tahiti (French Polynesia, France). ...
... Nowadays it is widespread from the Red Sea to the Indo-West Pacific. Its fairly recent records from Greece, Turkey, Malta, Italy, Cyprus, Croatia and Spain, more than 20 years after its first finding in the Red Sea, suggest that it is an invasive Lessepsian species that entered and established in the Mediterranean Sea via the Suez Canal (Rizgalla et al., 2018;Oskars & Malaquias, 2020). Nowadays, L. ovalis has been reported from the whole Mediterranean basin (Mifsud, 2007;Zenetos et al., 2010;Fernández-Vilert et al., 2018 and reference therein;Ragkousis et al., 2020), except from the Gulf of Lion and the Ligurian Sea. ...
... The mantle bordered with purple perfectly matches the 'L. cyanomarginata purple morph' (Figure 3) reported in the recent systematic revision of the genus Lamprohaminoea Habe, 1952 and ascribed to L. ovalis species (Oskars & Malaquias, 2020). ...
Seawater warming favours the northward range expansion of Lessepsian species in the Mediterranean Sea: the cephalaspidean Lamprohaminoea ovalis
Article
Full-text available
  • Jul 2022
  • J MAR BIOL ASSOC UK
Monitoring the spread of non-indigenous species is fundamental to study global warming effects on marine biodiversity. A valuable tool is represented by the continuous updating of the geographic range expansion of non-indigenous species. Lamprohaminoea ovalis is a Lessepsian mollusc initially recorded in the Mediterranean Sea in 2001. This paper reports its range expansion over the last 20 years related to water warming. The first record of Lamprohaminoea ovalis from the Ligurian Sea (NW Mediterranean) is also reported. Two individuals (about 10 mm length) were observed on a sub-vertical rocky bottom at 26 m depth displaying potential trailing behaviour. This recent finding extends the currently known distributional range of Lamprohaminoea ovalis, representing the northernmost occurrence of this non-indigenous species in the western Mediterranean Sea.
View
... Príncipe, Angola;Bernard, 1984;Martínez & Ortea, 1997;Rolán & Ryall, 1999). Likewise, the name H. ovalis is commonly employed to designate animals with tiny orange or yellow dots on the body occurring in the Eastern Pacific, between Mexico and Peru (Behrens & Hermosillo, 2005;Hermosillo et al., 2006;Valdés & Camacho-Garcia, 2004); nonetheless, H. ovalis was described by Pease (1868) from Tahiti and was recently reassigned to the genus Lamprohaminoea by Oskars and Malaquias (2020c), who confirmed the species to be widespread in the Indo-West Pacific and absent from the Eastern Pacific. In fact, in a previous study, Oskars & Malaquias (2019, as Haminoea sp.1 475) showed that dotted orange haminoeids from Peru were phylogenetically related to all other Atlantic and Eastern Pacific Haminoea species. ...
... Finally, we retrieved a lineage morphologically compatible with what has been named in recent literature as H. ovalis (Behrens & Hermosillo, 2005;Hermosillo et al., 2006;Valdés & Camacho-Garcia, 2004). However, as explained in the Introduction this name applies to an Indo-West Pacific species in the genus Lamprohaminoea (Oskars & Malaquias, 2020c;Pease, 1868). This Eastern Pacific species has globose smooth shells and a body doted by abundant tiny orange dots. ...
Molecular phylogeny of the marine snail genus Haminoea (Gastropoda, Cephalaspidea): A framework to study marine diversity and speciation
Article
Full-text available
  • Aug 2023
Haminoea are herbivorous, coastal snails occurring in temperate and tropical waters of the Atlantic and Eastern Pacific oceans, with one species present in temperate South Africa (Indian Ocean). The genus is taxonomically difficult as several available nominal species were introduced based on shell descriptions alone, or described based on subtle differences in morpho‐anatomical features, without a phylogenetic molecular framework. Fifteen species are currently accepted as valid in recent scientific literature and field guides (eight Eastern Atlantic, one temperate Indian Ocean, four Western Atlantic and three Eastern Pacific). Here we generate the first complete phylogeny (Bayesian and Maximum Likelihood) of this genus based on multilocus molecular data (COI, 12S rRNA, 16S rRNA, 28S rRNA) using a taxon set accumulated over a period of 15 years, coupled with species delimitation analyses methods (ABGD, ASAP, bPTP) and morpho‐anatomical studies. The goal of this study is to provide insights into the taxonomy, phylogenetic relationships and geographical distributions of species while generating a framework for future systematic reviews of the genus, as well as to study speciation and historical biogeography. Our results rendered four possible hypotheses of species diversity: with 14, 15, 19 and 20 candidate species and point to the fact that several taxa presently regarded as valid might be conspecific (e.g. H. orteai – H. templadoi – H. exigua ; and H. alfredensis – H. antillarum – H. orbignyana ), while highlighting the existence of a complex of four or five species often identified as H. elegans . Pervasive nomenclatural problems in the genus, including with the type species H. hydatis , are highlighted and discussed.
View
... The photographs were taken at a very shallow depth (1 to 2 m) over algae-covered rocks. Identification of the species was made according to Zenetos et al. (2004) and Oskars & Malaquias (2020). ...
... The Aegean Sea individuals of Lamprohaminoea ovalis were characterized by the combination of purple or dark blue-bordered mantle, white body, a large bluish spot separating the narrowly spaced eyes, and deeply bifurcated cephalic shield (Fig. 3), in accordance with Zenetos et al. (2004). The observed coloration fits the purple morph definition of Oskars & Malaquias (2020) and some individuals also bear vivid yellow round blotches along the body. In the Mediterranean Sea, the species has been observed both in the daytime and at night, from very shallow depths of 30 cm to as deep as 30 m on rocky surfaces covered by algae (Rudman, 2003;Zenetos et al., 2004;Rizgalla et al., 2018), which is consistent with our observations. ...
New Data on the Occurrence of Two Lessepsian Marine Heterobranchs, Plocamopherus ocellatus (Nudibranchia: Polyceridae) and Lamprohaminoea ovalis (Cephalaspidea: Haminoeidae), from the Aegean Sea
Article
Full-text available
  • Dec 2022
The authors have recently collected two Lessepsian heterobranchs from Turkey, namely Plocamopherus ocellatus Rüppell & Leuckart, 1828 and Lamprohaminoea ovalis (Pease, 1868), both of which were found significantly out of their known distribution ranges. The single individual of P. ocellatus collected at Akbük Cove is a new addition to the Aegean Sea malacofauna, while several individuals of L. ovalis observed from the Ayvalık Islands Nature Park and Saros Bay represent the northernmost occurrence limit of the species. Present findings suggest that P. ocellatus is currently a casual alien species in the region, while L. ovalis has established a breeding population in the northern Aegean Sea.
View
... Molecular work (Austin et al. 2018) showed that Phanerophthalmus olivaceous was indeed endemic to the Red Sea and different from several similar counterparts in the Indo-Pacifc, while Oskars and Malaquias (2020) proved exactly the opposite, also using molecular techniques, that the endemic Haminoea cyanomarginata (Heller & Thompson, 1983) formed part of the widespread and morphologically variable Indo-Pacifc species Lamprohaminoea ovalis. ...
View
... The cephalaspidean genus Haminoea Turton & Kingston [in Carrington], 1830 [Type species: Bulla hydatis Linnaeus, 1758, by monotypy] is found worldwide in temperate and tropical coasts. It has been relatively well-studied, with reviews based on both morphology and molecular approaches, providing additional insights into its history, biogeography, phylogeny, and supplementary bibliography (e.g., Rudman, 1971;Malaquias & Cervera, 2006;Bharate et al., 2018;Oskars, 2019;Oskars & Malaquias, 2020;Turani et al., 2023). ...
A new species of Haminoea in Brazilian coast (Cephalaspidea, Haminoeidae) as part of H. elegans group
Article
Full-text available
  • Jul 2024
Haminoea maray is introduced as a replacement for what was previously identified as H. elegans, now recognized as a complex comprising several species found on both sides of the Atlantic. This descriptive paper presents a comprehensive phenotypic study based on specimens collected from Ceará to São Paulo, Brazil, and had been previously recognized as a molecular variant. The newly described species inhabits estuarine environments with low salinity, exhibiting distinct conchological and anatomical features compared to other populations of H. elegans and related congeners. https://zoobank. org/936AAD86-91A6-459D-A6ED-9C3DC7F2E8FF.
View
... Molecular work (Austin et al. 2018) showed that Phanerophthalmus olivaceous was indeed endemic to the Red Sea and different from several similar counterparts in the Indo-Pacifc, while Oskars and Malaquias (2020) proved exactly the opposite, also using molecular techniques, that the endemic Haminoea cyanomarginata (Heller & Thompson, 1983) formed part of the widespread and morphologically variable Indo-Pacifc species Lamprohaminoea ovalis. ...
View
... perversa), reddish-brown (Aplysia depilans), and black (Aplysia vaccaria), with stripes or spotted patterns (Aglaja tricolorata). Although many euopisthobranchs have a dull color, the skin of tropical cephalaspideans can be colorful (Tibiriçá and Malaquias, 2017;Oskars and Malaquias, 2020). In strongly colored areas of A. californica skin, epidermal cells contain numerous electron-dense pigment vesicles about 0.6 μm in diameter, while in less colored areas epidermal cells contain fewer electron-dense vesicles or just vesicles with an electron-lucent content. ...
Euopisthobranchs: Integument
Chapter
  • Jan 2024
The integument comprises the epidermis formed by a layer of cells with apical microvilli and cilia, underlined by connective tissue with some muscle fibers, nerves, and different types of glands. Mucus is the main secretory product of the integument, but glands that release bioactive compounds are crucial for the chemical defense strategies of these animals. Blochmann's glands are one type of gland that occurs in cephalaspideans and anaspideans consisting of a very large single subepithelial cell surrounded by muscle fibers, with a duct that opens in the epidermis. The ink gland of anaspideans is formed by a cluster of Blochmann's glands located on the roof of the mantle cavity. The opaline gland is another kind of gland present in anaspideans, consisting of a cluster of very large secretory cells positioned beneath the floor of the mantle cavity. The secretions of the ink and opaline glands mix in the mantle cavity before being released to defend the sea hares from predators. Pigments contained in integument cells are responsible for the color of these animals, rendering them cryptic or conspicuous to advertise their toxicity or distastefulness, which is another important element of their defense.
View
... Similarly, Nimbs and Smith (2021) discovered the south-east Australian endemic species Dendrodoris gunnamatta Allan, 1932 to be a morphotype of the widespread Indo-Pacific Dendrodoris krusensternii (Gray, 1850). Studies have also revealed separate species within cryptic complexes (Golestani et al. 2019;Oskars and Malaquias 2020;Nimbs and Wilson 2021). ...
The curious case of Phyllidia ocellata and the first molecular data of three phyllidiid species from India (Gastropoda, Heterobranchia, Phyllidiidae)
Article
Full-text available
  • May 2023
The current study presents the first molecular data of three species of the family Phyllidiidae, Phyllidia ocellata, Phyllidia alyta and Phyllidiella rosans, from Indian waters. The P. ocellata molecular sequences closely match those available from the Pacific Ocean, whereas P. alyta and P. rosans form independent clades, confirming their identifications as distinct species. Phyllidia ocellata, frequently found in the Indo-Pacific tropical coral reefs, is renowned for its wide range of colours and external forms. Numerous variations have been found and are being examined at the molecular level, and the subject of this study is another variation that, until dissection and molecular analysis, was thought to be a colour form of Phyllidia multituberculata. Although India has a long history of heterobranch research, no phyllidiid species from Indian waters have ever been the subject of molecular research.
View
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
Article
Full-text available
  • Jul 2016
We present the latest version of the Molecular Evolutionary Genetics Analysis (MEGA) software, which contains many sophisticated methods and tools for phylogenomics and phylomedicine. In this major upgrade, MEGA has been optimized for use on 64-bit computing systems for analyzing bigger datasets. Researchers can now explore and analyze tens of thousands of sequences in MEGA. The new version also provides an advanced wizard for building timetrees and includes a new functionality to automatically predict gene duplication events in gene family trees. The 64-bit MEGA is made available in two interfaces: graphical and command line. The graphical user interface (GUI) is a native Microsoft Windows application that can also be used on Mac OSX. The command line MEGA is available as native applications for Windows, Linux, and Mac OSX. They are intended for use in high-throughput and scripted analysis. Both versions are available from www.megasoftware.net free of charge.
View
A molecular phylogeny of the Indo-West Pacific species of Haloa sensu lato gastropods (Cephalaspidea: Haminoeidae): Tethyan vicariance, generic diversity, and ecological specialization
Article
Full-text available
  • Jul 2019
The cephalaspidean gastropod genus Haminoea has been considered a worldwide radiation with species living in intertidal and shallow areas with algae, seagrass sandy-mud, mangroves, and coral reefs. Recently this monophyletic status was questioned and it was suggested that Haminoea proper only included Atlantic plus eastern Pacific species, whereas the Indo-West Pacific species were a separate radiation belonging to the genus Haloa. In this work we used an extended dataset of Haminoea sensu lato including to our best knowledge representatives of all Indo-West Pacific species, plus a large representation of Atlantic and eastern Pacific species. Bayesian and maximum likelihood molecular phylogenetic analyses using three mitochondrial (COI, 12S rRNA, 16S rRNA) and two nuclear genes (28S rRNA and Histone-3) were employed to study relationships and diversification including also the closely related genus Smaragdinella. Our results support a monophyletic Atlantic + eastern Pacific Haminoea clade and a monophyletic Indo-West Pacific radiation with five genera all defined by unique morphological characters and ecological requirements, namely Haloa proper with tropical and sub-tropical species spread across the Indo-West Pacific, Lamprohaminoea including only colourful species of tropical and sub-tropical affinity, Bakawan gen. nov. with species associated with mangrove habitats across the tropical eastern Indian Ocean and western Pacific, Papawera gen. nov. restricted to temperate waters of Australasia, and Smaragdinella the only cephalaspidean genus inhabiting intertidal hard substrates across sub-tropical and tropical regions of the Indo-West Pacific. This result suggests the role of the closure of the Tethys seaway structuring the phylogeny of worldwide "Haminoea" snails and of ecology driving the phylogenetic structure of the Indo-West Pacific radiation.
View
Systematic revision, diversity patterns and trophic ecology of the tropical Indo-West Pacific sea slug genus Phanerophthalmus A. Adams, 1850 (Cephalaspidea, Haminoeidae)
Article
Full-text available
  • Dec 2018
Phanerophthalmus is a genus of Indo-West Pacific sea slugs inhabiting seagrass and coral reefs with up to now seven species currently recognised as valid. The goals of this study are to revise the systematics of Phanerophthalmus, infer its phylogeny and patterns of diversity, as well as study its diet. Morphology was combined with molecular phylogenetics based on two mitochondrial (cytochrome c oxidase subunit I, 16S rRNA) and one nuclear (28S rRNA) genes. Molecular species delimitation methods (ABGD, DISSECT) were employed to aid delimiting species. Diet was assessed by gut content analysis. Seventeen species were recognised,
View
Description of a new species of Haminoea (Gastropoda: Cephalaspidea) from India, with an account of the diversity of the genus in the Indo-West Pacific
Article
Full-text available
  • Nov 2018
In this paper current knowledge on the diversity of the gastropod cephalaspidean genus Haminoea from India is revised. A comprehensive literature review was undertaken and novel specimens were collected. Specimens from India were DNA barcoded using the gene cytochrome c oxidase sub-unit I and a Bayesian gene tree together with an Automatic Barcode Gap Discovery (ABGD) species delimitation analysis were inferred to compare Indian samples with species from the Indo-West Pacific. The most comprehensive DNA data set to date of the genus Haminoea is included and new morpho-anatomical features of Indo-West Pacific species were generated through fine anatomical work and scanning electron microscopy. A critical appraisal of previous records of the country is included and a new species, Haminoea aptei sp. nov., is described from the Andaman Islands and Lakshadweep Islands, India. www.zoobank.org/urn:lsid:zoobank.org:pub:90C191A9-5CA6-4BC6-84E3-B1A26674FA1B
View
Beyond Capricornia: Tropical Sea Slugs (Gastropoda, Heterobranchia) Extend Their Distributions into the Tasman Sea
Article
Full-text available
  • Sep 2018
  • Diversity
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.
View
First records of the Red Sea alien mollusc Haminoea cyanomarginata (Gastropoda: Heterobranchia: Cephalaspidea) in the Western Mediterranean
Article
Full-text available
  • Jul 2018
The colonization of foreign species into the Mediterranean Sea has increased in number and geographic coverage over the past decades. For instance, the marine mollusc Haminoea cyanomargi-nata has scattered across the Central and Eastern Mediterranean since its description in the Red Sea by Heller and Thompson in 1983. In this study, we add the first records of the species in the Western Mediterranean basin and review the progression of its colonization from the Red Sea. The new records were obtained through the online database of the NGO called Catalan Opisthobranch Research Group (Spain), thus highlighting how citizen science platforms can provide an early warning for marine scientists and managers in relation to exogenous species. ARTICLE HISTORY
View
Histological, histochemical, and ultrastructural investigation of the male copulatory apparatus of Haminoea navicula (Gastropoda, Cephalaspidea)
Article
Full-text available
  • Jan 2018
Due to its biological and systematic importance, the morphology and function of the male copulatory apparatus of Haminoea navicula, a Cephalaspidea gastropod mollusk, was investigated by light and electron microscopy. These systems are poorly understood in haminoids, but are often used in the taxonomy of the genus. In H. navicula, the male copulatory apparatus comprises the penis within a penial sheath, a seminal duct and the prostate with two lobes. The penis is a muscular structure with a tip covered by spikes formed by muscular cells. The penial sheath consists of muscular tissue folds lined by an epithelium. Below this epithelium, polysaccharide-secreting cells and pigment cells were observed. A large number of vacuolar cells were found below the ciliated epithelium of the seminal duct. The proximal lobe of the prostate was formed by tubules that could be divided in basal, middle and apical zones, containing cells that secrete polysaccharides and proteins. The tubules of the prostate distal lobe contained a single type of secretory cells with vesicles that were stained by histochemical techniques for detection of polysaccharides and proteins. Ciliated cells were present along the tubules in both lobes of the prostate. This study revealed a complex prostate with five types of secretory cells, which secrete substances that should be involved in the maintenance and eventually also in the maturation of spermatozoa. A comparison with previous publications, shows that the male copulatory apparatus can differ substantially among cephalaspideans, even between H. navicula and non-European species attributed to this genus.
View
Aeolidia papillosa (Linnaeus, 1761) (Mollusca: Heterobranchia: Nudibranchia), single species or a cryptic species complex? A morphological and molecular study
Article
Full-text available
  • Jun 2016
Aeolidia papillosa (Linnaeus, 1761) is a well-known aeolidiid species that has been reported to have a worldwide distribution in cold–temperate waters, mainly from the northern hemisphere. Molecular tools have recently shown that most cosmopolitan species usually belong to a taxonomic species complex. Here we used integrative taxonomy to test the range of distribution of A. papillosa, and to assess the existence of a putative species complex that has been traditionally included as a single species under the name A. papillosa. Maximumlikelihood and Bayesian analyses of partial DNA sequences of the mitochondrial cytochrome c oxidase subunit I and 16S rRNA genes, and the nuclear gene histone 3, were used to infer phylogenetic trees. Automatic Barcode Gap Discovery (ABGD) species delimitation analyses and morphological study complemented the phylogenetic approach. Our results show that A. papillosa is a cosmopolitan and an amphi-Atlantic species, being distributed in the eastern and western Atlantic as well as in the eastern Pacific; however, some specimens from the UK and the Netherlands, together with specimens from Portugal, Galicia, and France, as well as the Californian and Oregon populations, emerge as two pseudocryptic species described herein: Aeolidia filomenae sp. nov. and Aeolidia loui sp. nov., respectively. Finally, the specimens from Chilean coasts, previously attributed to A. papillosa, belong to a different species, Aeolidia campbellii (Cunningham, 1871), that is a senior synonym of Aeolidia serotina Bergh, 1873.
View
The bubble snails (Gastropoda, Heterobranchia) of Mozambique: an overlooked biodiversity hotspot
Article
Full-text available
  • May 2016
This first account, dedicated to the shallow water marine heterobranch gastropods of Mozambique is presented with a focus on the clades Acteonoidea and Cephalaspidea. Specimens were obtained as a result of sporadic sampling and two dedicated field campaigns between the years of 2012 and 2015, conducted along the northern and southern coasts of Mozambique. Specimens were collected by hand in the intertidal and subtidal reefs by snorkelling or SCUBA diving down to a depth of 33 m. Thirty-two species were found, of which 22 are new records to Mozambique and five are new for the Western Indian Ocean. This account raises the total number of shallow water Acteonoidea and Cephalaspidea known in Mozambique to 39 species, which represents approximately 50 % of the Indian Ocean diversity and 83 % of the diversity of these molluscs found in the Red Sea. A gap in sampling was identified in the central swamp/mangrove bio-region of Mozambique, and therefore, we suggest that future research efforts concentrate on or at least consider this region.
View
An Illustrated Inventory of the Sea Slugs of New South Wales, Australia (Gastropoda: Heterobranchia).
Article
  • Feb 2017
Although the Indo-Pacific is the global centre of diversity for the heterobranch sea slugs, their distribution remains, in many places, largely unknown. On the Australian east coast, their diversity decreases from approximately 1000 species in the northern Great Barrier Reef to fewer than 400 in Bass Strait. While occurrence records for some of the more populated sections of the coast are well known, data are patchy for more remote areas. Many species have very short lifecycles, so they can respond rapidly to changes in environmental conditions. The New South Wales coast is a recognised climate change hot-spot and southward shifts in distribution have already been documented for several species. However, thorough documentation of present distributions is an essential prerequisite for identifying further range extensions. While distribution data are available in the public realm, much is also held privately as photographic collections, diaries and logs. This paper consolidates the current occurrence data from both private and public sources as part of a broader study of sea slug distribution in south-eastern Australia and provides an inventory by region. A total of 382 species, 155 genera and 54 families is reported from the mainland coast of New South Wales.
View