The anatomy and biology of alcyonarian-feeding aeolid opisthobranch molluscs and their development of symbiosis with zooxanthellae

The anatomy of seven species of aeolid opisthobranch molluscs is described. They are all considered to be specialized feeders on alcyonarian coelenterates and to belong to one genus Phyllodesmium (Glaucidae; Favorininae). Two species are considered to be new. Favorinus horridus Macnae, Aeolidia poindimiei Risbec, Cratena macphersonae Burn and another species not studied in this paper, Hervia serrata Baba, are transferred to Phyllodesmium from the genera in which they are currently placed. Myrrhine Bergh, Babaiella Risso-Dominguez and Phyllodesmiopsis Risso-Dominguez are considered synonyms of Phyllodesmium. The two new species feed on Xenia and P. poindimiei feeds on Telesto. It is shown that the species of Phyllodesmium exhibit an evolutionary series in the development of symbiosis with zooxanthellae. The zooxanthellae are obtained from the alcyonarians upon which the aeolids feed. Morphological peculiarities present in some members of the genus are considered to be associated with the symbiosis.     

Further studies on the anatomy and ecology of opisthobranch molluscs feeding on the scleractinian coral Pontes

Three further species of opisthobranch molluscs are reported to feed on the scleractinian coral Pontes in Tanzania. Further information on Cuthona poritophages Rudman, 1979, is also included. The anatomy of the aeolid Phestilla lugubris {Bergh, 1870, = P. sibogae Bergh, 1905) and a new species of Phestilla is described, as is the anatomy of the arminacean Pinufius rebus. The new species of Phestilla , and Pinufius , are, for the first time, reported to feed on Porites. Notes on the anatomy of the type-species of Phestilla, P. melanobrachia Bergh, 1874, are included to make possible a definition of the genus Phestilla.
Aspects of the feeding biology, life history, defence mechanisms and habitat specificity of the four Porites-feeding opisthobranchs are described and discussed. The four species are shown to have evolved radular teeth of remarkably similar shape. Each species utilizes a different part of the coral tissue as food. The three aeolids have replaced functional cnidosacs at the tip of their cerata with batteries of large secretory cells.
Phestilla lugubris and Pinufius rebus are also reported for the first time from the Great Barrier Reef, Queensland and the new species of Phestilla is reported from Queensland and Hawaii.     

Systematics and phylogeny of the caryophyllidia-bearing dorids (Mollusca, Nudibranchia), with descriptions of a new genus and four new species from Indo-Pacific deep waters

The phylogenetic relationships of the caryophyllidia-bearing dorids are studied, based on the examination of the type species of all the genera previously described. The phylogenetic hypothesis supports that the caryophyllidia-bearing dorids are a monophyletic group and the sister group of the clade formed by Astemnotus Ehrenberg, 1831 and Halgerda Bergh, 1880. Several genera previously considered as valid or regarded as uncertain are here synonymized: Peronodoris Bergh, 1904, Trippa Bergh, 1877, Phlegmodoris Bergh, 1878, Petelodoris Bergh, 1881, Kentrodoris Bergh, 1876, Audura Bergh, 1878, Centrodoris P. Fischer, 1883, Anisodoris Bergh, 1898, Awuka Er. Marcus, 1955, Rhabdochiia P. Fischer, 1883, Boreodoris Odhner, 1939, Dictyodoris Bergh, 1880, Gravieria Vayssiere, 1912, Aporodoris Ihering, 1886. The following genera are regarded as valid: Astemnotus, Atagema J.E. Gray, 1850, Jorunna Bergh, 1876, Platydoris Bergh, 1877, Diaulula Bergh, 1878, Rostanga Bergh, 1879, Halgerda Bergh, 1880, Baptodoris Bergh, 1884, Gargamella Bergh, 1894, Alloiodoris Bergh, 1904, Sclerodoris Eliot, 1904, Taringa Er. Marcus, 1955, Thorybopus Bouchet, 1977. The new genus Nophodoris is described based on two new species from New Caledonia deep waters. Two additional new species from New Caledonia belonging to the genera Atagema and Gargamella are also described. Nomenclatural and taxonomic problems are discussed, and several type species, neotypes and lectotypes are selected.     

PROTAEOLIDIELLA ATRA BABA, 1955 AND PLEUROLIDIA JULIAE BURN, 1966; ONE SPECIES, TWO FAMILIES (NUDIBRANCHIA)

The aeolid nudiberanch species Protaeolidiella atra Baba, 1955and Pleurolidia juliae Burn, 1966, sole species of the familiesProtaeolidiellidae and pleurolidiidae respectively, are shownto be conspecific. The apparent ‘primitive’ featuresof their morphology are re-examined and reinterpreted and itis suggested that the species is a member of the Fomily Aeolidiidae.Unlike other members of the family, which all feed on anthozoans,this species is highly specialised for feeding on the hydroidSolanderia fusca. The single species is shown to have a wideIndo-west Pacific distribution. Functional extra-ceratal lobesof the digestive gland are reported for the first time, froman aeolid without zooxanthellae symbiosis. (Received 4 October 1989; accepted 23 December 1989)     

A phylogenetic analysis and systematic revision of the cryptobranch dorids (Mollusca, Nudibranchia, Anthobranchia)

The phylogenetic relationships of the cryptobranch dorids are studied based on morphological characters of species belonging to all previously described genera. The phylogenetic hypothesis supports the cryptobranch dorids as a monophyletic group. There are two major clades within the Cryptobranchia: the radula‐less dorids (Porostomata), and the radula‐bearing dorids ( Labiostomata new taxon ). Labiostomata consists of those taxa sharing a more recent common ancestor with Actinocyclus than with Mandelia, and includes several monophyletic groups: Actinocyclidae, Chromodorididae, Dorididae and Discodorididae. The traditional group Phanerobranchia is probably paraphyletic. The new classification proposed for the Cryptobranchia addresses concepts of phylogenetic nomenclature, but is in accordance with the rules of the International Code of Zoological Nomenclature. The following genera of cryptobranch dorids are regarded as valid: Doris Linnaeus, 1758, Asteronotus Ehrenberg, 1831, Atagema J. E. Gray, 1850, Jorunna Bergh, 1876, Discodoris Bergh, 1877, Platydoris Bergh, 1877, Thordisa Bergh, 1877, Diaulula Bergh, 1878, Aldisa Bergh, 1878, Rostanga Bergh, 1879, Aphelodoris Bergh, 1879, Halgerda Bergh, 1880, Peltodoris Bergh, 1880, Hoplodoris Bergh, 1880, Paradoris Bergh, 1884, Baptodoris Bergh, 1884, Geitodoris Bergh, 1891, Gargamella Bergh, 1894, Alloiodoris Bergh, 1904, Sclerodoris Eliot, 1904, Otinodoris White, 1948, Taringa Er. Marcus, 1955 , Sebadoris Er. Marcus & Ev. Marcus, 1960, Conualevia Collier & Farmer, 1964, Thorybopus Bouchet, 1977, Goslineria Valdés, 2001, Pharodoris Valdés, 2001, Nophodoris Valdés & Gosliner, 2001. Several genera previously considered as valid are here regarded as synonyms of other names: Doridigitata d’Orbigny, 1839, Doriopsis Pease, 1860, Staurodoris Bergh, 1878, Fracassa Bergh, 1878, Archidoris Bergh, 1878, Anoplodoris Fischer, 1883, Etidoris Ihering, 1886, Phialodoris Bergh, 1889, Montereina MacFarland, 1905, Ctenodoris Eliot, 1907, Carryodoris Vayssière, 1919, Austrodoris Odhner, 1926, Guyonia Risbec, 1928, Erythrodoris Pruvot‐Fol, 1933, Neodoris Baba, 1938, Siraius Er. Marcus, 1955, Tayuva Ev. Marcus & Er. Marcus, 1967, Nuvuca Ev. Marcus & Er. Marcus, 1967, Doriorbis Kay & Young, 1969, Pupsikus Er. Marcus & Ev. Marcus, 1970, Percunas Ev. Marcus, 1970, Verrillia Ortea & Ballesteros, 1981 . The genera Artachaea Bergh, 1882, Carminodoris Bergh, 1889 and Homoiodoris Bergh, 1882 have been poorly described and no type material is known to exist. They are regarded as incertae sedis until more material becomes available. The genus names Xenodoris Odhner in Franc, 1968 and Cryptodoris Ostergaard, 1950 are unavailable within the meaning of the Code. Hexabranchus Ehrenberg, 1831 is not a cryptobranch dorid, as suggested by other authors, because of the lack of a retractile gill. Other nomenclatural and taxonomic problems are discussed, and several type species, neotypes and lectotypes are selected. © 2002 The Linnean Society of London. Zoological Journal of the Linnean Society, 2002, 136 , 535?636.     

On some species of Chelidonura (Opisthobranchia:Aglajidae) from Zanzibar and Fiji

The anatomy of specimens of Chelidonura philinopsis Eliot, 1903 and a new species of Chelidonura collected in Zanzibar, are described. Preserved specimens of Chelidonura, from Fiji, most probably C. varians Eliot, 1903 (=C. velutina Bergh, 1905) are discussed. Chelidonura philinopsis is compared with C. hirundinina {Quoy & Gaimard, 183 2) and it is suggested that at this stage they should remain as distinct species. C. punctata Eliot, 1903, the other species of the genus recorded from Zanzibar, is compared with two similarly coloured species from Japan, C. fulvipunctata, Baba, 1938 and C. tsurugensis, Baba & Abe, 1959.
The species suggest that the structure of the alimentary canal and the reproductive system (excluding the penis) are constant within the genus.     

Aeolid opisthobranch molluscs (Glaucidae) from the Indian Ocean and the south-west Pacific

Eight aeolid opisthobranch molluscs of the subfamilies Facelininae, Favorininae, and Herviellinae are reported from Tanzanian waters, and two species from Northwestern India. New records from Queensland, Australia greatly extend the range of two species reported from Tanzania. Phidiana militaris (Alder & Hancock) and P. indica (Bergh) are shown to be distinct and a species from New Zealand, originally identified as P. militaris , is shown to be new. P. bourailli (Risbec), previously reported only from New Caledonia, is described from Tanzania, as is a new species of Phidiana. Favorinus japonicus Baba is reported from Tanzania, the first published record outside Japan, a new species of Godiva is described from Tanzania and Queensland, and three new species of Sakuraeolis are described, one from India and two from Tanzania. A new species of Herviella is described from Tanzania.     

Here be dragons – phylogeography of Pteraeolidia ianthina (Angas, 1864) reveals multiple species of photosynthetic nudibranchs (Aeolidina: Nudibranchia)

The aeolid Pteraeolidia ianthina (Angas, 1864) is a strikingly‐coloured aeolid nudibranch, informally known as the ‘Blue Dragon’. It is recognised as an unusually widespread Indo‐Pacific species, with variation in colouration and morphology, and biogeographic differences in zooxanthellae (dinoflagellate symbionts of the genus Symbiodinium). This variation hints at possible cryptic species, which was tested here using phylogenetic analyses of mitochondrial DNA data (COI, 16S). Our results showed multiple well‐supported clades with slight but consistent differences in radular morphology and colouration, and thus we clarify one of the three available names. A temperate NSW clade showed a more elongate and pointed central radular tooth and lacked white body colouration, in comparison to a more variable tropical clade, which had a shorter and more blunt central tooth. The type locality of Pteraeolidia ianthina is Sydney Harbour, New South Wales (NSW), Australia, and according to our study, does not occur outside NSW. Pteraeolidia semperi (Bergh, 1870) and P. scolopendrella (Risbec, 1928) are removed from synonymy with P. ianthina. Wider phylogeographic sampling is required before resolving the availability of the two remaining names, and subclades within the tropical clade, but there is evidence to suggest multiple cryptic species exist. The biogeographic differences in symbionts, and the importance of their role in life history, suggests that changes in symbiosis may have helped drive divergence via local adaptation in the host nudibranchs. © 2015 The Linnean Society of London     

Molecular phylogeny and evolution of symbiosis in a clade of Indopacific nudibranchs

Previous efforts at understanding the evolution of the genus Phyllodesmium, based on morphological analyses, have been plagued by poorly supported phylogenies (Ortiz and Gosliner, 2008; Moore and Gosliner, 2009, in press). It has been suggested (Moore and Gosliner, 2009) that a molecular phylogeny might provide more insight into this history than can be easily discovered using morphological data. In this study, 658bp of the cytochrome c oxidase subunit I gene (CO1), 441bp of the mitochondrial large ribosomal subunit (16S) gene, and 328bp of a protein-coding nuclear gene (histone 3) were sequenced for 18 species of Phyllodesmium and six outgroup species. A total of 464 parsimony informative sites were used for parsimony, maximum likelihood, and Bayesian inference of phylogeny analyses. All three analyses produced similar topologies, with the exception of a single difference within the parsimony analysis. Bootstrap values and posterior probabilities provided strong support at many shallow nodes, and the monophyly of Phyllodesmium was supported in every case. Three distinct clades of Phyllodesmium are evident in this analysis. One of these represents the majority of asymbiotic taxa. Phyllodesmium poindimiei, an asymbiotic species, is clearly a member of a symbiotic clade and appears to have secondarily lost its symbiotic relationship with zooxanthellae. There was moderate support confirming similar topological trends seen in earlier morphological phylogenies, including the hypothesis that symbiotic species associating with zooxanthellae have evolved more recently than non-symbiotic species. Despite the inclusion of a presumably conservative nuclear locus, some deep nodes are still unresolved or are not well supported. Future inclusion of additional taxa and more slowly evolving loci will likely improve resolution of these deeper nodes. The subsequent phylogeny supports previous hypotheses by Rudman (1991), Kempf (1991) and Burghardt et al. (2008b) that evolution of more complex digestive gland structures is related to increased complexity of symbiosis with zooxanthellae and greater efficiency of photosynthetic activity. Our phylogeny also demonstrates that this symbiosis has evolved only once in Phyllodesmium and that azooxanthellate species are sister, rather than basal, to zooxanthellate species.     

Untangling the Spurilla neapolitana (Delle Chiaje, 1841) species complex: a review of the genus Spurilla Bergh, 1864 (Mollusca: Nudibranchia: Aeolidiidae)

Spurilla neapolitana (Delle Chiaje, 1823) was considered to be a species with a broad geographic range and substantial colour variability; however, analyses of mitochondrial and nuclear gene data revealed that it is a complex of five distinct species. Further anatomical and morphological examinations determined that coloration is one of the main diagnostic traits for all five species, although some display substantial colour pattern variation. As a result of this study, S. neapolitana is determined to be restricted to the Mediterranean and eastern Atlantic. Spurilla sargassicola Bergh, 1871 from the Caribbean is redescribed and confirmed as a valid species. The name Spurilla braziliana MacFarland, 1909 is retained for western Atlantic and Pacific populations. Two new species are described herein. S purilla onubensis sp. nov. occurs in Europe, with a range overlapping that of S. neapolitana. Finally, S purilla dupontae sp. nov. is found in the Bahamas. © 2014 The Linnean Society of London     

FURTHER STUDIES ON THE TAXONOMY AND BIOLOGY OF THE OCTOCORAL-FEEDING GENUS PHYLLODESMIUM EHRENBERG, 1831 (NUDIBRANCHIA: AEOLIDOIDEA)

The aeolid nudibranch genus Phyllodesmium (Mollusca: Gastropoda)is reviewed, three new species are described and further informationon the biology, anatomy and distribution on the eight previouslyknown species is reported. The genus Ennoia Bergh, 1896 is considereda synonym of Phyllodesmium and the type species Ennoia briareusredescribed. The genus Phyllodesmium is unique amongst the aeolidsin feeding on octocoral cnidarians. This has led to the evolutionof nudibranch- zooxanthellae symbioses, zooanthellae being obtainedfrom the octocoral prey. The adaptations developed throughoutthe genus are described and possible relationships between thespecies proposed. (Received 6 January 1990; accepted 20 May 1990)     

Interspecific comparison of the symbiotic relationship in corals with high and low rates of bleaching-induced mortality

Some coral species are more resistant than others to environmental factors that cause bleaching and bleaching-related mortality. This study compared aspects of the coral/zooxanthellae symbiosis in species and genera that suffered either high or low mortality during a bleaching event. These characteristics were assessed in Okinawa between March and June 1999, 5-10 months after the bleaching event there in August-September 1998. Species with low mortality rates generally had higher densities of zooxanthellae per square centimeter and a very low rate of release of degraded zooxanthellae. Low-mortality species also had more total coral tissue per square centimeter of coral surface area. The size of zooxanthellae varied little among species. The differences in these characteristics among coral species suggest that the symbiotic relationship operates very differently among coral species.     

Symbiosis-dependent gene expression in coral–dinoflagellate association: cloning and characterization of a P-type H+-ATPase gene

We report the molecular cloning of a H⁺-ATPase in the symbiotic dinoflagellate, Symbiodinium sp. previously suggested by pharmacological studies to be involved in carbon-concentrating mechanism used by zooxanthellae when they are in symbiosis with corals. This gene encodes a protein of 975 amino acids with a calculated mass of about 105 kDa. The structure of the protein shows a typical P-type H⁺-ATPase structure (type IIIa plasma membrane H⁺-ATPases) and phylogenetic analyses show that this new proton pump groups with diatoms in the Chromoalveolates group. This Symbiodinium H⁺-ATPase is specifically expressed when zooxanthellae are engaged in a symbiotic relationship with the coral partner but not in free-living dinoflagellates. This proton pump, therefore, could be involved in the acidification of the perisymbiotic space leading to bicarbonate dehydration by carbonic anhydrase activity in order to supply inorganic carbon for photosynthesis as suggested by earlier studies. To our knowledge, this work provides the first example of a symbiosis-dependent gene in zooxanthellae and confirms the importance of H⁺-ATPase in coral–dinoflagellate symbiosis.     

Diversity of algal endosymbionts (zooxanthellae) in octocorals: the roles of geography and host relationships

The presence, genetic identity and diversity of algal endosymbionts (Symbiodinium) in 114 species from 69 genera (20 families) of octocorals from the Great Barrier Reef (GBR), the far eastern Pacific (EP) and the Caribbean was examined, and patterns of the octocoral-algal symbiosis were compared with patterns in the host phylogeny. Genetic analyses of the zooxanthellae were based on ribosomal DNA internal transcribed spacer 1 (ITS1) region. In the GBR samples, Symbiodinium clades A and G were encountered with A and G being rare. Clade B zooxanthellae have been previously reported from a GBR octocoral, but are also rare in octocorals from this region. Symbiodinium G has so far only been found in Foraminifera, but is rare in these organisms. In the Caribbean samples, only Symbiodinium clades B and C are present. Hence, Symbiodinium diversity at the level of phylogenetic clades is lower in octocorals from the Caribbean compared to those from the GBR. However, an unprecedented level of ITS1 diversity was observed within individual colonies of some Caribbean gorgonians, implying either that these simultaneously harbour multiple strains of clade B zooxanthellae, or that ITS1 heterogeneity exists within the genomes of some zooxanthellae. Intracladal diversity based on ITS should therefore be interpreted with caution, especially in cases where no independent evidence exists to support distinctiveness, such as ecological distribution or physiological characteristics. All samples from EP are azooxanthellate. Three unrelated GBR taxa that are described in the literature as azooxanthellate (Junceella fragilis, Euplexaura nuttingi and Stereonephthya sp. 1) contain clade G zooxanthellae, and their symbiotic association with zooxanthellae was confirmed by histology. These corals are pale in colour, whereas related azooxanthellate species are brightly coloured. The evolutionary loss or gain of zooxanthellae may have altered the light sensitivity of the host tissues, requiring the animals to adopt or reduce pigmentation. Finally, we superimposed patterns of the octocoral-algal symbiosis onto a molecular phylogeny of the host. The data show that many losses/gains of endosymbiosis have occurred during the evolution of octocorals. The ancestral state (azooxanthellate or zooxanthellate) in octocorals remains unclear, but the data suggest that on an evolutionary timescale octocorals can switch more easily between mixotrophy and heterotrophy compared to scleractinian corals, which coincides with a low reliance on photosynthetic carbon gain in the former group of organisms.     

The adaptive bleaching hypothesis: experimental tests of critical assumptions

Coral bleaching, the loss of color due to loss of symbiotic zooxanthellae or their pigment, appears to be increasing in intensity and geographic extent, perhaps related to increasing sea surface temperatures. The adaptive bleaching hypothesis (ABH) posits that when environmental circumstances change, the loss of one or more kinds of zooxanthellae is rapidly, sometimes unnoticeably, followed by formation of a new symbiotic consortium with different zooxanthellae that are more suited to the new conditions in the host's habitat. Fundamental assumptions of the ABH include (1) different types of zooxanthellae respond differently to environmental conditions, specifically temperature, and (2) bleached adults can secondarily acquire zooxanthellae from the environment. We present simple tests of these assumptions and show that (1) genetically different strains of zooxanthellae exhibit different responses to elevated temperature, (2) bleached adult hosts can acquire algal symbionts with an apparently dose-dependent relationship between the concentration of zooxanthellae and the rate of establishment of the symbiosis, (3) and finally, bleached adult hosts can acquire symbionts from the water column.     

Evolutionary transitions in symbioses: dramatic reductions in bathymetric and geographic ranges of Zoanthidea coincide with loss of symbioses with invertebrates

Two fundamental symbiosis‐based trophic types are recognized among Zoanthidea (Cnidaria, Anthozoa): fixed carbon is either obtained directly from zooxanthellae photosymbionts or from environmental sources through feeding with the assistance of host‐invertebrate behaviour and structure. Each trophic type is characteristic of the suborders of Zoanthidea and is associated with substantial distributional asymmetries: suborder Macrocnemina are symbionts of invertebrates and have global geographic and bathymetric distributions and suborder Brachycnemina are hosts of endosymbiotic zooxanthellae and are restricted to tropical photic zones. While exposure to solar radiation could explain the bathymetric asymmetry it does not explain the geographic asymmetry, nor is it clear why evolutionary transitions to the zooxanthellae‐free state have apparently occurred within Macrocnemina but not within Brachycnemina. To better understand the transitions between symbiosis‐based trophic types of Zoanthidea, a concatenated data set of nuclear and mitochondrial nucleotide sequences were used to test hypotheses of monophyly for groups defined by morphology and symbiosis, and to reconstruct the evolutionary transitions of morphological and symbiotic characters. The results indicate that the morphological characters that define Macrocnemina are plesiomorphic and the characters that define its subordinate taxa are homoplasious. Symbioses with invertebrates have ancient and recent transitions with a general pattern of stability in host associations through evolutionary time. The reduction in distribution of Zoanthidea is independent of the evolution of zooxanthellae symbiosis and consistent with hypotheses of the benefits of invertebrate symbioses, indicating that the ability to persist in most habitats may have been lost with the termination of symbioses with invertebrates.     

Temperate and tropical algal-sea anemone symbioses

Abstract. In this review, we seek to develop new insights about the nature of algal‐sea anemone symbioses by comparing such associations in temperate and tropical seas. Temperate seas undergo pronounced seasonal cycles in irradiance, temperature, and nutrients, while high irradiance, high temperature, and low nutrients are seasonally far less variable in tropical seas. We compare the nature of symbiosis between sea anemones (= actinians) and zooxanthellae (Symbiodinium spp.) in both regions to test tropical paradigms against temperate examples and to identify directions for future research. Although fewer anemone species are symbiotic in temperate regions, they are locally dominant and ecologically important members of the benthic community compared to the tropics. Zooxanthella densities tend to be lower in temperate anemones, but data are limited to a few species in both temperate and tropical seas. Zooxanthella densities are far more stable over time in temperate anemones than in tropical anemones, suggesting that temperate symbioses are more resistant to fluctuations in environmental parameters such as irradiance and temperature. Light‐saturated photosynthetic rates of temperate and tropical zooxanthellae are similar, but temperate anemone hosts receive severely reduced carbon supplies from zooxanthellae during winter months when light is reduced. Symbiont transmission modes and specificity do not show any trends among anemones in tropical vs. temperate seas. Our review indicates the need for the following: (1) Investigations of other temperate and tropical symbiotic anemone species to assess the generality of trends seen in a few “model’ anemones. (2) Attention to the field ecology of temperate and tropical algal‐anemone symbioses, for example, how symbioses function under seasonally variable environmental factors and how zooxanthellae persist at high densities in darkness and winter. The greater stability of zooxanthella populations in temperate hosts may be useful to understanding tropical symbioses in which bleaching (loss of zooxanthellae) is of major concern. (3) Study of the evolutionary history of symbiosis in both temperate and tropical seas. Continued exploration of the phylogenetic relationships between host anemones and zooxanthella strains may show how and why zooxanthellae differ in anemone hosts in both environments.