Nicole Gravier-Bonnet

Hydroid nematophores: morphological, structural, and behavioural variety from old knowledge and new data

There is a rich old literature on nematothecae, which have been described from many species of nine families of thecate hydroids, but detailed knowledge of nematophores is from a very few species. Using both old data and new observations, information was gathered on species belonging to the genera Hydrodendron, Zygophylax, Antennella, Plumularia, Monotheca, Macrorhynchia, Gymnangium, and Thecocarpus. Specimens belonging to five families collected on the coral reefs of Reunion Island (SW Indian Ocean) were observed alive and videotaped to gather information on nematophores. Nematophores are classified and named here as belonging to three types. An amoeboid nematophore of the four plumularid families Kirchenpaueriidae, Halopterididae, Plumulariidae, and Aglaopheniidae usually consists of two parts, which are more separate in aglaophenids than in the others. The cnidostyle (or nematostyle) is fixed, is formed of ectoderm and endoderm, and includes a cluster of large nematocysts at its top. It is inferred to serve in defence because nematocysts inside the nematotheca can be fired when stimulated. The sarcostyle is a mobile amoeboid layer of ectoderm capable of considerable extension; those that are bilobed on top can extend in two directions at a time. The sarcostyle can emit small pseudopods on its edges that phagocytose particles at the surface of the perisarc. Its hypothesized function of cleaning the colony and providing nutrition in the form of small detrital particles and bacteria taken up by phagocytosis remains to be confirmed by experimentation. The cnidostyle-like nematophore of the Campanulinidae, Linolariidae, and Clathrozoidae is a fixed structure formed of a bilayered pedicel ending with a cluster of nematocysts able to fire while still inside the nematotheca, like the cnidostyle part of the amoeboid nematophore. It functions in defence as well. The tentacle-like nematophore of the Haleciidae and Lafoeidae, described here for the first time, is a single very extensible process provided with nematocysts that issue from the nematotheca and formed by a file of endodermal chordal cells surrounded by ectoderm. In halecids, nematocysts are not always gathered on the very top, forming what looks like a strongly capitate tentacle, as was previously thought, but can be more scattered, giving the structure a filiform appearance. This type has active movements, being able to twist and bend in all directions. Its prey capture function has not been demonstrated; a sensory function is more probable. Additional data have to be collected for more species to compare the types with more confidence, but they appear to have different origins for their considerably different morphologies, structures, and behaviour.

Swimming medusoid gonophores in two species of Sertularella (Cnidaria, Hydrozoa, Sertulariidae) from Réunion Island, Indian Ocean

Summary Two life cycle patterns predominate in thecate hydroids, those with alternating polyp and medusa stages, and those with fixed gonophores. Relatively few species release short-lived medusoids, also called swimming gonophores, that carry the gametes. In the family Sertulariidae, with its large number of taxa, this mode of metagenesis has been documented previously for only two species. It is described here for two others, Sertularella diaphana (Allman, 1885) and Sertularella n. sp., from the coastal waters of Reunion Island. Freshly collected fertile male and female colonies released medusoids near dawn, one per gonotheca. Strong contractions of the bell in the swimming movements induced the shedding of gametes. Once gametes were shed, medusoids quickly degenerated and died. The medusoids were similar morphologically in these two related species, and no obvious sexual dimorphism was noted. They were ovoid in shape, the spadix was eccentric, and a velum was present; but they lacked a mouth, tentacles, sense organs, and radial and circular canals as described earlier in Amphisbetia operculata (Linneus, 1758) and Sertularia marginata Kirchenpauer, 1864. However, the medusoids described here lacked exumbrellar nematocysts. Moreover, the spadix with its dense mass of gametes was different from all other described in being stuck from base to top on one side of the subumbrella in spite of hanging freely in the subumbrellar cavity. The hypothesis that this unusual reproductive mode in sertulariids has been underestimated is confirmed by these findings.

Phylogenetic relationships within Aglaopheniidae (Cnidaria, Hydrozoa) reveal unexpected generic diversity

Morphology can be misleading in the representation of phylogenetic relationships, especially in simple organisms like cnidarians and particularly in hydrozoans. These suspension feeders are widely distributed in many marine ecosystems, and the family Aglaopheniidae Marktanner‐Turneretscher, 1890 is among the most diverse and visible, especially on tropical coral reefs. The taxonomy of this family is based on morphological characters with emphasis on reproductive structures for the identification of genera. This study is the most comprehensive molecular phylogeny of the Aglaopheniidae to date, including six genera and 38 species, of which 13 were investigated for the first time and sampled on tropical coral reefs throughout the Indo‐Pacific region. For newly sampled individuals, we sequenced the 16S rRNA, the nuclear locus comprising the complete ITS1‐5.8S rRNA gene‐ITS2 and the first intron of the calmodulin nuclear gene. Phylogenetic analyses of the data revealed and confirmed a general polyphyly, or doubtful monophyly, of all sampled genera in tropical regions based on both the mitochondrial and nuclear markers. Our results revealed that several morphological characters used today are unsuited to resolve phylogenetic relationships between species and genera, as well as the high phyletic diversity within this family. Future revision of the classification of this family will require extensive geographic sampling and the use of an integrative approach.

Medusoid release and spawning of Macrorynchia philippina Kirchenpauer, 1872 (Cnidaria, Hydrozoa, Aglaopheniidae)

The life cycle of the aglaopheniid Macrorynchia philippina Kirchenpauer, 1872, is re-described from examination of live specimens collected from Reunion Island, Indian Ocean. Fertile colonies were collected on the outer slope of the coral reef and medusoid release happened a few hours later. Video sequences were recorded. Colonies were hermaphroditic: each phylactocarp contained one female and one male gonotheca. Sexual dimorphism was remarkable: sex could be recognized by colour, the female being red ochre, including about 40 oocytes disposed in a mosaic feature, and the male yellow ochre, having a homogeneous mass of spermatozoa. The blastostyle ran all around the gonangium near the closure of the two valves of the gonotheca, forming gubernacula. A ring of refringent corpuscles was clearly visible near the apex. Medusoids were indistinguishable inside the gonotheca. Male and female medusoids were released simultaneously at gamete maturity. Medusoid release involved the basal rupture of the blastostyle and the rupture of the links between the ectoderm surrounded the medusoid (the mantle), including the blastostyle (the mantle), and the gonothecal perisarc. While the two valves of the gonotheca were pushed and drew aside, the medusoid emerged by slipping out of the mantle that ruptured distally, forming a sheath; the bell of the medusoid did not contract. Immediately after emergence, quick and strong contractions of the bell allowed the medusoid to swim and induced spawning by breaking the ectoderm surrounding the gametic mass around the spadix. Spawning lasted only a few minutes: both oocytes and spermatozoa were expelled at each contraction. Spent medusoids remained alive only about 2 h. External fertilization gave rise to planulae 1 day later.

Cloning by releasing specialized frustules in a successful epiphytic zooxanthellate haleciid (Cnidaria, Hydrozoa, Haleciidae), with comments on stolonization and frustulation

Summary Investigations on the hydroid biodiversity of the Îles Glorieuses (Indian Ocean) were carried out during a 2-week field trip in November 2003. The coral reef flats were prospected by foot and by snorkelling at low tide from the beach to the outer reef front. Two brown algae, Turbinaria ornata and T. decurrens, were among the main seaweeds on both sides of the reef front. They were frequently covered by a zooxanthellate Halecium species, still unidentified but closely related to the Atlantic species Halecium nanum. Gonothecae of this haleciid were found only twice, but the colonies exhibited a large number of specialized frustules of a previously undescribed type, produced by budding. These propagules were located underneath the hydrothecae. They exhibited a special shape, boomerang- or tetrapod-like, with three to four branches provided with a thick ectoderm, and they detached from the parent colony. Settlement was facilitated by sticky secretions of the ectoderm around the frustule. This cloning process, occurring together with both the spreading of colonies by budding new hydranths and the occurrence of sexual reproduction, appeared to be an efficient reproductive strategy, giving rise to a large population and ensuring the success of Halecium sp. at the time of the study. Zooxanthellae are probably important to such success. Asexual reproduction by stolonization is commonly used among hydroids, whereas asexual reproduction by frustulation is scarcer. Species provided with much more specialized propagules, such as stolons in several epiphytic species, or with frustules as here described, are rare. Planktonic complex propagules, which differ in shape by including a hydranth and stolons and which are here considered a consequence of stolonization instead of frustulation, were previously described for Halecium pusillum as a reproductive process independent of environmental conditions. Specialized frustules as described here are certainly a feature of the life cycle of Halecium sp., but further investigations are needed to determine if their production is seasonally linked and if they are responsible for other than local dispersal.

Modern alongside traditional taxonomy—Integrative systematics of the genera Gymnangium Hincks, 1874 and Taxella Allman, 1874 (Hydrozoa, Aglaopheniidae)

We studied the diversity within the former genus Gymnangium in the South West Indian Ocean by using an integrative approach of both traditional (morphology-based) and modern molecular taxonomy. Nine species were recorded in the material collected. A total of 97 16S mitochondrial DNA sequences and 54 Calmodulin nuclear sequences from eight Gymnangium/Taxella species were analyzed. We found both morphological and molecular differences in the studied Gymnangium species that make it necessary to split the genus. It is proposed to revalidate the genus Taxella which is currently regarded as a synonym of Gymnangium. Two species of the genus Taxella (T. eximia and T. gracilicaulis), until now regarded as distinct species based on morphological characteristics, cluster together in one phylogenetic clade. Possible explanations are discussed. Two species from Madagascar new to science are herein described and rare species from the Indian Ocean islands are re-described.

Crustacea Decapoda of Glorieuses Islands, with notes on the distribution of the coconut crab ( Birgus latro ) in the western Indian Ocean

An inventory has been made of the decapod fauna of the Glorieuses Islands, western Indian Ocean (WIO), following the BIORECIE 2 Expedition to the Islands, 5–17 December 2012. Field data are complemented by a review of taxonomic studies for these islands. Overall 157 species are now reported from the Glorieuses Islands, including 61 new records. The presence of the coconut crab, Birgus latro , is confirmed from these islands, for the first time since 1884, and the WIO distribution of this endangered species is updated, based on observations made in the region since 2006.

The hydranth of Salacia tetracythara (Cnidaria: Hydrozoa: Sertulariidae) and its modified tentacles

Study of living colonies of Salacia tetracythara Lamouroux, 1816, led to an accurate description of the hydranths and adjoining tissues. A mantle is reported for the first time for this species, lining stem, hydrocladia and hydrotheca. An adcauline nematocyst clump located in the median part of the column, composed of large microbasic mastigophores, is also reported as a new structure for sertulariids. The hypothetical modified tentacles noted by Billard (1925) are confirmed and re-described. Among the 22-28 tentacles of the hydranth in a circlet, two exhibit nematocyst-bearing organs connected at base. These organs are massive, racket-shaped, refringent, and composed of large microbasic mastigophores. They do not affect the tentacles in respect of their general shape and behaviour. One nematocyst-bearing organ can sometimes be linked to more than one tentacle depending on its size. The abcauline position of the two modified tentacles imparts a strong bilateral symmetry to the hydranth. This location explains why only one modified tentacle was previously described from preserved material, the second being hidden by the first when hydranths are retracted inside the hydrotheca. The modified tentacles of S. tetracythara are compared with the nematodactyls of the genus Nemalecium, with the ligula found in several sertulariid species, and with nematophores described in other thecate families. Beside remarks on species taxonomy and distribution, incitation is given to the study, with emphasis especially on hydranths.

Non-released cryptomedusoid in the life cycle of Antennella sp. (Cnidaria, Hydrozoa, Halopterididae) from La Réunion, Indian Ocean

Summary Specimens of Antennella sp. were collected by scuba diving during the austral summer on the outer slope of the fringing reefs located on the western coast of La Réunion (55°30′E, 21°50′S) where the species forms microscopic colonies on red algae. A fertile colony was kept alive in a closed system in the laboratory. Like other Antennella species, it exhibits hermaproditism and sexual dimorphism: gonangia of both sexes are on the same stem, with female gonothecae being clearly bigger than male. In both sexes we observed cryptomedusoids with a subumbrellar cavity, an eccentric spadix surrounded by the gametes and a ring of refringent corpuscles on top. Male gonothecae have a compact blue-grey homogeneous mass of spermatozoa while females contain circa five white-opaque oocytes with a clearly visible darker nucleus. When the gametes were mature, one day after collection, medusoid tissues slid towards the base of the gonotheca in both sexes. Female gametes remained free inside the gonotheca while spermatozoa were liberated in the aquarium and fertilized oocytes. Several embryos at different stages of embryonic development (from morula to blastula) were incubated in a single gonotheca. The planula was not observed. This study revealed a previously undescribed pattern of sexual reproduction in the family Halopterididae involving unreleased cryptomedusoids instead of fixed sporosacs. This may be a more advanced regression stage of the medusa than free cryptomedusoids encountered in related families.