CNIDARIA, SCYPHOZOA) M Hingston, G Jarms, H Zibrowius
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THE ECOLOGY AND PHYLOGENY OF THE MEDITERRANEAN NAUSITHOIDAE (CNIDARIA, SCYPHOZOA) M Hingston, G Jarms, H Zibrowius To cite this version: M Hingston, G Jarms, H Zibrowius. THE ECOLOGY AND PHYLOGENY OF THE MEDITER- RANEAN NAUSITHOIDAE (CNIDARIA, SCYPHOZOA). Vie et Milieu / Life & Environment, Ob- servatoire Océanologique - Laboratoire Arago, 2007, pp.67-74. hal-03234921 HAL Id: hal-03234921 https://hal.sorbonne-universite.fr/hal-03234921 Submitted on 25 May 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. VIE ET MILIEU - LIFE AND ENVIRONMENT, 2007, 57 (1/2) : 67-74 THE ECOLOGY AND PHYLOGENY OF THE MEDITERRANEAN NAUSITHOIDAE (CNIDARIA, SCYPHOZOA) M. C. HINGSTON 1, G. JARMS 1*, H. ZIBROWIUS 2 1 Zoologisches Institut und Zoologisches Museum, Universität Hamburg, Martin Luther King Platz 3, 20146 Hamburg, Germany Present address: University of Auckland, School of Biological Science, Private Bag 92019, Auckland 1142, New Zealand 2 CNRS UMR6540-DIMAR, Centre d'Océanologie de Marseille, Station Marine d'Endoume, Rue Batterie des Lions, 13007 Marseille, France Corresponding author: [email protected] SCYPHOZOA A B S T R A C T. – Coronates occur in all oceans from coastal to abyssal waters. In the Mediter- CORONATAE ranean, three of the six local nausithoid species inhabit marine caves. They have a reduced NAUSITHOIDAE PHYLOGENY pelagic life stage in common, which presumably offers them advantages in cave or shallow MARINE CAVES water habitats, though the mechanisms diff e r. Within that small number of species, apogamy, parthenogenesis, hermaphrodity and brood care are encountered. In this study, knowledge of habitat and ecology of the Mediterranean Nausithoidae is compiled and the relationships of the species are investigated through a combined approach of morphological and molecular charac- ter analysis. Three clades are evidenced. These results are corroborated by studies of the life cycles and observations on the behaviour. INTRODUCTION photic zone, and a low level of hydrodynamic agitation. Knowledge of solitary nausithoid polyps as part of the There are an estimated 50 species belonging to the cave fauna is necessarily younger than that of deep-water Coronatae (Scyphozoa), the Nausithoidae (Bigelow, 1913) occurrences revealed by dredging and dates back to this being one of the six families. The family Nausithoidae period. The relative abundance of solitary stephanoscy- includes the genera Na u s i t h o e (K ö l l i k e r , 1853), Pa l e p h y r a phistomae in semi-obscure caves in the Marseille region (Haeckel, 1880) and T h e c o s c y p h u s ( We r n e r, 1980). T h e was discovered by Zibrowius during dives in 1964. These life cycle of Scyphozoa is an example of metagenesis and forms were first identified, tentatively, as S t e p h a n o s c y - typically consists of an alternation between a sessile, asex- phus simplex, but soon recognised by Werner as distinct ual polyp generation and a mobile, sexual medusa genera- forms leading to several trips to Marseille where live tion. Various alterations are derived from typical metagen- material was collected for him. Werner was the first who, esis. Of the eight species of Coronatae presently known in by rearing experiments, noticed the peculiar reductions in the Mediterranean, the holopelagic Periphylla periphylla the species’ lifecycles. Cave or coastal habitats of the has no polyp at all (Jarms et al. 1999) while the life cycle Mediterranean scyphistomae seem to be linked to an of Paraphyllina ransoni is still unknown (Jarms 2003). A emphasis on the polyp generation during metagenesis. further six species are assigned to the Nausithoidae. Whether or not the reduction of the medusae signifies Nausithoe punctata, N. werneri and N. marg i n a t a a l l a general trend in species found in marine caves, and how exhibit a typical metagenesis (Thiel 1936, Jarms 1990), often it occurred, on multiple occasions or only once, are but N. planulophora is apogamous, producing planuloids the actual questions. These questions can be expected to instead of ephyrae (Werner 1971, Werner 1983, Werner & be answered by examining the relations between species Hentschel 1983). Thecoscyphus zibrow i i is parthenogenet- with a complete metagenesis and those with a reduced life ic (Sötje 1998, Jarms & Sötje 1999). The hermaphroditic cycle. The systematic classification of the Coronatae is eumedusoids produced during strobilation in N. eumedu - l a rgely based on morphological characters, but, because s o i d e s remain attached to the strobila (Werner 1974). T h e of their simple morphology (Jarms 1991, 2002), they species with reduced life cycles were all found in marine have few morphological characters useful for analysis. caves. We therefore also use life cycle data and molecular mark- Autonomous diving techniques, having become more ers. Elsewhere, the latter have proven useful in cases and more widely employed by marine biologists since the where traditional phylogenetic reconstruction did not pro- 1950s and 60s, sparked an intense interest in the fauna of vide any solution (Bridge et al. 1995). A c o m b i n e d submarine caves with concomitant special attention being approach through a morphological character analysis and paid to similarities between cave and bathyal ecosystems a molecular analysis of the 5’ end of the 28s rDNA w a s (Harmelin et al. 1985, Vacelet et al. 1994): the absence of carried out. The results are compared to data on the light, low importation flux of organic matter from the species ecology. 68 M. C. HINGSTON, G. JARMS, H. ZIBROWIUS MATERIALAND METHODS group, but due to the close molecular grouping with the species N. marg i n a t a a more remote outgroup species was subsequently The specimens were collected by Zibrowius (since 1964), found in Ti b u ronia granro j o (Semaeostomeae, Ulmaridae, Gen- Werner (1975), Jarms (1981) and Sötje (2000). All species were bank accession number AY149900). kept alive at the Hamburg University following the protocols The alignment was carried out manually using GeneDoc developed by Werner (1971) and revised by Jarms (2002). Fur- (Nicholas et al. 1997). Parsimony informative sites were located ther material for morphological analysis was obtained from the with DnaSP (Rozas et al. 2003). Phylogenetic analyses of the Zoological Museum of the University of Hamburg. Ecological sequences were conducted with Mega2 (Kumar et al. 1 9 9 3 ) data were provided by Zibrowius who collected most of the using the distance method based on Tamura and Nei (1993). specimens. For the evaluation of the species morphology, a list Maximum parsimony, neighbour joining and minimum evolu- of known characters was compiled and used in the analysis. tion trees were generated. Bootstrap sequences were generated These characters include the shape of the chitinous exoskeleton, to test branch support (Felsenstein 1985). A network was creat- as described by the ratio of diameter to the length of the tube, ed using the split decomposition method (Bandelt & Dress termed “Formquotient” by Jarms (1991). The Formquotient at 1992) of the program Splits Tree (Huson 1996). It allowed for two and five mm tube length was used as a character state for the concurrent presentation of more than one possible means of the specific growth pattern of the polyps (with the exception of branching, thus coherent data were shown as a tree while uncer- N. punctata, which exhibits colonial growth). The structure of tain data were given as a wide network (Page & Holmes 1998). the outer tube layer varied, the presence or absence of stripes was defined as a character state. The teeth were also used to Table I. - List of morphological characters used for the phyloge- define characters, v i a their presence or absence as well as their netic analysis of the Mediterranean Nausithoidae. n u m b e r. Lamellar thickenings of the inner wall were considered 1 – Formquotient at 2 mm: 0: larger or equal to 0.2, 1: smaller as another character. The soft body of the polyp had few charac- than 0.2, ?: indistinguishable due to colonial growth pattern. ters, only the maximal number of tentacles was used in this 2 – Formquotient at 5 mm: 0: larger or equal to 0.2, 1: smaller study. The observed processes of strobilation offered more char- than 0.2, ?: indistinguishable due to colonial growth pattern. acter states. Ephyra characters included the occurrence or 3 – Structure of outer layer of tube: 0: regularely structured absence of tentacles. Medusae characters were defined by the with perpendicular vertical and horizontal marks, 1: modi- occurrence of rhopalia, the shape of the manubrium and the fied outer structure. number and origin of gonads. A complete list of the characters is 4 – Existence of tooth whorl: 0: with tooth whorl, 1: without given in Table I. The morphological analysis was carried out tooth whorl. with A t o rella vanhoeffeni (Coronatae, Atorellidae) as outgroup. 5 – Number of teeth in whorl: 0: 8 teeth, 1: 16 teeth, ?: without The defined characters where incorporated into an unweighted tooth whorl. matrix. Missing characters were treated as neutral. The matrix 6 – Surface teeth on whorl: 0: few to None, 1: many, ?: without was analysed using a maximum parsimony method within the tooth whorl.