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Change from Planktonic to Benthic Development : Is Life OCEANOLOGICA ACTA- VOL. 19- W 3-4 ~ -----~- Polychaeta Change from planktonic Terebellidae Life cycles Dispersal to benthic development: Structures of retention Evolution is life cycle evolution an adaptive Polychètes Térébellidae Cycle de vie answer to the constraints of dispersal? Dissémination Structures de rétention Evolution Michel BHAUD and Jean-Claude DUCHÊNE Observatoire océanologique, Université Paris VI - Pierre et Marie Curie, Laboratoire Arago, BP 44, 66651 Banyuls-sur-mer Cedex, France. Received 30/03/95, in revised form 23/10/95, accepted 14/11/95. ABSTRACT Current research on recruitment of benthic marine invertebrates is, to a large extent, concemed with the consequences of larval planktonic development in water masses entailing dispersal, a milieu which appears unfavourable for a suc­ cessful recruitment. In this paper, the origin of benthic development is tentatively considered as a response to the constraints of dispersal. Examples among annelid polychaetes are taken from persona! work and from the literature. i) Life cycles in the subantarctic area provide good indications of a correlation between direct development and environmental pressure enhancing dispersal (due to turbulence and advection which would carry the planktonic larvae away from a suitable habitat). ii) Experimental analysis of the li fe cycle of Eupolymnia nebulosa in the Mediterranean shows that gelatinous egg masses reduce the ability of larvae to spread and consequently increase retention in areas more suitable for the adults. iii) Examination of a large number of geographie sites where a very reduced habitat area is reported indicates that developmental patterns may involve weak dispersal to secure the return of Iarvae. From an evolutionary point of view, the direction of the transformation of life cycle patterns in the polychaete class may be inferred from the large number of solutions adopted by benthic development. The observations suggest that this pattern is derived. The case of E. nebulosa, which exhibits two developmental strategies, suggests also that the direct deve­ lopment found in populations of the Mediterranean Sea is a derived condition from the free development found elsewhere e.g. the English Channel. Evolution from benthopelagic development to benthic development is frequent, yet the reversion to planktonic development is also observed. We suggest that changes in the physical conditions of the environment disrupt and modify the life cycle; these unbalanced conditions may occur several times over the course of the evo­ lution of a family. RÉSUMÉ Du développement planctonique au développement benthique : l'évolution des cycles de vie est-elle une réponse aux contraintes de dissémination ? Les recherches actuelles sur le recrutement s'appliquent pour une large part aux conséquences du développement larvaire planctonique dans un milieu dispersif qui apparaît négatif pour un recrutement satisfaisant. A l'échelle de temps évolu­ tive, ce couplage soulève la question de l'origine du développement benthique. On tente de montrer que ce type de développement chez les annélides polychètes est considéré comme une réponse aux contraintes de dissémination. Pour cette 335 M. BHAUD, J.-C. DUCHÊNE démonstration on examine plusieurs situations tirées de nos propres travaux et de la littérature. a) Les cycles de vie de la province subantarctique fournissent une bonne corrélation entre le développement direct prédominant et les forces de dis­ sémination extrêmement prononcées. b) L'analyse du cycle de vie de Eupolym­ nia nebulosa permet de démontrer que les masses gélatineuses contenant les larves réduisent la capacité de dissémination de ces larves et empêchent la colo­ nisation sur des zones défavorables au maintien des adultes. c) L'examen d'un ensemble d'espèces, caractérisées par une surface d'habitat très réduite, indique la nécessité d'une faible dissémination. Du point de vue évolutif, la direction de la transformation du type de développement peut être identifiée. A l'échelle de la classe des Polychètes, le grand nombre de solutions adoptées par le développe­ ment direct suggère une origine secondaire de ce mode de développement. Le cas particulier fourni par E. nebulosa avec deux stratégies de développement, suggère que le contrôle des larves en Méditerranée est dérivé par rapport au développement libre connu sur tout le reste de l'aire spécifique. Cependant cette direction d'évolution n'est probablement pas unique. Le retour vers le dévelop­ pement benthoplanctonique est aussi observé et l'on suggère que les variations des conditions physiques de l'environnement peuvent briser le cycle de vie et le modifier. Ce déséquilibre peut se produire plusieurs fois et dans des directions différentes au cours de la vie de la lignée familiale. OceanologicaActa, 1996, 19,3-4,335-346. INTRODUCTION tand geographical population patterns and levels of recroît• ment. There are divergent views on the advantages/disad­ Among marine invertebrates, three spatially defined modes vantages of dispersal during the larval phase of benthic of development are generally recognized: benthoplankto­ species. Palmer and Strathmann ( 1981) state that feeding nic, holoplanktonic and holobenthic. The benthoplanktonic larvae living simultaneously in the plankton receive little if pattern takes place in two ecosystems: the plankton and the any advantage from an increased scale of dispersal. benthos; the transfer from one to the other occurs with an Grahame and Branch ( 1985) after examining a variety of ontogenetic transformation, namely metamorphosis. Such opinions on the utility of the planktonic period state that "complex life cycles" (Sinclair, 1988) are widespread in with ali these contrasting views, the significance of the dis­ marine systems where approximately 80 % of species exhi­ persal phase linked with pelagie development remains pro­ bit a life cycle that includes a thorough metamorphosis, blematic. Sinclair ( 1988) offers good arguments that reten­ often accompanied by a spatial transfer. Severa! conditions tion by physical oceanographie processes is a matter of are required for a complex life cycle to occur and to ensure selection rather than of dispersal. Roughgarden ( 1989) the perpetuity of the species. Constraints fall into two large argues that if dispersal were the paramount factor in a life categories: those developed in time relative to the different cycle, one would expect the dispersal to be carried out by steps of ontogenesis (Bhaud, 1994); and those linked with the adult when development is benthic. space. In this paper we will deal with this second kind of If physical oceanographie processes create conditions for constraint. Sorne difficulties concerning the achievement successful reproduction, it is of interest to investigate, on of bentho-planktonic life cycles can be expected, as deve­ the evolutionary time scale, the possible selective pressures lopment must alternate between two different ecosystems. of advection and mixing. Most discussions on evolution of Though advection and turbulence of water masses can be life cycles concern strategies developed only by species efficient in spreading passive larvae, these conditions can that are benthic when adult. Holoplanktonic cycles are also be dangerous to the larvae as they may be carried generally neglected (Chia, 1976; Cazaux, 1981; Jablonski away from a suitable habitat; to ensure adult survival, the and Lutz, 1983; Bhaud, 1994; Mileikovsky, 1971, 1976; larvae must reach a suitable benthic environment. In Scheltema, 1989). More often, the problem is limited to the contrast, holoplanktonic or holobenthic development energy requirements in terms of egg size and storage occurs in only one ecosystem. Species adopting these pat­ content for species with contrasting life cycles. Environ­ terns do not need to change from one ecosytem to another mental conditions relative to spatial constraints are neglec­ to complete their life cycle; thereby they avoid the quest ted. Another complication is that observed strategies are for a suitable environment. assumed to have emerged from an ancestral life history Many papers deal with biological-physical interactions (as pattern. The prevailing opinion is that the benthoplanktonic summarized in Mann and Lazier, 1991; Rothschild, 1988) developmental pattern is probably the ancestral condition and especially with the importance of physical structures (Jagersten, 1972; Schroeder and Hermans, 1975; Strath­ on the maintenance of populations (Banse, 1986; All­ mann, 1985; Radashevsky, 1994 ). Reproductive strategies dredge and Hamner, 1980; Kingsford, 1990; Lefèvre, take root in both the phyletic history of the group (ultimate 1990; Pineda, 1991; Rothlisberg et al., 1983). Ali these causation) and in the changing environmental conditions papers come to similar conclusions concerning the need to (proximate causation). Among the latter, constraints of dis­ take watermass circulation into account in order to unders- persal and energy available for development have been 336 LI FE CYCLE EVOLUTION IN POL YCHAETES recognized. Three life-history patterns are available to Three strategies to esape from dispersal constralnts reduce dispersal (Fig. 1): i) evolution towards benthic development through a reduction in, or the suppression of, bendto-planktonic development the planktonic larval phase; ii) conservation of the bentho­ (e<otrophy) planktonie life cycle but with behavioural adaptation of long larval planktonic life planktonic larvae (such as vertical migrations)
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