Evidence of chemical communication during the gametogenesis of holothuroids

Ecology, July, 1996 by Jean-Francois Hamel, Annie Mercier

INTRODUCTION

Chemical communication is a widely studied topic of ecological importance in the animal kingdom. In recent years, a great deal of knowledge has been gathered from studies in insects and fish on the synthesis, physical structure, and functional properties of pheromones, as well as on how they are perceived and exert their action (Shorey 1976, Leroy 1987, Hardie 1991, Radl and Linsenmair 1991, Cork et al. 1992). Pheromones are also known to play various roles in the maturation, hormonal cycles, and mating events of mammals (Leroy 1987, Agosta 1992).

The number of unresolved questions in the field of chemical communication among marine invertebrates probably justifies the important surge of interest in this subject. A large amount of work in this field deals with predator-prey interactions (Coll and Sammarco 1988, Lawrence 1991, Legault and Himmelman 1993). Nevertheless, pheromones in invertebrates are presumed to serve in congener recognition, search for suitable colonizing area, and communication of potential threats. To date, most of the work has brought significant clues in favor of the existence of chemical mediators during many events related to reproduction in marine invertebrates. Examples include the studies of Boily-Marer (1974), Boily-Marer and L'Homme (1986) and Zeeck et al. (1988) who described the induction of the nuptial dance in polychaetes by pheromones. Pheromones were also proposed to be the major inducers of courtship, moulting, and mating in crustaceans (Atema and Engstrom 1971, Atema et al. 1979, Eisner 1980, Gleeson 1980, 1982, Conner et al. 1981, Atema and Cowan 1986, Cowan 1991).

Reports of chemical communication among echinoderms are very scarce and some remain speculative. Run et al. (1988) indicated that a sex-specific contact chemoreception could partially explain sex recognition in the sea star Archaster typicus. Ormond et al. (1973) showed that an active component released by the gonad of the sea star Acanthaster planci induced reproductive behavior and spawning in nearby mature adults. Furthermore, studies on deep-sea echinoderms imply that chemical cues play a role in gametogenic seasonality (Tyler et al. 1982, Tyler and Gage 1984) and spawning synchronization (Tyler et al. 1982, Young et al. 1992). However, the proximate mechanisms by which deep-sea animals synchronize spawning or gametogenesis to ensure successful fertilization remain unknown (Young et al. 1992). Hamel and Mercier (1995a) found that chemical communication during an aggregative behavior in the sea star Leptasterias polaris seemed to play a role in gametogenic synchronization, mostly during the late stages of gamete maturation before spawning. The paired mating of the sea star Neosmilaster georgianus was also presumed to be regulated by chemical mediators (Slattery and Bosch 1993). McEuen (1988) suggested that synchronization of spawning among sea cucumbers in the field could be enhanced by sex pheromones. Finally, Miller (1989) discussed the periodic presence of a long-lived bio-activated sex-specific substance in natural seawater during the reproductive season of sea stars, and suggested that benthic invertebrates may communicate their sexual identity and readiness to spawn by means of waterborne pheromones.

To our knowledge, the existence and implications of chemical communication among individuals in gametogenesis have not been presented for any invertebrate. Most of the attention has been directed toward the correlation of gametogenesis with environmental conditions. Photoperiod has been shown experimentally to be the main factor responsible for synchronizing gametogenic events of shallow-water echinoderms (Pearse and Eernisse 1982, Pearse and Walker 1986, Pearse et al. 1986a, b, Bay-Schmith and Pearse 1987, McClintock and Watts 1990). Increasing temperature and food supply seem to constitute the other most determinant factors (Ito et al. 1989, Chia and Walker 1991, Pearse and Cameron 1991). It is proposed that the environmental fluctuations perceived by the organisms initiate a reaction leading to somatic changes and modifications in the reproductive metabolism, possibly through gene activation or hormone synthesis (Schoenmakers 1980, Schoenmakers and Dieleman 1981, Shirai and Walker 1988, Hines et al. 1992, Walker et al. 1992, Barker and Xu 1993). It is not as easy to explain the onset and harmonious interindividual development of gametogenesis under total darkness in entire populations, whether exposed to similar or distinct local environmental conditions. It becomes especially important for freely spawning marine invertebrates that may waste a large portion of their gametes if this synchronization is not well orchestrated.

Our investigation revealed that environmental factors, coupled with various endogenous reactions, could not adequately explain the synchronous initiation and harmonious development of gamete synthesis in male and female Cucumaria frondosa. This brought up an interesting question: are chemical mediators involved in the harmonious interindividual development of gametes? We have approached this study of reproductive rhythmicity by examining the progress of gametogenesis in populations of C. frondosa, in the field and in laboratory, under various experimental conditions. This work is the first to explore the role of chemical mediators during gametogenesis of a population of marine invertebrates, while providing basic data and explaining a possible synergism with environmental factors.