Click
here to close Hello! We notice that
you are using Internet Explorer, which is not supported by Echinobase
and may cause the site to display incorrectly. We suggest using a
current version of Chrome,
FireFox,
or Safari.
Sci Rep
2018 Jan 10;81:239. doi: 10.1038/s41598-017-18655-6.
Show Gene links
Show Anatomy links
Chemicals released by male sea cucumber mediate aggregation and spawning behaviours.
Marquet N
,
Hubbard PC
,
da Silva JP
,
Afonso J
,
Canário AVM
.
Abstract
The importance of chemical communication in reproduction has been demonstrated in many marine broadcast spawners. However, little is known about the use of chemical communication by echinoderms, the nature of the compounds involved and their mechanism(s) of action. Here, the hypothesis that the sea cucumber Holothuria arguinensis uses chemical communication for aggregation and spawning was tested. Water conditioned by males, but not females, attracted both males and females; gonad homogenates and coelomic fluid had no effect on attraction. Male spawning water, but not female spawning water, stimulated males and females to release their gametes; the spermatozoa alone did not induce spawning. H. arguinensis male spawning water also induced spawning in the phylogenetically related H. mammata. This indicates that males release pheromones together with their gametes that induce spawning in conspecifics and possibly sympatric species. Finally, the male pheromone seems to be a mixture with at least one labile compound (biological activity is lost after four hours at ambient temperature) possibly including phosphatidylcholines. The identification of pheromones in sea cucumbers offers a new ecological perspective and may have practical applications for their aquaculture.
Figure 1. Schematic representation of the experimental setup used in the attraction experiment. (a) Overhead view showing the entry area A, the stimulus and control sides B or C. (b) Side view showing the position of the camera IR-C and light source IR-L. SC indicates the initial positioning of the test sea cucumber.
Figure 3. Percentage of first choice (a,b) and relative time (c,d) spent in the coelomic fluid (stimulus) and in the control arm (sea water). M corresponds to male receiver and F to female receiver. Error bars are one standard deviation.
Figure 4. Percentage of first choice (a,b) and relative time (c,d) spent in the gonad (ovary and testis) homogenate (stimulus) and in the control arm (sea water). M corresponds to male receiver and F to female receiver. Error bars are one standard deviation.
Figure 5. (a,b) LC-MS single ion traces of methanol extracts at m/z 808.7 under positive polarity. (a) Male before (blue) and after (red) spawning; (b) female before (blue) and after (red) spawning. (c,d) Fragmentation spectra. (c) MS2(808.7); (d) MS2(790.5), the standard 1,2-stearoyl phosphatidylcholine. The inserted structures were assigned to ion with m/z 184.1. The arrows indicate the fragmented peaks.
Figure 6. (a,b) LC-MS single ion traces of methanol extracts at m/z 287 under positive polarity. (a) Male before (blue) and after (red) spawning; (b) female before (blue) and after (red) spawning. (c–e) Fragmentation spectra of m/z 287. (c) MS2(287); (d) MS3(287→245); (e) MS4(287→245→203). The arrows indicate the fragmented peaks.
Babcock,
Synchronous multispecific spawning on coral reefs: potential for hybridization and roles of gamete recognition.
1995, Pubmed
Babcock,
Synchronous multispecific spawning on coral reefs: potential for hybridization and roles of gamete recognition.
1995,
Pubmed
Bahrami,
Discovery of novel saponins from the viscera of the sea cucumber Holothuria lessoni.
2014,
Pubmed
,
Echinobase
Beach,
Spawning pheromone in crown-of-thorns starfish.
1975,
Pubmed
,
Echinobase
Borrero-Pérez,
Molecular systematics of the genus Holothuria in the Mediterranean and Northeastern Atlantic and a molecular clock for the diversification of the Holothuriidae (Echinodermata: Holothuroidea).
2010,
Pubmed
,
Echinobase
Caballes,
Environmental and biological cues for spawning in the crown-of-thorns starfish.
2017,
Pubmed
,
Echinobase
Campbell,
Escape and aggregation responses of three echinoderms to conspecific stimuli.
2001,
Pubmed
,
Echinobase
Caulier,
When a repellent becomes an attractant: harmful saponins are kairomones attracting the symbiotic Harlequin crab.
2013,
Pubmed
,
Echinobase
Cook,
The use of push-pull strategies in integrated pest management.
2007,
Pubmed
Cross,
Phosphatidylcholine enhances the acrosomal responsiveness of human sperm.
1994,
Pubmed
Cummins,
Molluscan attractins, a family of water-borne protein pheromones with interspecific attractiveness.
2005,
Pubmed
Gould,
Polyspermy prevention in marine invertebrates.
2003,
Pubmed
Hall,
The crown-of-thorns starfish genome as a guide for biocontrol of this coral reef pest.
2017,
Pubmed
,
Echinobase
Hamel,
Prespawning Behavior, Spawning, and Development of the Brooding Starfish Leptasterias polaris.
1995,
Pubmed
,
Echinobase
Hardege,
Peptide pheromones in female Nereis succinea.
2004,
Pubmed
Harrison,
Mass spawning in tropical reef corals.
1984,
Pubmed
Hsu,
Electrospray ionization with low-energy collisionally activated dissociation tandem mass spectrometry of glycerophospholipids: mechanisms of fragmentation and structural characterization.
2009,
Pubmed
Kanatani,
Maturation-inducing substance in starfishes.
1973,
Pubmed
,
Echinobase
Kato,
Neuronal peptides induce oocyte maturation and gamete spawning of sea cucumber, Apostichopus japonicus.
2009,
Pubmed
,
Echinobase
Levitan,
Sex-specific spawning behavior and its consequences in an external fertilizer.
2005,
Pubmed
,
Echinobase
Levitan,
Sperm limitation in the sea.
1995,
Pubmed
Levitan,
Influence of Body Size and Population Density on Fertilization Success and Reproductive Output in a Free-Spawning Invertebrate.
1991,
Pubmed
,
Echinobase
Li,
Bile Acid secreted by male sea lamprey that acts as a sex pheromone.
2002,
Pubmed
Long,
Use of phosphatidylcholine to improve the function of turkey semen stored at 4°C for 24 hours.
2012,
Pubmed
Marshall,
Sperm release strategies in marine broadcast spawners: the costs of releasing sperm quickly.
2007,
Pubmed
Matsumura,
Phosphatidylcholine profile-mediated group recognition in catfish.
2007,
Pubmed
Mercier,
Endogenous and exogenous control of gametogenesis and spawning in echinoderms.
2009,
Pubmed
,
Echinobase
Mita,
Localization and characterization of phosphatidylcholine in sea urchin spermatozoa.
1991,
Pubmed
,
Echinobase
Painter,
Characterization of Aplysia attractin, the first water-borne peptide pheromone in invertebrates.
1998,
Pubmed
Pennington,
THE ECOLOGY OF FERTILIZATION OF ECHINOID EGGS: THE CONSEQUENCES OF SPERM DILUTION, ADULT AGGREGATION, AND SYNCHRONOUS SPAWNING.
1985,
Pubmed
,
Echinobase
Reuter,
Influence of sperm and phytoplankton on spawning in the echinoid Lytechinus variegatus.
2010,
Pubmed
,
Echinobase
Shimizu,
Bioactive marine natural products, with emphasis on handling of water-soluble compounds.
1985,
Pubmed
Siefkes,
Use of physiological knowledge to control the invasive sea lamprey (Petromyzon marinus) in the Laurentian Great Lakes.
2017,
Pubmed
Starr,
Direct coupling of marine invertebrate spawning with phytoplankton blooms.
1990,
Pubmed
,
Echinobase
THORSON,
Reproductive and larval ecology of marine bottom invertebrates.
1950,
Pubmed
Tominaga,
Reproduction and development of the conspicuously dimorphic brittle star Ophiodaphne formata (Ophiuroidea).
2004,
Pubmed
,
Echinobase
Witzgall,
Sex pheromones and their impact on pest management.
2010,
Pubmed
Wyatt,
Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates.
2010,
Pubmed
Yambe,
L-Kynurenine, an amino acid identified as a sex pheromone in the urine of ovulated female masu salmon.
2006,
Pubmed
Yund,
How severe is sperm limitation in natural populations of marine free-spawners?
2000,
Pubmed