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.
PLoS One
2017 Mar 28;123:e0173964. doi: 10.1371/journal.pone.0173964.
Show Gene links
Show Anatomy links
Environmental and biological cues for spawning in the crown-of-thorns starfish.
Caballes CF
,
Pratchett MS
.
Abstract
Sporadic outbreaks of the coral-eating crown-of-thorns starfish are likely to be due, at least in part, to spatial and temporal variation in reproductive and settlement success. For gonochoric and broadcast spawning species such as crown-of-thorns starfish, spawning synchrony is fundamental for achieving high rates of fertilization. Highly synchronized gamete release within and among distinct populations is typically the result of the entrainment of neurohormonal endogenous rhythms by cues from the environment. In this study, we conducted multiple spawning assays to test the effects of temperature change, reduced salinity and nutrient enrichment of seawater, phytoplankton, gametes (sperm and eggs), and the combined effect of sperm and phytoplankton on the likelihood of spawning in male and female crown-of-thorns starfish. We also investigated sex-specific responses to each of these potential spawning cues. We found that (1) abrupt temperature change (an increase of 4°C) induced spawning in males, but less so in females; (2) males often spawned in response to the presence of phytoplankton, but none of the females spawned in response to these cues; (3) the presence of sperm in the water column induced males and females to spawn, although additive and synergistic effects of sperm and phytoplankton were not significant; and (4) males are more sensitive to the spawning cues tested and most likely spawn prior to females. We propose that environmental cues act as spawning ''inducers'' by causing the release of hormones (gonad stimulating substance) in sensitive males, while biological cues (pheromones) from released sperm, in turn, act as spawning ''synchronizers'' by triggering a hormonal cascade resulting in gamete shedding by conspecifics. Given the immediate temporal linkage between the timing of spawning and fertilization events, variability in the extent and synchronicity of gamete release will significantly influence reproductive success and may account for fluctuations in the abundance of crown-of-thorns starfish.
Fig 1. Proportion of starfish that spawned in response to cues.(a) seawater temperature, (b) water quality, (c) phytoplankton, (d) conspecific gametes, (e) sperm and phytoplankton. FSW = 0.2-μm filtered seawater; LS-FSW = low salinity filtered seawater; NE-FSW = nutrient-enriched filtered seawater; PP = combination of three phytoplankton species. Bars traversing the dashed lines represent spawning of more than 50% of individuals exposed to a given treatment.
Fig 2. Response time and cumulative probability of spawning in male and female crown-of-thorns starfish after exposure to environmental and biological cues.(a) seawater temperature, (b) water quality, (c) phytoplankton, (d) conspecific gametes, (e) sperm and phytoplankton. Solid circles are individual spawning events and different letters indicate significant differences based on multiple comparisons (Holm-Šídák) after Log-rank analyses. FSW = 0.2-μm filtered seawater; LS-FSW = low salinity filtered seawater; NE-FSW = nutrient-enriched filtered seawater; PP = combination of three phytoplankton species.
Fig 3. Schematic diagram of proposed cascade model for spawning induction and synchrony in response to environmental and biological cues.Grey arrows are responses to environmental cues and black arrows refer to biological cues. Neurohormonal mechanisms are based on Giese and Kanatani [14] and Mita et al. [15]. GSS = gonad-stimulating substance (relaxin-like gonad stimulating peptide); MIH = maturation-inducing hormone; MPF = maturation-promoting factor; FEBD = follicular envelop breakdown; GVBD = germinal vesicle breakdown.
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
Babcock,
Sperm Diffusion Models and In Situ Confirmation of Long-Distance Fertilization in the Free-Spawning Asteroid Acanthaster planci.
1994,
Pubmed
,
Echinobase
Beach,
Spawning pheromone in crown-of-thorns starfish.
1975,
Pubmed
,
Echinobase
Benzie,
The Effects of Sperm Concentration, Sperm:Egg Ratio, and Gamete Age on Fertilization Success in Crown-of-Thorns Starfish (Acanthaster planci) in the Laboratory.
1994,
Pubmed
,
Echinobase
Brauer,
Triggering of the stomach eversion reflex of Acanthaster planci by coral extracts.
1970,
Pubmed
,
Echinobase
Brodie,
Are increased nutrient inputs responsible for more outbreaks of crown-of-thorns starfish? An appraisal of the evidence.
2005,
Pubmed
,
Echinobase
Devlin,
Mapping the pollutants in surface riverine flood plume waters in the Great Barrier Reef, Australia.
2012,
Pubmed
Hamel,
Prespawning Behavior, Spawning, and Development of the Brooding Starfish Leptasterias polaris.
1995,
Pubmed
,
Echinobase
Kanatani,
Maturation-inducing substance in starfishes.
1973,
Pubmed
,
Echinobase
Kubota,
1-Methyladenine-producing cell in starfish testis.
1977,
Pubmed
,
Echinobase
Levitan,
Sex-specific spawning behavior and its consequences in an external fertilizer.
2005,
Pubmed
,
Echinobase
Mellin,
Marine protected areas increase resilience among coral reef communities.
2016,
Pubmed
,
Echinobase
Mercier,
Endogenous and exogenous control of gametogenesis and spawning in echinoderms.
2009,
Pubmed
,
Echinobase
Pentreath,
Neurobiology of echinodermata.
1972,
Pubmed
,
Echinobase
Reuter,
Influence of sperm and phytoplankton on spawning in the echinoid Lytechinus variegatus.
2010,
Pubmed
,
Echinobase
Schroeder,
Inter-annual variability of wet season freshwater plume extent into the Great Barrier Reef lagoon based on satellite coastal ocean colour observations.
2012,
Pubmed
Starr,
Direct coupling of marine invertebrate spawning with phytoplankton blooms.
1990,
Pubmed
,
Echinobase
Wooldridge,
Environmental triggers for primary outbreaks of crown-of-thorns starfish on the Great Barrier Reef, Australia.
2015,
Pubmed
,
Echinobase