Environmental influences on the reproductive biology and early life history of the crown-of-thorns starfish

Caballes, Ciemon Frank (2017) Environmental influences on the reproductive biology and early life history of the crown-of-thorns starfish. PhD thesis, James Cook University.

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Population outbreaks of the coral-eating crown-of-thorns starfish, Acanthaster spp., often result in extensive coral mortality with highly extended recovery times, thereby contributing significantly to sustained and ongoing declines in coral cover across the Indo-Pacific. Long-term or permanent solutions depend on filling crucial gaps in our knowledge of the biology of crown-of-thorns starfish, particularly its reproductive biology and early life history, to understand the initiation and spread of outbreaks. Populations of crown-of-thorns starfish are typically predisposed to major fluctuations due to inherent properties of their life history such as high fecundity, high fertilization rates, and short generation times. However, densities vary enormously in space and time, pointing to major fluctuations in reproductive success. The overarching question therefore is: what limits recruitment success in crown-of-thorns starfish and which stages or processes in its life cycle are most vulnerable to these constraints? Small environmental perturbations that trigger life-stage-specific responses can have pronounced effects on recruitment success and hence, on the dynamics of adult populations. My research explored the role of environmental factors on (1) gametogenesis and reproductive timing; (2) spawning induction and synchronicity; (3) fertilization and embryonic development; and on (4) larval vitality, in relation to maternal provisioning and larval nutrition.

To assess gametogenic activity and reproductive timing in crown-of-thorns starfish, intensive and extensive sampling of crown-of-thorns starfish from Australia's Great Barrier Reef (GBR) was conducted. This study revealed marked inter-annual variation in reproductive timing and output, possibly depending on local environmental conditions. In the first sampling season (September 2013 to March 2014), there was only minor and repeated spawning that occurred over a highly protracted spawning period, while in the second sampling season (September 2014 to March 2015), there was evidence of comprehensive and synchronous spawning by crown-of-thorns starfish.

I then examined the role of environmental and biological cues for spawning in crown-of-thorns starfish. 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, I 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. I also investigated sex-specific responses to each of these potential spawning cues. I 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 were more sensitive to the spawning cues tested and most likely spawn prior to females. These results suggest 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.

Following spawning, larval stages develop in the water column for at least 14-16 days, where environmental factors could constrain survivorship and effective development. The persistence and success of marine invertebrate populations is fundamentally dependent upon larval survival and settlement; hence the variable sensitivity of planktonic stages and processes (i.e. gametes, fertilization, embryonic development) to environmental stressors (e.g. temperature, salinity, pH) may be a potential population bottleneck. Here, I compared sperm swimming speeds and proportion of motile sperm and rates of fertilization and early development under a range of environmental variables (temperature: 20-36°C, salinity: 20-34 psu, and pH: 7.4-8.2) to identify environmental tipping points and thresholds for reproductive success. I also tested the effects of water-soluble compounds derived from eggs on sperm activity. This study demonstrated that gametes, fertilization, and embryonic development are robust to a wide range of temperature, salinity, and pH levels that are outside the range found at the geographical limits of adult distribution and can tolerate environmental conditions that exceed expected anomalies as a result of climate change. Water-soluble compounds associated with eggs also enhanced sperm activity, particularly in environmental conditions where sperm motility was initially limited. These findings suggest that fertilization and embryonic development of crown-of-thorns starfish are tolerant to a wide range of environmental conditions, though environmental constraints on recruitment success may occur at later ontogenic stages.

Previous studies on crown-of-thorns starfish have primarily focused on the effects of water quality and nutrient availability on larval growth and survival, while the role of maternal nutrition on reproduction and larval development has been overlooked. To examine the effects of maternal nutrition on oocyte size and early larval development, I pre-conditioned females for 60 days on diets of preferred coral (Acropora abrotanoides) versus non-preferred coral prey (Porites rus) and compared resulting gametes and progeny to those produced by females that were starved over the same period. Females fed ad libitum with Acropora increased in weight, produced heavier gonads and produced larger oocytes compared to Porites-fed and starved females. Fed starfish (regardless of whether it was Acropora or Porites) produced bigger larvae with larger stomachs and had a higher frequency of normal larvae that reached the late bipinnaria / early brachiolaria stage compared to starved starfish. Females on Acropora diet also produced a higher proportion of larvae that progressed to more advanced stages faster compared to Porites-fed starfish, which progressed faster than starved starfish. These results suggest that maternal provisioning can have important consequences for the quality and quantity of progeny.

Based on these findings, I proceeded to test whether maternal provisions from the egg were able to offset limitations imposed by limited access to exogenous sources of nutrients during the formative stages of larval development. This study examined the individual, additive, and interactive effects of endogenous (maternal diet: Acropora, Porites, mixed, and starved) and exogenous (larval diet: high concentration at 10⁴ cells·mL⁻¹, low concentration at 10³ algal cells·mL⁻¹, and starved) nutrition on the survival, growth, morphology, and development of larvae of the crown-of-thorns starfish. Female starfish on Acropora and mixed diet produced bigger oocytes compared to Porites-fed and starved treatments. Using oocyte size as a proxy for maternal provisioning, endogenous reserves in the oocyte had a strong influence on initial larval survival and development. This suggests that maternal reserves can delay the onset of obligate exogenous food acquisition and allow larvae to endure prolonged periods of poor environmental nutritive conditions or starvation. The influence of exogenous nutrition became more prominent in later stages, whereby none of the starved larvae reached the mid-to-late brachiolaria stage 16 days after the onset of the ability to feed. There was no significant difference in the survival, development, and competency of larvae between high and low food treatments. Under low algal food conditions, larvae compensate by increasing the length of ciliated feeding bands in relation to the maximum length and width of the larval body, which improve food capture and feeding efficiency. However, the effects of endogenous nutrition persisted in the later developmental stages, as larvae from starved females were unable to develop larger feeding structures in response to food-limiting conditions. Phenotypic plasticity influenced by endogenous provisions and in response to exogenous food availability may be an important strategy in boosting the reproductive success of crown-of-thorns starfish, leading to population outbreaks.

The tolerance of early life history stages and processes to a suite of environmental stressors and the plasticity in reproductive behavior and larval morphology add to a growing list of traits that predispose crown-of-thorns starfish to pronounced fluctuations in abundance. Taken together, these results demonstrate that variable sensitivity of early life history stages and processes to environmental factors can have flow-on effects that disproportionately impact recruitment success and population replenishment in crown-of- thorns starfish. The cumulative effects of environmental variables on the success of different stages and processes in the life cycle of crown-of-thorns starfish ultimately dictate the available number of larvae that settle and recruit on reefs, and consequently, the patterns of abundance of adult crown-of thorns starfish.

Item ID: 51628
Item Type: Thesis (PhD)
Keywords: Acanthaster outbreaks, cleavage, coral reefs, crown-of-thorns, disturbances, gastrulation, Great Barrier Reef, larval development, larval nutrition, maternal provisioning, pH, phenotypic plasticity, salinity, sperm activity, temperature
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Additional Information:

For this thesis, Ciemon Caballes received the Dean's Award for Excellence 2018.

Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Pratchett, Morgan S., Caballes, Ciemon F., Rivera-Posada, Jairo A., and Sweatman, Hugh P.A. (2014) Limits to understanding and managing outbreaks of crown-of-thorns starfish (Acanthaster spp.). Oceanography and Marine Biology, 52. pp. 133-200.

Chapter 3: Caballes, Ciemon F., and Pratchett, Morgan S. (2014) Reproductive biology and early life history of the crown-of-thorns starfish. In: Whitmore, Eric, (ed.) Echinoderms: ecology, habitats and reproductive biology. Marine Biology . Nova Science Publishers, New York, NY, USA, pp. 101-146.

Chapter 5: Caballes, Ciemon Frank, and Pratchett, Morgan S. (2017) Environmental and biological cues for spawning in the crown-of-thorns starfish. PLoS One, 12 (3).

Chapter 6: Caballes, Ciemon Frank, Pratchett, Morgan S., Raymundo, Maia L., and Rivera-Posada, Jairo A. (2017) Environmental tipping points for sperm motility, fertilization, and embryonic development in the crown-of-thorns starfish. Diversity, 9 (1). pp. 1-18.

Chapter 7: Caballes, Ciemon Frank, Pratchett, Morgan S., Kerr, Alexander M., and Rivera-Posada, Jairo A. (2016) The role of maternal nutrition on oocyte size and quality, with respect to early larval development in the coral-eating starfish, Acanthaster planci. PLoS ONE, 11 (6). pp. 1-21.

Chapter 8: Caballes, Ciemon Frank, Pratchett, Morgan S., and Buck, Alexander C.E. (2017) Interactive effects of endogenous and exogenous nutrition on larval development for crown-cf-thorns starfish. Diversity, 9 (1). p. 15.

Date Deposited: 22 Nov 2017 04:15
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 70%
06 BIOLOGICAL SCIENCES > 0608 Zoology > 060803 Animal Developmental and Reproductive Biology @ 30%
SEO Codes: 96 ENVIRONMENT > 9604 Control of Pests, Diseases and Exotic Species > 960407 Control of Pests, Diseases and Exotic Species in Marine Environments @ 40%
97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 60%
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