The energetics of scleractinian coral larvae and implications for dispersal

Graham, Erin Marie (2012) The energetics of scleractinian coral larvae and implications for dispersal. PhD thesis, James Cook University.

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Dispersal is a key process in the ecology and evolution of species. For sessile marine invertebrates like corals, the larval stage is the only means of dispersal, making this stage fundamentally important. Factors governing the dispersal potential of scleractinian corals include oceanographic conditions and the length of time coral larvae spend in the plankton. For lecithotrophic, broadcast-spawned coral larvae, the pelagic larval duration (PLD) will largely depend on larval energetics; that is, the amount of maternally-derived energy reserves available and the rate at which these reserves are used. The overall aim of this thesis was to investigate the energetics of scleractinian coral larvae to enhance understanding of the dispersal potential of corals, knowledge that is necessary for the design of marine protected areas and other management strategies needed to protect coral reefs. I first established the temporal dynamics of larval energy use by quantifying temporal changes in lipid content and respiration rates throughout the larval phase for a range of species. Building on these findings, I quantified how the dynamics of larval energetics changed under different experimental temperatures, to improve understanding of how climate change may influence larval dispersal and coral population connectivity. Finally, I considered how larval energetics affected post-settlement survival and growth to gain insights into whether time spent in the plankton might reduce a coral's ability to contribute to post-settlement demography (i.e., "realized" dispersal). Lecithotrophic marine invertebrate larvae generally have shorter PLDs than planktotrophic larvae. However, non-feeding coral larvae have larval durations far exceeding predictions based on their energetics, raising questions about how they achieve such longevity. In this thesis, I measured temporal changes in metabolic rates and lipid content of larvae of four species of reef corals (Goniastea aspera, Acropora tenuis, A. nasuta, and A. spathulata) to determine whether changes in energy use through time contribute to their extended PLDs (Chapter 2). The temporal dynamics of both metabolic rates and lipid content were highly consistent among species. Metabolic rates pre-fertilization were low, and then increased rapidly during development to peak 1-2 days after spawning, when larvae began swimming. Rates then declined by up to two orders of magnitude over the following week, and remained low thereafter. Consistent with patterns in metabolic rates, lipid depletion was rapid during development, before slowing dramatically from about ten days onwards. Throughout this extended period of low metabolism, larvae continued to swim, complete metamorphosis, and showed no increase in mortality rates. The capacity of non-feeding coral larvae to enter a low-metabolism state soon after becoming competent significantly extends their dispersal potential, thereby accruing connectivity advantages typically associated with planktotrophy. Temperature is an important environmental variable affecting the metabolism of ectothermic organisms. Predicted increases in sea-surface temperatures due to climate change are likely to alter the energy use of coral larvae and thus influence the dispersal potential of corals. Using a regression-based approach, I quantified the effect of five temperatures on the survival and energy use of A. tenuis larvae (Chapter 3). Temperature had a significant effect on larval survival, with increasing temperature leading to a monotonic increase in mortality rates. Contrary to my expectation that metabolic rates would increase with temperature, however, temperature had a parabolic effect on peak respiration rates and lipid use during development: rates declined as temperatures either increased above or decreased below ambient. Moreover, temperature did not appear to affect larvae during the extended period of low metabolism. My results suggest that even small differences in temperature from ambient affect coral larval dispersal potential. In particular, increased metabolism associated with warming temperatures leads to faster development, which increases the potential for self-recruitment, while higher mortality decreases the proportion of a larval cohort that survives for longer dispersal distances. Thus, connectivity among coral populations, which critically underpins reef resilience, is likely to decline in the near future.

Demographic connectivity requires both the dispersal of individuals between sub-populations, and their subsequent contribution to population dynamics. For non-feeding marine larvae, the capacity to delay settlement enables greater dispersal distances, but the energetic cost of delayed settlement can adversely impact post-settlement fitness. Accordingly, I assessed whether delayed settlement influences either mortality rates or growth rates for the first six weeks following settlement of A. tenuis larvae (Chapter 4). Larvae that were settled at two, four, and six weeks after spawning, and then deployed in the field, showed negligible effects of delayed settlement on post-settlement survival and time to initial budding for colony formation. Between-cohort differences in budding rate were best explained by temporal variation in the post-settlement acquisition of zooxanthellae. The potential for coral larvae to remain in the pelagic zone for increased periods of time, with little or no effect on post-settlement survival and growth, suggests that the costs of delayed settlement are largely confined to those accrued during the larval phase itself. This indicates that larvae that successfully settle after extended periods in the plankton are likely to make meaningful demographic contributions to benthic dynamics. Thus the predicted trade-off between delayed settlement and post-settlement fitness appears to be less applicable to reef-building scleractinian corals than other taxa with non-feeding larvae.

In conclusion, my research has identified a potentially novel physiological attribute of coral larvae that offers an explanation for their exceptionally long larval durations compared to other non-feeding marine invertebrate larvae. Specifically, coral larvae enter a low-metabolism state soon after competence is acquired, and they are able to maintain this state for many weeks, even at temperatures several degrees above ambient. Consistent with this, coral larvae that successfully settle after spending more time in the plankton survive and grow at rates similar to those of corals spending less time in the plankton. Nevertheless, in a warmer world, coral connectivity will likely decline due to temperature-dependent increases in larval mortality and development. The broader implications of these findings for the long-term persistence of coral metapopulations under climate change will depend on the relative importance of local population maintenance, versus replenishment from other sub-populations.

Item ID: 29583
Item Type: Thesis (PhD)
Keywords: coral larvae; metabolic rates; lipid content; respiration; dispersal potential of corals; effect of temperature; delayed settlement; local population maintenance
Date Deposited: 11 Oct 2013 02:07
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 100%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 100%
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