Early life history of the scleractinian cold-water coral Caryophyllia huinayensis from a naturally acidified Chilean Fjord

Abstract

Scleractinian cold-water corals (CWCs) are a diverse group of the phylum Cnidaria. As structuring species, they sustainably change the abiotic and biotic environment and thus maintain a self-organized habitat that supports a diverse associated fauna. Furthermore, they play a key role in regional carbon cycles by coupling benthic and pelagic ecosystems. Their reproduction can follow two different modes, brooding of larvae and broadcast spawning of gametes. Additionally, the reproduction of unisexual polyps (gonochorism) and hermaphroditism results in two sexual strategies, and two known asexual reproductive mechanisms (fragmentation and fission). Scleractinian CWC ecosystems are present globally and predominantly occur in deep waters. Hence, their accessibility is limited, which has hampered a comprehensive understanding of certain aspects of their life cycle, including gametogenesis, dispersal, metamorphosis from larva to polyp and early skeletogenesis. Consequently, the potential impact of the predicted ocean acidification (OA) on the early life cycle of scleractinian CWCs remains elusive.

The aim of this thesis is therefore to describe the reproductive biology of the scleractinian CWC Caryophyllia (Caryophyllia) huinayensis and to predict the possible impacts of OA on its early life history based on observational and experimental evidence. Both in vitro and in situ investigations were carried out to determine the reproductive mode and strategy, gametogenesis, potential dispersal mechanism, and the effect of aragonite undersaturation of seawater (Ωarag < 1) and low seawater pH on early skeletogenesis and oogenesis of this scleractinian CWC, respectively.

Observations revealed that C. huinayensis broods larvae, which are released throughout the year. At the end of a one-week planktonic stage, larvae settle and initiate metamorphosis, developing their first set of tentacles within two days. Skeletal formation and the development of the second set of tentacles started ca. 5 days after settlement. Zooplankton feeding, and the development of the third and fourth set of tentacles started ca. 21, 153 and 895 days after settlement, respectively (Chapter 2). During a three-year in vitro maintenance period, we documented reverse development in adult polyps through an ontogenetic reversal process, occurring spontaneously and without environmental stressors, as corroborated by in situ evidence. Termed “polyp dropout”, this phenomenon entails tissue retraction and tissue detachment from the skeleton. The detached polyps can survive for several weeks, but we never observed re-settlement (Chapter 3). Should re-settlement occur in situ, polyp dropout would mark a potential new mechanism, aligning with Stanley´s “naked coral” hypothesis, which explains how corals may have endured the Permian-Triassic mass extinction.

The early skeletogenesis of this scleractinian CWC was described using both real-time in vivo polarized light microscopy (PLM) and scanning electron microscopy (SEM) (Chapter 4). Remarkably, early skeletogenesis in this species follows a similar temporal and sequential development pattern to that of warm-water scleractinian corals. This suggests the presence of a genetically encoded body plan in scleractinian CWC, orchestrating a precisely timed biomineralization processes from the micro to macroscale during the early stages of development.

Additionally, I revealed that aragonite undersaturation of seawater (Ωarag < 1 ) has no effect on skeletal formation during early skeletogenesis, as C huinayensis recruits are still able to build integral micro- and macrostructural crystal morphologies (Chapter 4). Although the precise mechanism enabling scleractinian CWCs recruits to compensate for Ωarag < 1 remains elusive, it seems that the early life stages of C. huinayensis are equipped to cope with the projected alteration in seawater Ωarag by the end of the century. However, it should be noted that compensating for changes in seawater pH and its resultant alteration in seawater Ωarag is known to require higher energy expenditure, potentially leading to imbalances in energy utilization.

In a naturally acidified fjord in Chile, I utilized histological methods to investigate the effect of low seawater pH, and its interaction with temperature and oxygen on the reproductive biology of C. huinayensis across all seasons (Chapter 5). My findings indicate that the seawater pH effect varies depending on the interaction with environmental parameters. This suggests that C. huinayensis reproduction is influenced by a mixture of environmental and endogenous factors.

Overall, this thesis contributes to the understanding of the reproductive biology, potential dispersal mechanisms, and early life cycle of scleractinian CWCs, using C. huinayensis as a model species. It emphasises the importance of understanding a species' reproductive strategy and mode, and dispersal mechanism, which in all provide insights into its potential phylogeography, distribution, and habitat colonization ability. In this study, I present the first documentation from the larval stage up to three years post-settlement of a scleractinian CWC. The findings demonstrate that, with their heterotrophic feeding, CWCs develop at a rate similar to that of scleractinian warm-water corals, despite significant environmental differences. Moreover, the opportunity to rear newly settled polyps allowed the first assessment of the effect of Ωarag < 1 on early skeletogenesis, revealing an integral formation of skeletal structures. Moreover, we observed that seawater pH an its interaction with temperature and oxygen showed inconsistent effects on reproduction, suggesting that other environmental and endogenous factors also play a significant role in reproductive processes.

Based on these results, I suggest that future studies should consider reproduction as a critical factor in assessing the overall effect of ocean acidification. A pressing question remains as to whether the combination of rising ocean temperatures and OA will affect the early life stages of these corals. The foundational knowledge of reproductive biology and its interaction with OA, along with the tools developed during this study, provide a way to address this question and shed light on the response of scleractinian CWCs to our changing planet.