Quantifying the benthic metabolism of tropical coral reefs and seagrasses in a changing climate

Mallon, Jennifer (2023) Quantifying the benthic metabolism of tropical coral reefs and seagrasses in a changing climate. PhD thesis, University of Glasgow.

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Tropical coastal regions are home to around a third of the world’s population, where entire communities depend upon ecosystem services derived from an interconnected network of coral reefs, seagrasses, mangroves, and associated fauna. The tropical coastal zone incorporates numerous unique and widely distributed habitats, from mangroves to mud flats, however this thesis focusses on two interconnected marine tropical ecosystems. Coral reefs and seagrasses are global biodiversity hotspots with high rates of productivity which fuel coastal biogeochemical cycling. Seagrasses support blue carbon sequestration, sediment retention, and provide critical habitat. Biogenic calcification by coral reef organisms constructs massive calcium carbonate (CaCO3)structures, as calcifying organisms deposit skeletons over thousands of years. This robust CaCO3 structure protects coastlines from storms by absorbing the impact of wave energy and is critical for maintaining healthy shores. Coral skeletons form a uniquely intricate architecture which provides habitat for diverse ecological communities and many economically important species. However, anthropogenic climate change threatens the ecological function of these systems. High concentrations of carbon dioxide (CO2) are absorbed into the oceans, resulting in ocean acidification and warming waters, with catastrophic impacts on calcifying organisms. As the global climate crisis threatens coastal ecosystems and the services they provide, the development of metrics to track and predict changes to ecosystem function are essential for advancing scientific conservation efforts.

Biogeochemical measurements of benthic metabolism are proposed as an efficient tool for long-term and high-resolution tracking of changes to species composition and ecosystem function. Benthic metabolism in coastal ecosystems describes carbon cycling driven by biological processes: inorganic (calcification – dissolution) and organic carbon metabolism (photosynthesis – respiration). These processes can be measured from changes in sea water chemistry; specifically dissolved oxygen (DO), dissolved inorganic carbon (DIC), and total alkalinity (TA). Changes to these parameters can be used to measure net metabolic flux between the benthos and seawater and can be used to quantify the carbon cycling processes of coastal ecosystems. Calculating the balance of net community calcification (NCC) to net community production (NCP) provides insight into benthic composition and ecological function and has potential as a method for monitoring change. This approach has been particularly useful for coral reef ecosystems, as their ecological complexity and biodiversity presents a unique logistical challenge for research.

Coral reefs are already substantially degraded and highly vulnerable to the impact of climate change effects such as ocean warming and acidification. Catastrophic declines in coral cover and the negative impact of warming and ocean acidification on calcifying organisms threatens the potential for coral reef structural growth and maintenance, and some reefs are already net dissolving. In response to declines in calcifying corals, reef restoration efforts aim to rebuild coral reefs using a variety of techniques to propagate coral fragments and produce juvenile corals which can be transplanted on the reef. However, differences in the physiological processes of the species used in such programs require further evaluation. To address this research gap, rates of metabolism were measured in individual fragments of important coral reef calcifiers, with significant differences detected between species of coral and between coral and crustose coralline algae (CCA). The organisms selected for this study have distinct functions in terms of reef calcification. Acropora cervicornis have rapid growth rates and an intricate branching morphology, while Orbicella faveolata and Siderastrea Siderea are slow-growth, massive reef-builders. The abundant and opportunistic Porites astreoides are known for their increasing dominance on degraded coral reefs, and crustose coralline algae create a cement-like covering which encrusts and strengthens reef substrate. Ex-situ incubations under natural ambient light demonstrated that individual rates of calcification and photosynthesis are different between species, and shift in response to light over a diurnal cycle. The highest photosynthesis and calcification values were measured at solar noon for all species, followed by a plateau, reflecting a hyperbolic relationship with light. Metabolism irradiance models demonstrated similar light-response curves in the 2 massive coral species and the opportunistic P. astreoides, while branching A. cervicornis metabolism was lower and aligned more closely with CCA than the other coral species. Metabolic maxima for photosynthesis (Pmax) and calcification (Gmax) were extracted from the models and demonstrated a positive linear relationship between the different organisms, indicating a link between the energy produced by photosynthesis and respiration with calcification across functional groups. The data were interpreted in the context of total carbon metabolism (Mtot), and this was proposed as a novel metric for quantifying the balance of inorganic to organic carbon cycling.

A range of methods have been developed to quantify benthic metabolism in the field; from isolation of the benthic community using incubation chambers to autonomous sensor deployments for instantaneous measurements of ecosystem metabolism, each with unique advantages and limitations. In-situ measurements are critical for quantifying metabolism of complex communities, which cannot be reliably recreated in ex-situ settings. Due to the myriad of environmental influences affecting benthic metabolism in the field, benthic incubation chambers have been used to isolate benthic organisms and the water surrounding them so that any biogeochemical changes in the water column are the result of biological activity within the chamber. Benthic chambers usually consist of transparent enclosures which allow sunlight to penetrate, and often have a submersible pump installed to drive water flow over the study organisms. A sampling port facilitates measurement of dissolved oxygen and carbonate chemistry so that metabolic rates can be tracked. Following a review of the benthic chamber designs currently available, a gap was identified for a chamber that is lowcost, made from easily accessible materials, large enough to incubate a community, and minimally invasive. A simple benthic chamber design was created and trialled to address these design criteria. The benthic chamber performed in line with the other existing chamber designs available, while substantially cutting costs. The chambers were deployed in two case studies to measure productivity of seagrass and coral reef patches. Productivity measurements agreed with previous estimates for both ecosystems tested, and the coral reef patches incubated also showed a hyperbolic relationship with light, aligning with the diurnal trends measured in the ex-situ incubations of individual coral reef calcifiers. The benthic chamber presented here is an affordable and feasible option for field studies of benthic metabolism.

At the broader ecosystem or large community scale, benthic metabolism can be tracked over large bodies of water and over longer time scales. Using flow respirometry and benthic boundary layer approaches, it is possible to measure biogeochemical flux in coastal waters without interrupting natural flow and environmental drivers. In the final experiment of this thesis, multiple methods were used to measure benthic metabolism of a seagrass-sediment dominated bay. The methods selected represent some of the key approaches developed over the last ~70 years. Lagrangian flow, control volume, and benthic ecosystem and acidification measurement systems (BEAMS) approaches were tested over 48 hours, alongside benthic incubation chambers and discrete water sampling. There was strong agreement between Lagrangian, control volume and BEAMS for net community production (NCP) measurements, and integrated rates were aligned with results from chamber incubations. Net community calcification (NCC) was relatively low, and the Lagrangian approach was more sensitive to the NCC signal than BEAMS. The metabolic rates scaled with light conditions following a hyperbolic model, with variations in coefficients and model fits between the data sets collected. Linear regressions between NCC and NCP demonstrated distinct relationships between night and day, again highlighting the importance of diel cycles in quantifying coastal carbon cycles.

The findings of this thesis enhance the current understanding of the metabolic processes taking place in tropical marine ecosystems and supports future research by providing novel metrics and methods for quantifying benthic metabolism. At each scale, from the organism to the ecosystem, the influence of light was established as a key driver of benthic metabolism. This research has direct impact and application for conservation of coral reefs and seagrasses and will support future endeavours to quantify carbon cycling of coastal ecosystems.

Item Type: Thesis (PhD)
Qualification Level: Doctoral
Subjects: G Geography. Anthropology. Recreation > GC Oceanography
G Geography. Anthropology. Recreation > GE Environmental Sciences
Colleges/Schools: College of Science and Engineering > School of Geographical and Earth Sciences
Supervisor's Name: Bass, Dr. Adrian
Date of Award: 2023
Depositing User: Theses Team
Unique ID: glathesis:2023-83381
Copyright: Copyright of this thesis is held by the author.
Date Deposited: 03 Feb 2023 10:59
Last Modified: 03 Feb 2023 10:59
Thesis DOI: 10.5525/gla.thesis.83381
URI: https://theses.gla.ac.uk/id/eprint/83381
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