Corals are more than the sum of their colonies: a network science perspective on the role of coral complexity and its consequences for coral reef health.

• Online Access: http://hdl.handle.net/2047/D20394204

A better understanding of coral reefs as complex adaptive systems responding to multiple perturbations is necessary in determining the near-term fate of coral reefs. By using a complex systems approach, including network analyses, we can begin to piece apart underlying mechanisms for resistance and resilience on reefs while considering the whole system. Resistance is a system's ability to tolerate a disturbance or stress until loss of functionality occurs and resilience is its ability to adjust system activity when faced with disturbance or stress and recover to a functional state of persistence. This dissertation explores the structure and adaptability of three complex systems on coral reefs - the scleractinian gastrovascular system, coral symbiotic associations with Symbiodiniaceae, and coral disease dynamics. Chapter one describes mixing and oxygen dynamics within individual polyps of a coral. I determined key time scales of mixing in polyp coelentera by using microelectrodes to measure oxygen concentration after a light-to-dark transition in three polyps each of three colonies of Montastraea cavernosa in the laboratory. The gastrovascular system was modeled as an electrical network where voltage represents oxygen concentration, current represents oxygen flux, capacitors represent volume compartments, and resistors represent impedance to oxygen flux. The time constant of mixing, defined as the time needed for the system to disperse 63.2% of the fluid in the coelenteron, was determined from the oxygen dynamics in the coelenteron as modeled by a resistor-capacitor network. Time constants were on the order of three minutes and oxygen dynamics were well fit by the model prediction. The microenvironment within polyps of M. cavernosa can respond as fast or faster than their external environment can fluctuate. Different coral species associate with different species of symbiotic algae in the family Symbiodiniaceae, creating a complex network of symbiotic associations on a reef. Chapters two and three explore coral symbiosis networks at global and reef scales. Coral bleaching is the breakdown of the association between the coral host and its endosymbiotic algae in response to increasing temperatures. In chapter two, I analyzed a global network of coral-symbiont associations for resistance to temperature stress and robustness to various perturbations. My novel bleaching model determined resistance of the networks to increasing temperature by removing links when the environmental temperature surpassed their weight, a temperature threshold for individual host-symbiont pairs based on known physiological responses. Ecological robustness, how much perturbation is needed to decrease the number of nodes by 50%, was determined for multiple removal models. I showed that the global network of associations between corals and Symbiodiniaceae and its distribution of thermal tolerances are non-random, resulting in a system with higher sensitivity to environmental perturbations. By limiting our spatial scale and expanding our temporal scale, we can start to answer questions about coral symbiosis resilience. Thus, in chapter three, I repetitively monitored and sampled a coral-Symbiodiniaceae network in Bocas del Toro, Panama from January 2017 to January 2018, during which the reef experienced two high-temperature bleaching events. I explored how Symbiodiniaceae communities varied across host species, depth, and time. Temporal networks of the symbiotic associations were used to assess differences in association patterns that led to structural and/or functional resilience to repeat heat stress events. I defined structural resilience as a system's ability to either resist changing the structure of associations or return to the initial structure after a disturbance. Functional resilience is a system's ability to recover in relation to its health and function, but it may also undergo structural changes during that recovery. Although 20-100% of every species was visibly bleached during one or both of the bleaching events, less than 50% of each species at each depth was still bleached by the recovered time point. Structures of Symbiodiniaceae co-occurrence networks and coral-symbiont networks varied through time indicating that on a reef scale, coral-symbiont associations responded to changing environmental conditions. Lastly, chapter four investigates the epizootiology of the stony coral tissue loss disease (SCTLD) outbreak in the lower Florida Keys at multiple temporal and spatial scales (among reefs ~1 km and within reefs ~10 m). In May 2018, three sites without signs of SCTLD were established along an offshore to nearshore gradient. Corals within two 10 m x 10 m quadrats at each site were mapped, and the percentage of living tissue and maximum colony diameter were measured. We quantified disease state for each colony every two-three weeks until December 2019. SCTLD was first noted within the offshore and midchannel reef sites in early October 2018 and later appeared at the nearshore site in early February 2019. SCTLD was negatively correlated with thermal stress. Although Porites strigosa, Dichocoenia stokesii, Colpophyllia natans, and Diploria labyrinthiformis were the most susceptible species at our sites, reefs with more Montastraea cavernosa and Orbicella faveolata colonies had greater tissue loss associated with SCTLD. The disease was more severe within sites with high species diversity, low colony density, and high coral cover. SCTLD disproportionately affected larger colonies. The spatial analyses suggest that 1) SCTLD followed a contagious disease model within small (< 10 m) spatial scales, 2) colonies within 2 m of a diseased coral were at higher risk for subsequently showing disease signs, and 3) most often initial transmission among reefs occurred on spatial scales larger than a 10 m radius.