With marine heat waves increasing in intensity and frequency due to climate change, it is important to understand how thermal disturbances will alter coral reef ecosystems, which are highly susceptible to thermally-induced, mass bleaching events. In Moorea, French Polynesia, we evaluated the response and fate of stony coral following a major thermal stress event in 2019 that caused a substantial amount of branching coral (dominantly Pocillopora) to bleach and die. We investigated whether Pocillopora colonies that occurred within territorial gardens protected by the farmerfish Stegastes nigricans were less susceptible to or survived bleaching better than Pocillopora on adjacent, undefended substrate. Bleaching prevalence (proportion of the sampled colonies affected) and severity (proportion of a colony’s tissue that bleached), which were quantified for >1,100 colonies shortly after they bleached, did not differ between colonies within or outside of defended gardens. By contrast, the fates of 399 focal colonies followed for a year revealed that a bleached coral within a garden was a third less likely to suffer complete colony death and, for survivors, about twice as likely to recover to its pre-bleaching cover of living tissue compared to Pocillopora outside of a farmerfish garden. Our findings indicate that while residing in a farmerfish garden may not reduce the bleaching susceptibility of a coral during thermal stress, it does help buffer a bleached coral against severe outcomes. This oasis effect of farmerfish gardens, where survival and recovery of thermally-damaged corals are enhanced, is another mechanism that helps explain why large Pocillopora colonies are far more abundant in farmerfish territories than elsewhere in the lagoons of Moorea, despite gardens being much less common. As such, farmerfish may have a growing role in maintaining the resilience of branching corals as the frequency and intensity of marine heat waves continue to increase.

ABSTRACT

Echinoid herbivores and coral reef resilience

Stella Ann Swanson

Anthropogenic impacts and climate change are increasing the frequency and intensity at which ecosystems are being perturbed. On tropical reefs, disturbances can result in loss of live coral and sometimes initiate a transition to an alternative community state, frequently one dominated by macroalgae. Because algae-dominated reefs may have lower productivity, decreased species diversity and reduced ecosystem services, there has been considerable interest in elucidating the mechanisms that mediate a transition to an algae dominated state or the re-establishment of coral. In this dissertation I explore how physical attributes of a coral reef and the echinoid and fish communities control algal growth and influence the return to coral dominance.

Recent disturbances in Moorea, French Polynesia offer an opportunity to examine the effects of architectural complexity of the substrate on recruitment of new coral colonists. I explore how the success of new coral colonists is affected by variation in structural complexity, particularly with respect to the skeletons of recently-killed branching coral. I quantified growth and survival of juvenile pocilloporid corals on structurally complex Pocillopora skeletons and on massive Porites, then generated quantitative predictions about the role these different types of substrates play in the replenishment of coral populations in the lagoons of Moorea. Results revealed that recruitment to dead branching Pocillopora structures is high, yet very low subsequent survival of those recruits, due to fast erosion of their host, indicates that dead Pocillopora structures are a sink for corals at vulnerable life stages.

Microhabitats on dead coral structure can also provide important habitat for new coral colonists. Survivorship of young corals can be greater in crevices and holes than on exposed surfaces, due to incidental or targeted predation by herbivores and corallivores. Thus, other taxa that influence the availability of crevice space can indirectly mediate coral recruitment. Bioeroding echinoids have the potential to affect settlement and early survival of corals through their influence on crustose coralline algae (CCA) and/or the provision of crevice space. In Moorea, the echinoid Echinometra mathaei create distinctive crevices that enhance the small-scale structural complexity of the reef and are associated with high cover of CCA within and surrounding them. This study demonstrates that the microhabitats created by E. mathaei on slower eroding Porites coral provide favorable habitat for recruitment of coral, thereby bioeroding sea urchins could have an overall positive impact on the coral community.

In 2013, an unknown agent resulted in rapid mortality of echinoid populations in the lagoon of Moorea. In the final portion of this dissertation, I describe the nature of the decline in D. savignyi populations, and report how the benthic community responded over the first 2.5 years following the abrupt mortality event. Additionally, I experimentally tested the ability for fish and remaining sea urchin herbivores to control algal growth on this reef and determined the rate of algal colonization in the absence of these herbivores. Despite high abundances prior to their demise, the loss of D. savignyi did not result in an increase in macroalgae or a shift in community structure. The experimental results suggest that fish herbivores were able to compensate for the loss of the echinoids by rapidly consuming any enhanced algal growth. Furthermore, the establishment of algae in Moorea appears more slow than may occur on other tropical reefs in the absence of herbivory.

Coral reefs are currently threatened by both natural and human-driven disturbances, and climate change scenarios suggest that the health of future reefs is uncertain. To better inform management and preservation of coral reef ecosystems, it is critical that we understand the mechanisms that support recovery of coral habitat after coral mortality events. Macroalgae can inhibit coral recovery by preventing recruitment and growth of corals after a disturbance, leading to a shift in the dominant benthic community from coral to macroalgae. These macroalgal habitats do not support the same diversity of fish and other species as healthy coral reefs, and are thus undesirable on large scales. This dissertation addresses some processes that are important in the establishment and persistence of these macroalgal phase shifts. Through an enhanced understanding of macroalgal persistence, we may be able to identify (and protect) key species and processes that are critical to promoting coral reef recovery.

I used the macroalga Turbinaria ornata as a model species to examine the potential for herbivore-algal feedbacks that can promote persistent macroalgal phase shifts. This species is perennial and patches appear to persist inter-annually once established. In areas where macroalgae is present, Turbinaria largely dominates the benthic community. Results of observational studies of tagged Turbinaria patches suggest that Turbinaria populations exhibit positive population growth (both number of adult thalli and patch area increased over a 2 year period). Several factors including high turnover rates of thalli, year-round reproduction, and a buffer of immature individuals that may act as a “seed bank” following a disturbance may contribute to the expansion of this species in the lagoons of Moorea.

In addition, I used field experiments to assess the potential for associational refuge to provide a mechanism for Turbinaria persistence in the lagoons of Moorea. Results from these experiments suggest that an associational refuge may facilitate persistence of Turbinaria, as predation on small vulnerable individuals (< 2 cm in length) is reduced when associated with larger, less palatable adults. However, the significance of this refuge depends on the local abundance of browsing herbivores that can consume macroalgae. An associational refuge that results in higher recruit survival in the presence of herbivory could represent a self-reinforcement mechanism that could facilitate the establishment and multi-generational persistence of Turbinaria patches on coral reefs.

To determine the effects of herbivore pressure on the development and persistence of a macroalgal community, I examined the effects of herbivores on mature (dominated by the late stage macroalga Turbinaria ornata) and early stage (dominated by turf algae) algal communities. Results suggest that the effects of herbivores depend upon the initial conditions of the benthic community, and this may have implications for management practices for disturbed, degraded and healthy reefs. Herbivores, particularly browsing fish that can consume mature macroalgae, appear to be limited in their capacity to remove established macroalgae. These critical species appear to be present in low abundance in some habitats, and are targeted as part of a local fishery. In contrast, other herbivores (grazers that consume turf algae and immature macroalgae) appear to readily limit the development of macroalgal communities. I also found that herbivores differentially influence the richness of macroalgal communities depending on the initial macroalgal community. Specifically, an initial presence of the mature macroalga, Turbinaria ornata, enhanced richness of macroalgal assemblage even as herbivore pressure increased. At the same level of herbivore pressure, communities with Turbinaria present had greater richness than communities that initially were dominated by turf algae, even after two years. Results from this experiment provide some of the first empirical tests of hysteresis (path-dependency) in reef recovery, and reinforce the importance of different herbivore functional groups at different points along the recovery trajectory.

Overall, this research highlights characteristics of macroalgae and interactions between macroalgal and herbivore communities that can drive persistent macroalgal phase shifts in coral reef ecosystems. This information may be used to develop sustainable management and conservation strategies to preserve these valuable ecosystems and the services that they provide for local communities.

Global conditions are changing, leading to novel settings in which ecosystems must operate. In particular, ecological disturbances that were once rare are becoming commonplace, like heatwaves both on land and in the ocean that cause widespread mortality of species and leave behind legacies that pose new challenges to the resilience of contemporary ecosystems. Coral reefs, for example, have historically been afflicted mainly by tropical storms that create reef-scouring waves, but in recent decades, episodes of coral bleaching caused by marine heatwaves have become an additional, prevalent source of mass coral mortality. Tropical storms tend to remove corals from the reef entirely, whereas marine heatwaves that cause coral bleaching kill corals but leave their stony skeletons intact – a type of material legacy. When these structures are left in place, this creates a fundamentally different post-disturbance environment in which reef recovery must take place and poses an uncertain future for these incredibly important ecosystems.

In my dissertation research, I explored how shifting disturbance regimes on coral reefs affect the capacity for these ecosystems to rebound from disturbance and regain their pre-disturbance identity, structure, and function. Through a combination of mathematical modeling, remote sensing, and field experimentation, I compared the impacts of tropical storms and coral bleaching on reef resilience, investigating how dead coral skeletons modify key ecological processes and influence trajectories of community assembly after disturbance. I found that dead coral skeletons impair key ecological processes that underpin coral resilience, like top-down control of macroalgae (spatial competitors of coral) by herbivores, and the successful recruitment of new coral colonies. The impairment of these two critical processes can erode coral resilience and ultimately increase the occurrence of transitions from reefs dominated by corals to those dominated by macroalgae. More encouragingly, however, I found that removing dead skeletons after bleaching can mitigate these negative impacts, offering a promising avenue to explore for the management of coral reefs that have been perturbed by disturbances that leave in place large standing stocks of dead coral skeleton. As material legacies become more prominent ecological features, a critical need emerges to understand the powerful roles they play in altering ecosystem resilience, as well as the roles we may be able to play in leveraging these legacies for desirable management outcomes.