Influence of marine-based industries on coral health and disease

The recent global emergence of coral disease outbreaks and subsequent coral mortality is commonly linked with human activities, however almost nothing is known about the influence of marine-based industries on coral disease. Given the growing demand for coastal development and natural resource extraction in locations that overlap with coral reefs, and growth of industries that rely on coral reefs, particularly tourism and fishing, resource managers need tools to combat coral disease epizootics and prevent future outbreaks. Research presented in this thesis identifies factors associated with industries that influence coral disease and evaluates existing and potential management tools for mitigating their impacts.\ud \ud Concentrating tourism activities can be an effective way to closely manage high-use parks and minimise the effects of visitors on plants and animals, however, the effects of reef-based tourist facilities on coral health have not been assessed. In partnership with reef managers and the tourism industry, in Chapter 2, I test the effectiveness of concentrating tourism activities on reefs with and without permanent tourist platforms as a strategy for managing tourism on coral reefs in the Great Barrier Reef Marine Park. Coral diseases were 15 times more prevalent at reefs with offshore tourism platforms than at nearby reefs without platforms. The maximum prevalence and maximum number of cases of each disease type occurred at reefs with permanently moored tourism platforms. Diseases affected 10 coral genera from 7 families at reefs with platforms, but only 4 coral genera from 3 families at reefs without platforms. The greatest number of disease cases occurred within the spatially dominant acroporid corals, which exhibited 18-fold greater disease prevalence at reefs with versus without platforms. Neither the percent cover of acroporids nor overall coral cover differed significantly between reefs with and without platforms, which suggests that neither factor was responsible for the elevated levels of disease. Identifying how tourism activities facilitate coral disease will help ensure ongoing conservation of coral assemblages and tourism.\ud \ud Recreational scuba diving on coral reefs is one of the fastest growing tourism sectors globally. Although physical injury and sedimentation associated with intensive dive tourism has been documented extensively, other impacts on coral health are unknown. In Chapter 3, I compare the prevalence of 4 coral diseases and 8 other indicators of compromised health at five of the highest and lowest used dive sites around the small community-managed island of Koh Tao, Thailand. The mean prevalence of healthy corals at low-use sites (79%) was twice that at high-use sites (45%). I found a 3-fold increase in coral disease prevalence at high-use sites, and significant increases in sponge overgrowth, physical injury, tissue necrosis from sediment, and non-normally pigmented coral tissues. Sediment necrosis was strongly associated with white syndrome prevalence across all sites. Injured corals were more susceptible to skeletal eroding band disease only at high-use sites, suggesting that additional stressors associated with use intensity facilitate disease development. Unexpectedly, I observed 113 corals entangled in derelict fishing line, of which 87% had ciliates associated with skeletal eroding band disease initiating from lesion boundaries, increasing disease susceptibility 5-fold compared to non-entangled corals, an unreported mechanism of coral mortality associated with fishing gear. Use of numerous indicators of coral health increases understanding of impacts associated with rapid tourism growth. Identifying practical management strategies, such as spatially separating multiple reef-based activities, is necessary to balance the expansion of tourism and maintenance of coral health.\ud \ud The rapid pace of coastal development near sensitive coral reef ecosystems necessitates a comprehensive understanding of the impacts that development activities have on all aspects of coral health. While elevated sedimentation and turbidity are often cited as drivers of reef decline, their influence on coral disease prevalence has never been investigated in situ. In Chapter 4, coral health surveys were conducted along a dredging-associated sediment plume gradient to assess the relationship between sedimentation, turbidity and coral health near Montebello and Barrow Islands, Western Australia. Reefs exposed to the highest number of days under the sediment plume (296 to 347 days) had 2-fold higher levels of disease, largely driven by increases in white syndromes, and a 6-fold increase in other signs of compromised coral health, relative to reefs with little or no plume exposure (0 to 9 days). Multivariate modeling and ordination incorporating sediment exposure level, coral community composition and cover, predation and multiple thermal stress indices provided further confirmation that the level of sediment plume exposure was the main driver of elevated disease and other indicators of compromised coral health. This study provides the first empirical evidence linking sedimentation and turbidity with elevated coral disease prevalence in situ. Minimising sedimentation and turbidity associated with coastal development will provide an important management tool for controlling coral disease epizootics.\ud \ud A limited number of options are available for directly managing diseases in marine environments. In Chapter 5, the utility of marine reserves for mitigating coral disease was assessed for the first time in the Great Barrier Reef Marine Park. Comparisons of coral disease assemblages and the prevalence of six individual diseases among sites with protection versus sites with fishing revealed that no-take reserves resulted in a 3- fold reduction in pooled coral disease prevalence. Of the 31 explanatory factors tested, including habitat and environmental characteristics, fish assemblages, and differences in fishing gear restrictions, a multivariate regression demonstrated that protection from fishing was the primary factor explaining variability in coral disease assemblages. Further, significant partial correlations with coral damage and the abundance of derelict fishing line indicate that direct damage associated with line fishing is the primary driver of differences between protection levels. Gear restrictions within fished zones did not improve coral health, instead I found significantly greater levels of skeletal eroding band disease, white syndromes, coral damage, and derelict fishing line when gear was restricted, compared to unrestricted. Moreover, within fished zones, the prevalence of skeletal eroding band disease, coral damage, and fishing line increased with increasing proximity to the nearest reserve boundary, signifying that fishers target areas just outside of reserve boundaries due to ease of accessibility from boat moorings located within reserves or perceptions that fish stocks are less depleted near reserve boundaries. This study concludes that both protection from fishing and spatially managing use-intensity within fished areas are important strategies to improve coral health.\ud \ud This thesis consistently demonstrates that reducing stressors associated with marine-based industries can ameliorate coral health and alleviate the impacts of disease. Identifying and implementing effective management strategies to improve coral health represent practical tools for increasing the resilience of vulnerable reef ecosystems in a changing climate and developing world

Ecology and Pathology of Novel Plaque-Like Growth Anomalies Affecting a Reef-Building Coral on the Great Barrier Reef

Here we identify ecological and structural characteristics of a novel plaque-like growth anomaly (GA) at outbreak levels in a population of the staghorn coral, Acropora muricata, on the Great Barrier Reef. The smooth appearance of the plaques results from thickening of skeletal structures comprising the coenosteum, leading to infilling of spaces between corallites, and was associated with hyperplasia and hypertrophy of calicodermal cells. This resulted in a 2-fold reduction in corallite height, a 1.6-fold increase in corallite width, and a 2.3-fold increase in the thickness of the calicodermal layer compared to healthy corallites. Plaque-like GAs affected ~67% of corals surveyed, and on average, encased 50% of the surface area of diseased branches. Progression rates along branches averaged 0.22mm day-1 over a 2.5-month period. GAs spread throughout colonies but their presence did not affect the linear extension rates of branches. Reproductive products were absent in 55% of GA tissues, and when present, mean oocyte and spermary numbers were reduced by 50%. However, when present, mean sizes of oocytes and spermaries did not differ between healthy and GA tissues. Symbiodinium densities were also reduced by 50% in polyps within GA tissues, which were characterized by an absence of polyp structure and chaotic arrangement of gastrovascular canals, compromising host nutrition. A 3-fold increase in stores of the immune-related precursor, prophenoloxidase, within GA tissues compared to healthy tissue suggests a primed immune response. Concomitantly, only 35% of prophenoloxidase was converted to the active enzyme phenoloxidase compared to 81% in healthy tissues, consistent with inhibition of immune-related enzymatic reactions by an unknown causative agent. The increasing frequency of emerging disease hotspots highlights the importance of understanding sublethal effects of diseases that have important implications for the fitness and long-term resilience of coral populations

Scuba diving damage and intensity of tourist activities increases coral disease prevalence

Recreational diving and snorkeling on coral reefs is one of the fastest growing tourism sectors globally. Damage associated with intensive recreational tourist use has been documented extensively on coral reefs, however other impacts on coral health are unknown. Here, we compare the prevalence of 4 coral diseases and 8 other indicators of compromised coral health at high and low use dive sites around the island of Koh Tao, Thailand. Surveys of 10,499 corals reveal that the mean prevalence of healthy corals at low use sites (79%) was twice that at high use sites (45%). We also found a 3-fold increase in coral disease prevalence at high use sites, as well as significant increases in sponge overgrowth, physical injury, tissue necrosis from sediment, and non-normally pigmented coral tissues. Injured corals were more susceptible to skeletal eroding band disease only at high use sites, suggesting that additional stressors associated with use intensity facilitate disease development. Sediment necrosis of coral tissues was strongly associated with the prevalence of white syndromes, a devastating group of diseases, across all sites. We did not find significant differences in mean levels of coral growth anomalies or black band disease between high and low use sites. Our results suggest that several indicators of coral health increase understanding of impacts associated with rapid tourism development. Identifying practical management strategies, such as spatial management of multiple reef-based activities, is necessary to balance growth of tourism and maintenance of coral reefs

Assessing baseline levels of coral health in a newly established marine protected area in a global scuba diving hotspot

While coral reefs are increasingly threatened worldwide, they are also increasingly used for recreational activities. Given the environmental and socio-economic significance of coral reefs, understanding the links between human activities and coral health and evaluating the efficacy of marine protected areas (MPAs) as a management regime to prevent further deterioration are critically important. The aim of this study was to quantify indicators of coral health at sites inside and outside a newly rezoned MPA framework in the dive tourism hotspot of Koh Tao, Thailand. We found that patterns in the health and diversity of coral communities one year on did not reflect the protected status conferred by newly zoned MPAs, but instead reflected past history of recreational use around the island. Sites characterised as past high-use sites had lower mean percent cover of hard corals overall and of corals in the typically disease- and disturbance-susceptible family Acroporidae, but higher mean cover of species in the more weedy family Agariciidae. Past high use sites also had higher mean prevalence of infectious diseases and other indicators of compromised health. Sites within the newly established MPAs are currently subjected to higher levels of environmental and anthropogenic pressures, with sedimentation, algal overgrowth, feeding scars from Drupella snails, and breakage particularly prevalent compared to sites in non-MPA areas. Given the greater prevalence of these factors within protected sites, the capacity of the MPA framework to effectively prevent further deterioration of Koh Tao's reefs is unclear. Nevertheless, our study constitutes a strong baseline for future long-term evaluations of the potential of MPAs to maintain coral health and diversity on highly threatened reefs

Protected areas mitigate diseases of reef-building corals by reducing damage from fishing

Parks and protected areas have been instrumental in reducing anthropogenic sources of damage in terrestrial and aquatic environments. Pathogen invasion often succeeds physical wounding and injury, yet links between the reduction of damage and the moderation of disease have not been assessed. Here, we examine the utility of no-take marine reserves as tools for mitigating diseases that affect reef-building corals. We found that sites located within reserves had fourfold reductions in coral disease prevalence compared to non-reserve sites (80 466 corals surveyed). Of 31 explanatory variables assessed, coral damage and the abundance of derelict fishing line best explained differences in disease assemblages between reserves and non-reserves. Unexpectedly, we recorded significantly higher levels of disease, coral damage, and derelict fishing line in non-reserves with fishing gear restrictions than in those without gear restrictions. Fishers targeting stocks perceived to be less depleted, coupled with enhanced site access from immediately adjacent boat moorings, may explain these unexpected patterns. Significant correlations between the distance from mooring sites and prevalence values for a ciliate disease known to infest wounded tissue (r = −0.65), coral damage (r = −0.64), and the abundance of derelict fishing line (r = −0.85) corroborate this interpretation. This is the first study to link disease with recreational use intensity in a park, emphasizing the need to evaluate the placement of closures and their direct relationship to ecosystem health. Since corals are modular, ecological processes that govern reproductive and competitive fitness are frequently related to colony surface area therefore, even low levels of cumulative tissue loss from progressing diseases pose significant threats to reef coral persistence. Disease mitigation through reductions in physical injury in areas where human activities are concentrated is another mechanism by which protected areas may improve ecosystem resilience in a changing climate

Ecology and pathology of novel plaque-like growth anomalies affecting a reef-building coral on the great barrier reef

Here we identify ecological and structural characteristics of a novel plaque-like growth anomaly (GA) at outbreak levels in a population of the staghorn coral, Acropora muricata, on the Great Barrier Reef. The smooth appearance of the plaques results from thickening of skeletal structures comprising the coenosteum, leading to infilling of spaces between corallites, and was associated with hyperplasia and hypertrophy of calicodermal cells. This resulted in a two-fold reduction in corallite height, a 1.6-fold increase in corallite width, and a 2.3-fold increase in the thickness of the calicodermal layer compared to healthy corallites. Plaque-like GAs affected ~67% of corals surveyed, and on average, encased 50% of the surface area of diseased branches. Progression rates along branches averaged 0.22 mm day over a 2.5-month period. GAs spread throughout colonies but their presence did not affect the linear extension rates of branches. Reproductive products were absent in 55% of GA tissues, and when present, mean oocyte and spermary numbers were reduced by 50%. However, when present, mean sizes of oocytes and spermaries did not differ between healthy and GA tissues. Symbiodinium densities were also reduced by 50% in polyps within GA tissues, which were characterized by an absence of polyp structure and chaotic arrangement of gastrovascular canals, compromising host nutrition. A three-fold increase in stores of the immune-related precursor, prophenoloxidase, within GA tissues compared to healthy tissue suggests a primed immune response. Concomitantly, only 35% of prophenoloxidase was converted to the active enzyme phenoloxidase compared to 81% in healthy tissues, consistent with inhibition of immune-related enzymatic reactions by an unknown causative agent. The increasing frequency of emerging disease hotspots highlights the importance of understanding sublethal effects of diseases that have important implications for the fitness and long-term resilience of coral populations

Analyzing Health of Forcibly Displaced Communities through an Integrated Ecological Lens

Health care among forcibly displaced persons is frequently driven by siloed approaches. Aspects of the built environment, social factors, and the bidirectional relationship between the changing ecosystem and residents are often ignored in health policy design and implementation. While recognizing factors that create a preference for siloed approaches and appreciating the work of humanitarian agencies, we argue for a new data-driven and holistic approach to understand the health of the forcibly displaced. It should be rooted in the realities of the emergence of new diseases, dynamic demographics, and degrading environments around the displaced communities. Such an approach envisions refugee and internally displaced camps as dynamic, complex ecosystems that alter, and are altered by, spatial and temporal factors. At the root of this approach is the necessity to work across disciplines, to think holistically, to go beyond treating single ailments, and to develop ethical approaches that provide dignity to those who are forcibly displaced

Appendix A. Additional tables, methods, and results.

Additional tables, methods, and results