Specificity, stability and comparative physiology of coral-Symbiodinium mutualisms: Evaluating the potential for acclimation and/or adaptation in reef corals

The relationship between reef corals and endosymbiotic dinoflagellates is fundamental to the existence of coral reefs. To evaluate the fidelity of coral-Symbiodinium mutualisms, corals maintained in aquaria for years were analyzed by denaturant gradient gel electrophoresis (DGGE). Comparing Symbiodinium populations of captive aquarium colonies with known associations in nature is a practical way of examining partner flexibility. The finding of "normal" symbiont populations in corals existing under highly variable conditions supports the premise that most coral colonies possess stable associations. High sensitivity real-time PCR (rtPCR) was used to evaluate background populations of the putatively stress-tolerant Symbiodinium D in reef corals of the Caribbean. Analyses of samples collected during periods of environmental stability indicate the ability of Symbiodinium D to associate with a wider diversity of host taxa than previously recognized. To gain a broader perspective with regard to the ecology of Symbiodinium D1a, rtPCR and DGGE were used to evaluate the symbiont populations of reef corals from Barbados before and after the 2005 mass coral bleaching. Background populations were observed in 56% of the host genera prior to observations of bleaching. These findings indicate that 'stress', not 'bleaching', caused the displacement of 'natural' symbiont population and the opportunistic proliferation of D1a in many host taxa. Of the 12 host taxa monitored before and after the bleaching event, there was a 40% increase in colonies hosting Symbiodinium D1a. Together, these studies elucidate the mechanism responsible for recent observations reporting the emergence of Symbiodinium D following thermal disturbances. These observations are now most easily explained as the disproportionate growth of existing in hospite symbiont populations, rather than novel symbiont acquisition subsequent to bleaching. To evaluate the comparative "fitness" of corals able to host multiple symbiont types, rates of calcification were measured in P. verrucosa hosting either Symbiodinium C1b-c or D1 at elevated temperature. Rates of calcification decreased significantly for both host-symbiont combinations, but differences attributable to symbiont composition were not detected. This research improves our knowledge of the symbiosis biology and ecology of reef corals and contributes information necessary to most accurately predict the response of these ecosystems to global climate changes.

The Impact of Hurricane Georges on Soft-Bottom, Back Reef Communitites: Site- and Species-Specific Effects in South Florida Seagrass Beds

Seagrass beds are the dominant benthic marine communities in the back reef environment of the Florida Keys. At a network of 30 permanent monitoring stations in this back reef environment, the seagrass Thalassia testudinum Banks & Soland. ex Koenig was the most common marine macrophyte, but the seagrasses Syringodium fi liforme Kuetz., and Halodule wrightii Aschers., as well as many taxa of macroalgae, were also commonly encountered. The calcareous green macroalgae, especially Halimeda spp. and Penicillus spp., were the most common macroalgae. The passage of Hurricane Georges on September 25, 1998 caused an immediate loss of 3% of the density of T. testudinum, compared to 19% of the S. fi liforme and 24% of the calcareous green algae. The seagrass beds at three of the stations were completely obliterated by the storm. Stations that had little to moderate sediment deposition recovered from the storm within 1 yr, while the station buried by 50 cm of sediment and the two stations that experienced substantial erosion had recovered very little during the 3 yrs after the storm. Early colonizers to these severely disturbed sites were calcareous green algae. Hurricanes may increase benthic macrophyte diversity by creating disturbed patches with the landscape, but moderate storm disturbance may actually reduce macrophyte diversity by removing the early successional species from mixed-species seagrass beds.

Diel Patterns of Patch Reef Community Dynamics in a Caribbean Back-Reef System

Back-reef seascapes represent critical habitat for juvenile and adult fishes. Patch reef, seagrass, and mangrove habitats form a heterogeneous mosaic, often linked by species that use reefs as structure during the day and make foraging migrations into soft-bottom habitat at night. Artificial reefs are used to model natural patch reefs, however may not function equivalently as fish habitat. To study the relative value of natural and artificial patch reefs as fish habitat, these communities in the Sea of Abaco, Bahamas were compared using roving diver surveys and time-lapse photography. Diel turnover in fish abundance, recorded with time-lapse photography and illuminated by infrared light, was quantified across midday, dusk, and night periods to explore possible effects of reef type (artificial vs. natural) on these patterns. Diurnal communities on natural reefs exhibited greater fish abundance, species richness, and functional diversity compared to artificial reefs. Furthermore, both types of reef communities exhibited a significant shift across the diel period, characterized by a decline in total fish density at night, especially for grunts (Haemulidae). Cross-habitat foraging migrations by diurnal or nocturnal species, such as haemulids, are likely central drivers of this twilight turnover and can represent important energy and nutrient subsidies. Time-lapse surveys provided more consistent measures of reef fish assemblages for the smaller artificial reef habitats, yet underestimated abundance of certain taxa and species richness on larger patch habitats when compared to the roving diver surveys. Time-lapse photography complemented with infrared light represent a valuable non-invasive approach to studying behavior of focal species and their fine-scale temporal dynamics in shallow-reef communities.

High natural gene expression variation in the reef-building coral Acropora millepora: potential for acclimative and adaptive plasticity

Background: Ecosystems worldwide are suffering the consequences of anthropogenic impact. The diverse ecosystem of coral reefs, for example, are globally threatened by increases in sea surface temperatures due to global warming. Studies to date have focused on determining genetic diversity, the sequence variability of genes in a species, as a proxy to estimate and predict the potential adaptive response of coral populations to environmental changes linked to climate changes. However, the examination of natural gene expression variation has received less attention. This variation has been implicated as an important factor in evolutionary processes, upon which natural selection can act. Results: We acclimatized coral nubbins from six colonies of the reef-building coral Acropora millepora to a common garden in Heron Island (Great Barrier Reef, GBR) for a period of four weeks to remove any site-specific environmental effects on the physiology of the coral nubbins. By using a cDNA microarray platform, we detected a high level of gene expression variation, with 17% (488) of the unigenes differentially expressed across coral nubbins of the six colonies (jsFDR-corrected, p < 0.01). Among the main categories of biological processes found differentially expressed were transport, translation, response to stimulus, oxidation-reduction processes, and apoptosis. We found that the transcriptional profiles did not correspond to the genotype of the colony characterized using either an intron of the carbonic anhydrase gene or microsatellite loci markers. Conclusion: Our results provide evidence of the high inter-colony variation in A. millepora at the transcriptomic level grown under a common garden and without a correspondence with genotypic identity. This finding brings to our attention the importance of taking into account natural variation between reef corals when assessing experimental gene expression differences. The high transcriptional variation detected in this study is interpreted and discussed within the context of adaptive potential and phenotypic plasticity of reef corals. Whether this variation will allow coral reefs to survive to current challenges remains unknown.

Does landscape context affect habitat value? The importance of seascape ecology in back-reef systems

Seascape ecology provides a useful framework from which to understand the processes governing spatial variability in ecological patterns. Seascape context, or the composition and pattern of habitat surrounding a focal patch, has the potential to impact resource availability, predator-prey interactions, and connectivity with other habitats. For my dissertation research, I combined a variety of approaches to examine how habitat quality for fishes is influenced by a diverse range of seascape factors in sub-tropical, back-reef ecosystems. In the first part of my dissertation, I examined how seascape context can affect reef fish communities on an experimental array of artificial reefs created in various seascape contexts in Abaco, Bahamas. I found that the amount of seagrass at large spatial scales was an important predictor of community assembly on these reefs. Additionally, seascape context had differing effects on various aspects of habitat quality for the most common reef species, White grunt Haemulon plumierii. The amount of seagrass at large spatial scales had positive effects on fish abundance and secondary production, but not on metrics of condition and growth. The second part of my dissertation focused on how foraging conditions for fish varied across a linear seascape gradient in the Loxahatchee River estuary in Florida, USA. Gray snapper, Lutjanus griseus, traded food quality for quantity along this estuarine gradient, maintaining similar growth rates and condition among sites. Additional work focused on identifying major energy flow pathways to two consumers in oyster-reef food webs in the Loxahatchee. Algal and microphytobenthos resource pools supported most of the production to these consumers, and body size for one of the consumers mediated food web linkages with surrounding mangrove habitats. All of these studies examined a different facet of the importance of seascape context in governing ecological processes occurring in focal habitats and underscore the role of connectivity among habitats in back-reef systems. The results suggest that management approaches consider the surrounding seascape when prioritizing areas for conservation or attempting to understand the impacts of seascape change on focal habitat patches. For this reason, spatially-based management approaches are recommended to most effectively manage back-reef systems.

Macroalgae Decrease Growth and Alter Microbial Community Structure of the Reef-Building Coral, Porites astreoides

With the continued and unprecedented decline of coral reefs worldwide, evaluating the factors that contribute to coral demise is of critical importance. As coral cover declines, macroalgae are becoming more common on tropical reefs. Interactions between these macroalgae and corals may alter the coral microbiome, which is thought to play an important role in colony health and survival. Together, such changes in benthic macroalgae and in the coral microbiome may result in a feedback mechanism that contributes to additional coral cover loss. To determine if macroalgae alter the coral microbiome, we conducted a field-based experiment in which the coral Porites astreoides was placed in competition with five species of macroalgae. Macroalgal contact increased variance in the coral-associated microbial community, and two algal species significantly altered microbial community composition. All macroalgae caused the disappearance of a γ-proteobacterium previously hypothesized to be an important mutualist of P. astreoides. Macroalgal contact also triggered: 1) increases or 2) decreases in microbial taxa already present in corals, 3) establishment of new taxa to the coral microbiome, and 4) vectoring and growth of microbial taxa from the macroalgae to the coral. Furthermore, macroalgal competition decreased coral growth rates by an average of 36.8%. Overall, this study found that competition between corals and certain species of macroalgae leads to an altered coral microbiome, providing a potential mechanism by which macroalgae-coral interactions reduce coral health and lead to coral loss on impacted reefs.

Development of Gene Expression Markers of Acute Heat-Light Stress in Reef-Building Corals of the Genus Porites

Coral reefs are declining worldwide due to increased incidence of climate-induced coral bleaching, which will have widespread biodiversity and economic impacts. A simple method to measure the sub-bleaching level of heat-light stress experienced by corals would greatly inform reef management practices by making it possible to assess the distribution of bleaching risks among individual reef sites. Gene expression analysis based on quantitative PCR (qPCR) can be used as a diagnostic tool to determine coral condition in situ. We evaluated the expression of 13 candidate genes during heat-light stress in a common Caribbean coral Porites astreoides, and observed strong and consistent changes in gene expression in two independent experiments. Furthermore, we found that the apparent return to baseline expression levels during a recovery phase was rapid, despite visible signs of colony bleaching. We show that the response to acute heat-light stress in P. astreoides can be monitored by measuring the difference in expression of only two genes: Hsp16 and actin. We demonstrate that this assay discriminates between corals sampled from two field sites experiencing different temperatures. We also show that the assay is applicable to an Indo-Pacific congener, P. lobata, and therefore could potentially be used to diagnose acute heat-light stress on coral reefs worldwide.

Acclimatization of the tropical reef coral Acropora millepora to hyperthermal stress

The demise of reef-building corals potentially lies on the horizon, given ongoing climate change amid other anthropogenic environmental stressors. If corals cannot acclimatize or adapt to changing conditions, dramatic declines in the extent and health of the living reefs are expected within the next half century. The primary and proximal global threat to corals is climate change. Reef-building corals are dependent upon a nutritional symbiosis with photosynthetic dinoflagellates belonging to the group Symbiodinium. . The symbiosis between the cnidarian host and algal partner is a stress-sensitive relationship; temperatures just 1°C above normal thermal maxima can result in the breakdown of the symbiosis, resulting in coral bleaching (the loss of Symbiodinium and/or associated photopigments) and ultimately, colony death. As ocean temperatures continue to rise, corals will either acclimatize or adapt to changing conditions, or will perish. By experimentally preconditioning the coral Acropora millepora via sublethal heat treatment, the coral acquired thermal tolerance, resisting bleaching during subsequent hyperthermal stress. The complex nature of the coral holobiont translates to multiple possible explanations for acclimatization: acquired thermal tolerance could potentially originate from the host itself, the Symbiodinium, or from the bacterial community associated with the coral. By examining the type of in hospite Symbiodinium and the bacterial community prior acclimation and after thermal challenge, it is shown that short-term acclimatization is not due to a distinct change in the dinoflagellate or prokaryote community. Though the microbial partnerships remain without considerable flux in preconditioned corals, the host transcriptome is dynamic. One dominant pattern was the apparent tuning of gene expression observed between preconditioned and non-preconditioned treatments, showing a modulated transcriptomic response to stress. Additionally several genes were upregulated in association with thermal tolerance, including antiapoptotic genes, lectins, and oxidative stress response genes. Upstream of two of these thermal tolerance genes, inhibitor of NFκB and mannose-binding lectin, DNA polymorphisms were identified which vary significantly between the northern and southern Great Barrier Reef. The impact of these mutations in putative promoter regions remains to be seen, but variation across thermally-disparate geography serves to generate hypotheses regarding the role of regulatory element evolution in a coral adaptation context.

Density-Dependent Effects of Coral Reef Restoration on Herbivory and Community Interactions

Coral reefs are among the most productive ecosystems in the world. Yet, with their recent declines due to disease, climate change, and overfishing, restoration of these habitats is one of the main concerns for ecologists, resource managers, and government organizations. Coral reef restoration aims to promote key ecosystem processes to shift these habitats to their historical state of high coral cover, but few studies have focused on effective ways to promote resilience. In addition, little is known about the impact of restoration on the fish communities. The aim of this study is to understand how the community of herbivorous fishes is affected by the density of coral outplants inside a special protection area located in the Florida Keys National Marine Sanctuary. Grazing rates, number of visits and time spent foraging were compared using video footage of sites previously devoid of corals, and six months after coral restorations had occurred. Coral transplantations did not appear to attract herbivores nor increase grazing rates of fishes. Instead Sparisoma and Acanthurus fishes appear to respond to changes in the environment by modifying their grazing behavior. However, there was an observed increase in visits by Acanthurus species after transplantation for all the sites sampled within the reef. These fishes seemed to prefer low coral cover sites for grazing. This study highlights the importance of examining coral restorations impacts at the community level. Understanding how restoration influences herbivores and other guilds of reef fishes will allow individuals to not only determine if these habitats are returning to their “original” state, but provide more information on the ways these systems cope with changes in the environment.

A Comparative Study of Concurrent Acoustic and Diver Survey Data, and Fish Community Descriptions of a High Latitude Coral Reef, Florida, USA

Fisheries independent data on relatively unstudied nekton communities were used to explore the efficacy of new tools to be applied in the investigation of shallow coastal coral reef habitats. These data obtained through concurrent diver visual and acoustic surveys provided descriptions of spatial community distribution patterns across seasonal temporal scales in a previously undocumented region. Fish density estimates by both diver and acoustic methodologies showed a general agreement in ability to detect distributional patterns across reef tracts, though magnitude of density estimates were different. Fish communities in southeastern Florida showed significant trends in spatial distribution and seasonal abundance, with higher estimates of biomass obtained in the dry season. Further, community composition shifted across reef tracts and seasons as a function of the movements of several key reef species.

Non-consumptive effects of predators in coral reef communities and the indirect consequences of marine protected areas

Predators exert strong direct and indirect effects on ecological communities by intimidating their prey. Non-consumptive effects (NCEs) of predators are important features of many ecosystems and have changed the way we understand predator-prey interactions, but are not well understood in some systems. For my dissertation research I combined a variety of approaches to examine the effect of predation risk on herbivore foraging and reproductive behaviors in a coral reef ecosystem. In the first part of my dissertation, I investigated how diet and territoriality of herbivorous fish varied across multiple reefs with different levels of predator biomass in the Florida Keys National Marine Sanctuary. I show that both predator and damselfish abundance impacted diet diversity within populations for two herbivores in different ways. Additionally, reef protection and the associated recovery of large predators appeared to shape the trade-off reef herbivores made between territory size and quality. In the second part of my dissertation, I investigated context-dependent causal linkages between predation risk, herbivore foraging behavior and resource consumption in multiple field experiments. I found that reef complexity, predator hunting mode, light availability and prey hunger influenced prey perception of threat and their willingness to feed. This research argues for more emphasis on the role of predation risk in affecting individual herbivore foraging behavior in order to understand the implications of human-mediated predator removal and recovery in coral reef ecosystems.^

Non-Consumptive Effects of Predators in Coral Reef Communities and the Indirect Consequences of Marine Protected Areas

Predators exert strong direct and indirect effects on ecological communities by intimidating their prey. Non-consumptive effects (NCEs) of predators are important features of many ecosystems and have changed the way we understand predator-prey interactions, but are not well understood in some systems. For my dissertation research I combined a variety of approaches to examine the effect of predation risk on herbivore foraging and reproductive behaviors in a coral reef ecosystem. In the first part of my dissertation, I investigated how diet and territoriality of herbivorous fish varied across multiple reefs with different levels of predator biomass in the Florida Keys National Marine Sanctuary. I show that both predator and damselfish abundance impacted diet diversity within populations for two herbivores in different ways. Additionally, reef protection and the associated recovery of large predators appeared to shape the trade-off reef herbivores made between territory size and quality. In the second part of my dissertation, I investigated context-dependent causal linkages between predation risk, herbivore foraging behavior and resource consumption in multiple field experiments. I found that reef complexity, predator hunting mode, light availability and prey hunger influenced prey perception of threat and their willingness to feed. This research argues for more emphasis on the role of predation risk in affecting individual herbivore foraging behavior in order to understand the implications of human-mediated predator removal and recovery in coral reef ecosystems.

Investigating Stakeholders’ Preferences for Coral Reef Research Funding in Florida

Abstract: Heavily used and highly valuable, the Florida Reef is one of the world's most threatened ecosystems. Stakeholders from a densely urbanized coastal region in proximity to the reef system recognize its degradation, but their comprehension of climate change and commitment to pay for sustainable management and research funding have been opaque. With an emphasis on recreational anglers, residential stakeholders were surveyed online about their marine activities, perceptions of resources and threats, and willingness to pay (WTP) for dedicated coral reef research funding in Florida. The majority of stakeholders are wealthy, well educated, and politically independent. Supermajorities favored the two scenarios of taxation for a Florida Coral Reef Research Fund, and the scenario with matching federal funds earned higher support. In regression analyses, several factors emerged as significant contributors to stakeholders’ preferences, and the four recurring factors in extended models were prioritizing the environment over the economy, donating to environmental causes, concern about coral reefs, and concern about climate change, with the latter indicating a recent shift of opinion. Status in terms of income and education were found insignificant, and surprisingly income was negatively correlated with WTP. Perceptions through lenses of environmental and emotional attachments appear to overwhelm conventional status-based factors. Applied statewide, the first scenario's extrapolated WTP (based on a sales tax rate of 2.9%) would generate $675 million annually, and the extrapolated WTP under the second scenario, with matching federal funds (based on a sales tax rate of 3.0%) would generate $1.4 billion. Keywords: willingness to pay, coral reef research, taxation, climate change, stakeholder, perceptions, Florida Reef, recreational fishing, anglers

Does Landscape Context Affect Habitat Value? The Importance of Seascape Ecology in Back-reef Systems

Seascape ecology provides a useful framework from which to understand the processes governing spatial variability in ecological patterns. Seascape context, or the composition and pattern of habitat surrounding a focal patch, has the potential to impact resource availability, predator-prey interactions, and connectivity with other habitats. For my dissertation research, I combined a variety of approaches to examine how habitat quality for fishes is influenced by a diverse range of seascape factors in sub-tropical, back-reef ecosystems. In the first part of my dissertation, I examined how seascape context can affect reef fish communities on an experimental array of artificial reefs created in various seascape contexts in Abaco, Bahamas. I found that the amount of seagrass at large spatial scales was an important predictor of community assembly on these reefs. Additionally, seascape context had differing effects on various aspects of habitat quality for the most common reef species, White grunt Haemulon plumierii. The amount of seagrass at large spatial scales had positive effects on fish abundance and secondary production, but not on metrics of condition and growth. The second part of my dissertation focused on how foraging conditions for fish varied across a linear seascape gradient in the Loxahatchee River estuary in Florida, USA. Gray snapper, Lutjanus griseus, traded food quality for quantity along this estuarine gradient, maintaining similar growth rates and condition among sites. Additional work focused on identifying major energy flow pathways to two consumers in oyster-reef food webs in the Loxahatchee. Algal and microphytobenthos resource pools supported most of the production to these consumers, and body size for one of the consumers mediated food web linkages with surrounding mangrove habitats. All of these studies examined a different facet of the importance of seascape context in governing ecological processes occurring in focal habitats and underscore the role of connectivity among habitats in back-reef systems. The results suggest that management approaches consider the surrounding seascape when prioritizing areas for conservation or attempting to understand the impacts of seascape change on focal habitat patches. For this reason, spatially-based management approaches are recommended to most effectively manage back-reef systems.