1. Kuffner, I.B., E. Bartels, A. Stathakopoulos, I.C. Enochs, G. Kolodziej, L.T. Toth, and D.P. Manzello. Plasticity in skeletal characteristics of nursery-raised staghorn coral, Acropora cervicornis. Coral Reefs, 36(3):679-684, doi:10.1007/s00338-017-1560-2 2017

    Abstract:

    Staghorn coral, Acropora cervicornis, is a threatened species and the primary focus of western Atlantic reef restoration efforts to date. We compared linear extension, calcification rate, and skeletal density of nursery-raised A. cervicornis branches reared for 6 months either on blocks attached to substratum or hanging from PVC trees in the water column. We demonstrate that branches grown on the substratum had significantly higher skeletal density, measured using computerized tomography, and lower linear extension rates compared to water-column fragments. Calcification rates determined with buoyant weighing were not statistically different between the two grow-out methods, but did vary among coral genotypes. Whereas skeletal density and extension rates were plastic traits that depended on grow-out method, calcification rate was conserved. Our results show that the two rearing methods generate the same amount of calcium carbonate skeleton but produce colonies with different skeletal characteristics and suggest that there is genetically-based variability in coral calcification performance.

  2. Staley, C., T. Kaiser, M.L. Gidley, I.C. Enochs, P.R. Jones, K.D. Goodwin, C.D. Sinigalliano, M.J. Sadowsky, and C.L. Chun. A next-generation sequencing approach to characterize the impacts of land-based sources of pollution on the microbiota of southeast Florida coral reefs. Applied and Environmental Microbiology, 83(10):e03378-16, doi:10.1128/AEM.03378-16 2017

    Abstract:

    Coral reefs are dynamic ecosystems known for decades to be endangered due, in large part, to anthropogenic impacts from land-based sources of pollution (LBSP). In this study, we utilized an Illumina-based next-generation sequencing approach to characterize prokaryotic and fungal communities from samples collected off the southeast coast of Florida. Water samples from coastal inlet discharges, oceanic outfalls of municipal wastewater treatment plants, treated wastewater effluent before discharge, open ocean samples, and coral tissue samples (mucus and polyps) were characterized to determine relationships between microbial communities in these matrices and those in reef water and coral tissues. Significant differences in microbial communities were noted among all sample types but varied between sampling area. Contamination from outfalls was found to be the greatest potential source of LBSP influencing native microbial community structure among all reef samples, although pollution from inlets was also noted. Notably, reef water and coral tissue communities were found to be more greatly impacted by LBSP at southern reefs, which also experienced the most degradation during the course of the study. Results of this study provide new insights into how microbial communities from LBSP can impact coral reefs in Southeast Florida and suggest that wastewater outfalls may have a greater influence on the microbial diversity and structure of these reef communities than do contaminants carried in runoff although the influence of runoff and coastal inlet discharge on coral reefs are still substantial.

  3. Camp, E.F., D.J. Smith, C. Evenhuis, I. Enochs, D. Manzello, S. Woodcock, and D.J. Suggett. Acclimatization to high-variance habitats does not enhance physiological tolerance of two key Caribbean corals to future temperature and pH. Philosophical Transactions of the Royal Society B, 283(1831):20160442, doi:10.1098/rspb.2016.0442 2016

    Abstract:

    Corals are acclimatized to populate dynamic habitats that neighbor coral reefs. Habitats such as seagrass beds exhibit broad diel changes in temperature and pH that routinely expose corals to conditions predicted for reefs over the next 50-100 years. However, whether such acclimatization effectively enhances physiological tolerance to, and hence provides refuge against, future climate scenarios remains unknown. Also, whether corals living in low-variance habitats can tolerate present-day high-variance conditions remains untested. We experimentally examined how pH and temperature predicted for the year 2100 affects the growth and physiology of two dominant Caribbean corals (Acropora palmata and Porites astreoides) native to habitats with intrinsically low (outer-reef terrace, LV) and/or high (neighboring seagrass, HV) environmental variance. Under present-day temperature and pH, growth and metabolic rates (calcification, respiration, and photosynthesis) were unchanged for HV versus LV populations. Superimposing future climate scenarios onto the HV and LV conditions did not result in any enhanced tolerance to colonies native to HV. Calcification rates were always lower for elevated temperature and/or reduced pH. Together, these results suggest that seagrass habitats may not serve as refugia against climate change if the magnitude of future temperature and pH changes is equivalent to neighboring reef habitats.

  4. Cortés, J., I.C. Enochs, J. Sibjaja-Cordero, L. Hernández, J.J. Alvarado, O. Breedy, J.A. Cruz-Barraza, O. Esquivel-Garrote, C. Fernández-García, A. Hermosillo, K.L. Kaiser, P. Medina-Rosas, A. Morales-Ramírez, C. Pacheco, H. Reyes-Bonilla, R. Riosmena-Rodríguez, C. Sánchez-Noguera, F.A. Zapata, E. Wieters, and A. Pérez-Matus. Marine biodiversity of eastern tropical Pacific coral reefs. In Coral Reefs of the Eastern Tropical Pacific: Persistence and Loss in a Dynamic Environment, P.W. Glynn, D.P. Manzello, and I. Enochs (eds.). Springer Netherlands, 203-250, doi:10.1007/978-94-017-7499-4_7 2016

    Abstract:

    The eastern tropical Pacific (ETP) is an isolated oceanic region exposed to extreme oceanographic conditions, including low salinity, low pH, high temperatures during El Niño, and low temperatures during La Niña and seasonal upwelling. The coral reefs in this region have a relatively limited suite of species compared to other coral reef areas of the world, but much like more diverse reefs the species present interact in complex ways. Here we synthezise the knowledge of taxonomic groups of reef organisms from prokaryotes to vertebrates, including algae, sponges, cnidarians, annelids and other worms, molluscs, crustaceans, echinoderms and fishes. We also present summaries on the biodiversity of associated functional groups and habitats, including (a) reef zooplankton and cryptic fauna, and (b) soft benthic environments, rhodolith beds and mesophotic environments. Several factors that structure the biodiversity of ETP coral reefs are explored, including biological, physical, and chemical controls. ETP coral reefs are relatively simple systems that can be used as models for studying biodiversity and interactions among species. We conclude this review by highlighting pressing research needs, from very basic inventories to more sophisticated studies of cryptic assemblages, and to investigations on the impacts of natural and anthropogenic effects on ETP coral reef biodiversity.

  5. Enochs, I.C., and P.W. Glynn. Corallivory in the eastern Pacific. In Coral Reefs of the Eastern Tropical Pacific: Persistence and Loss in a Dynamic Environment, P.W. Glynn, D.P. Manzello, and I. Enochs (eds.). Springer Netherlands, 315-337, doi:10.1007/978-94-017-7499-4_10 2016

    Abstract:

    Eastern Pacific reef ecosystems are home to a diverse assemblage of corallivorous fishes and invertebrates. It is therefore not surprising that there is a rich history of research on corallivores in the eastern Pacific. In fact, much of what is known today on the topic of corallivory has built upon studies from the eastern Pacific region. Here we review the progression of our understanding of eastern Pacific corallivory and corallivores. We discuss the behavior and ecology of these specialized consumers, dividing our analysis into the larger conspicuous taxa such as the crown-of-thorns sea star (Acanthaster planci) and the guineafowl puffer (Arothron meleagris), as well as into the smaller cryptic species such as the pustulate egg shell (Jenneria pustulata) and coral crustacean guards (Trapezia spp., Alpheus lottini). The majority of species that consume coral tissues are facultative corallivores, feeding on corals only incidentally. Both the negative and positive interactions of corallivores to their prey/hosts are reviewed. We address detrimental direct consumption of coral and how it can ultimately influence growth form, species distributions, population structure, and the asexual reproduction of corals. We examine the cleaning behavior of some corallivorous species, as well as their territorial tendencies, which may potentially lead to the exclusion of more lethal coral predators. Despite the high diversity of corallivore taxa, no population outbreaks have been observed in the eastern Pacific; coral colony growth rates and reef accretion proceed apace. Finally, we explore the far-reaching implications of the corallivore feeding strategy, touching on the connections that ultimately link coral biomass with higher trophic levels and the rest of the reef ecosystem.

  6. Enochs, I.C., and P.W. Glynn. Trophodynamics of eastern Pacific coral reefs. In Coral Reefs of the Eastern Tropical Pacific: Persistence and Loss in a Dynamic Environment, P.W. Glynn, D.P. Manzello, and I. Enochs (eds.). Springer Netherlands, 291-314, doi:10.1007/978-94-017-7499-4_9 2016

    Abstract:

    Trophic interactions on eastern Pacific coral reefs are complex and highly dynamic, ever changing due to numerous biological and physical factors. In this chapter, we first address the sources of energy at the base of food webs, i.e., photosynthetic carbon fixation by benthic algae and endosymbiotic zooxanthellae, secondarily derived organic deposits, detritus, and fecal matter, as well as demersal (within reef) and allochthonous plankton food sources. Next we consider consumers, covering the major reef trophic guilds in the eastern Pacific—suspension feeders, deposit and detritus feeders, herbivores, carnivores (predators and carnivorous grazers), as well as scavengers. The diversity and relative abundance of consumer taxa are described and considered in terms of their ecological roles in community processes. The complex interplay of these guilds is examined through food webs constructed for Panama, Cabo Pulmo reef in the Gulf of California, Mexico, and the Floreana Island rocky reef in the Galápagos Islands. Finally, the effects of physical and biotic perturbations on food webs, interactions, indirect effects, and trophic cascades conclude this review.

  7. Enochs, I.C., D.P. Manzello, A. Tribollet, L. Valentino, G. Kolodziej, E.M. Donham, M.D. Fitchett, R. Carlton, and N.N. Price. Elevated colonization of microborers at a volcanically acidified coral reef. PLoS ONE, 11(7):e0159818, doi:10.1371/journal.pone.0159818 2016

    Abstract:

    Experiments have demonstrated that ocean acidification (OA) conditions projected to occur by the end of the century will slow the calcification of numerous coral species and accelerate the biological erosion of reef habitats (bioerosion). Microborers, which bore holes less than 100 μm diameter, are one of the most pervasive agents of bioerosion and are present throughout all calcium carbonate substrates within the reef environment. The response of diverse reef functional groups to OA is known from real-world ecosystems but, to date, our understanding of the relationship between ocean pH and carbonate dissolution by microborers is limited to controlled laboratory experiments. Here we examine the settlement of microborers to pure mineral calcium carbonate substrates (calcite) along a natural pH gradient at a volcanically acidified reef at Maug, Commonwealth of the Northern Mariana Islands (CNMI). Colonization of pioneer microborers was higher in the lower pH waters near the vent field. Depth of microborer penetration was highly variable both among and within sites (4.2–195.5 μm) over the short duration of the study (3 mo.), and no clear relationship to increasing CO2 was observed. Calculated rates of biogenic dissolution, however, were highest at the two sites closer to the vent and were not significantly different from each other. These data represent the first evidence of OA-enhancement of microboring flora colonization in newly available substrates and provide further evidence that microborers, especially bioeroding chlorophytes, respond positively to low pH. The accelerated breakdown and dissolution of reef framework structures with OA will likely lead to declines in structural complexity and integrity, as well as possible loss of essential habitat.

  8. Enochs, I.C., D.P. Manzello, G. Kolodziej, S.H.C. Noonan, L. Valentino, and K.E. Fabricius. Enhanced macroboring and depressed calcification drive net dissolution at high CO2 coral reefs. Proceedings of the Royal Society B, 283(1842):20161742, doi:10.1098/rspb.2016.1742 2016

    Abstract:

    Ocean acidification (OA) impacts the physiology of diverse marine taxa; among them corals that create complex reef framework structures. Biological processes operating on coral reef frameworks remain largely unknown from naturally high-carbon-dioxide (CO2) ecosystems. For the first time, we independently quantified the response of multiple functional groups instrumental in the construction and erosion of these frameworks (accretion, macroboring, microboring, and grazing) along natural OA gradients. We deployed blocks of dead coral skeleton for roughly 2 years at two reefs in Papua New Guinea, each experiencing volcanically enriched CO2, and employed high-resolution micro-computed tomography (micro-CT) to create three-dimensional models of changing skeletal structure. OA conditions were correlated with decreased calcification and increased macroboring, primarily by annelids, representing a group of bioeroders not previously known to respond to OA. Incubation of these blocks, using the alkalinity anomaly methodology, revealed a switch from net calcification to net dissolution at a pH of roughly 7.8, within Intergovernmental Panel on Climate Change's (IPCC) predictions for global ocean waters by the end of the century. Together these data represent the first comprehensive experimental study of bioerosion and calcification from a naturally high-CO2 reef ecosystem, where the processes of accelerated erosion and depressed calcification have combined to alter the permanence of this essential framework habitat.

  9. Enochs, I.C., D.P. Manzello, H.H. Wirshing, R. Carlton, and J. Serafy. Micro-CT analysis of the Caribbean octocoral Eunicea flexuosa subjected to elevated pCO2. ICES Journal of Marine Science, 73(3):910-919, doi:10.1093/icesjms/fsv159 2016

    Abstract:

    Rising anthropogenic carbon dioxide has resulted in a drop in ocean pH, a phenomenon known as ocean acidification (OA). These acidified waters have many ramifications for diverse marine biota, especially those species which precipitate calcium carbonate skeletons. The permanence of coral reef ecosystems is, therefore, closely related to OA stress as habitat-forming corals will exhibit reduced calcification and growth. Relatively little is known concerning the fate of other constituent taxa which may either suffer concomitant declines or be competitively favored in acidified waters. Here, we experimentally (49 d) test the effects of next century predictions for OA (pH = 7.75, pCO2 = 1081 µatm) vs. near-present-day conditions (pH = 8.01, pCO2 = 498 µatm) on the common Caribbean octocoral Eunicea flexuosa. We measure linear extension of this octocoral and use a novel technique, high-resolution micro-computed tomography, to measure potential differences in the morphology of calcified internal skeletal structures (sclerites) in a 2 mm apical section of each branch. Despite the use of highly accurate procedures, we found no significant differences between treatments in either the growth of E. flexuosa branches or the structure of their sclerites. Our results suggest a degree of resilience to OA stress and provide evidence that this octocoral species may persist on Caribbean coral reefs, despite global change.

  10. Glynn, P.W., D.P. Manzello, and I.C. Enochs (eds.). Coral Reefs of the Eastern Tropical Pacific: Persistence and Loss in a Dynamic Environment. Springer Netherlands, 657 pp., doi:10.1007/978-94-017-7499-4 2016

    Abstract:

    This book documents and examines the state of health of coral reefs in the eastern tropical Pacific region. It touches on the occurrence of coral reefs in the waters of surrounding countries, and it explores their biogeography, biodiversity, and condition relative to the El Niño-Southern Oscillation and human impacts. Additionally contained within is a field that presents information on many of the species presented in the preceding chapters.

  11. Enochs, I.C., D.P. Manzello, E.M. Donham, G. Kolodziej, R. Okano, L. Johnston, C. Young, J. Iguel, C.B. Edwards, M.D. Fox, L. Valentino, S. Johnson, D. Benavente, S.J. Clark, R. Carlton, T. Burton, Y. Eynaud, and N.N. Price. Shift from coral to macroalgae dominance on a volcanically acidified reef. Nature Climate Change, 5(12):1083-1088, doi:10.1038/nclimate2758 2015

    Abstract:

    Rising anthropogenic CO2 in the atmosphere is accompanied by an increase in oceanic CO2 and a concomitant decline in seawater pH. This phenomenon, known as ocean acidification (OA), has been experimentally shown to impact the biology and ecology of numerous animals and plants, most notably those that precipitate calcium carbonate skeletons, such as reef-building corals. Volcanically acidified water at Maug, Commonwealth of the Northern Mariana Islands (CNMI) is equivalent to near-future predictions for what coral reef ecosystems will experience worldwide due to OA. We provide the first chemical and ecological assessment of this unique site and show that acidification-related stress significantly influences the abundance and diversity of coral reef taxa, leading to the often-predicted shift from a coral to an algae-dominated state. This study provides field evidence that acidification can lead to macroalgae dominance on reefs.

  12. Enochs, I.C., D.P. Manzello, R.D. Carton, D.M. Graham, R. Ruzicka, and M.A Collela. Ocean acidification enhances the bioerosion of a common coral reef sponge: Implications for the persistence of the Florida Reef Tract. Bulletin of Marine Science, 91(2):271-290, doi:10.5343/bms.2014.1045 2015

    Abstract:

    The increase in anthropogenic carbon dioxide in seawater, termed ocean acidification (OA), depresses calcification rates of coral and algae, and may contribute toward reef ecosystem degradation. To test how future OA conditions will influence biologically-mediated dissolution (bioerosion) of coral by the common Caribbean boring sponge Pione lampa (de Laubenfels, 1950), we conducted a series of carefully controlled incubations and used changes in total alkalinity (TA) to calculate calcium carbonate dissolution. We present data showing a positive relationship between seawater pCO2 and chemical bioerosion that predict a 99% increase in chemical erosion before the end of the century, more than double the expected decline in coral calcification rate. To examine how OA-enhanced erosion will influence reef ecosystem persistence, we incorporated these and other data into a carbonate budget model of 37 reefs along the Florida Reef Tract (FRT). Our model showed that all FRT reefs had a positive CaCO3 budget [mean = 8.257 (SE 0.8077) kg m−2 yr−1] in preindustrial times, whereas approximately 89% of reefs presently exhibit net erosion. Present-day reef-specific calcification would need to increase by 29.4% to compensate for projected end of the century OA-enhancement of total bioerosion. These findings show that OA may accelerate Caribbean and Atlantic coral reef degradation more rapidly than previously predicted

  13. Manzello, D.P., I.C. Enochs, G. Kolodziej, and R. Carlton. Coral growth patterns of Montastraea cavernosa and Porites astreoides in the Florida Keys: The importance of thermal stress and inimical waters. Journal of Experimental Marine Biology and Ecology, 471:198-207, doi:10.1016/j.jembe.2015.06.010 2015

    Abstract:

    The calcification and extension rates of two species of scleractinian coral (Montastraea cavernosa, Porites astreoides) were measured in corals experimentally transplanted to paired inshore and offshore locations in the Upper, Middle, and Lower Florida Keys from 2010 to 2011. Growth rates were compared with respect to 1) shelf location, 2) species, 3) region, and 4) temperature. Transplanted corals on inshore reefs generally calcified less than those at paired offshore sites, but these differences were only significant in a few cases. This difference in growth is likely because of two thermal stress events that occurred inshore, but not offshore, as growth records from cores of P. astreoides revealed significantly higher extension and calcification inshore from 2001–2013. The core data confirmed that the years 2010–2012 were a period of depressed growth inshore. Calcification and extension rates of the experimental corals were not statistically different between M. cavernosa and P. astreoides within a given site. The only exceptions were that calcification was higher in M. cavernosa at the Middle Keys inshore site. The Middle Florida Keys sites had the lowest rates of calcification, supporting the hypothesis that the influence of Florida Bay waters in this region contributes to poor reef development. Mean calcification rates negatively correlated with metrics of cold stress in M. cavernosa and heat stress in P. astreoides. The lack of a significant correlation between heat stress and mean calcification in M. cavernosa may help explain this species persistence on today's reefs. Maximum calcification and mean extension, however, were negatively correlated with maximum running 30-day mean temperature, showing that the growth of M. cavernosa is not completely insensitive to warm water stress. The ‘weedy’ life-history strategy of P. astreoides may compensate for the sensitivity of calcification rates to heat stress reported here, allowing this species to maintain the stable populations that have been observed throughout Florida and the wider Caribbean.

  14. Manzello, D.P., I.C. Enochs, G. Kolodziej, and R. Carlton. Recent decade of growth and calcification of Orbicella faveolata in the Florida Keys: An inshore-offshore comparison. Marine Ecology Progress Series, 521:81-89, doi:10.3354/meps11085 2015

    Abstract:

    Coral reefs along the Florida Keys portion of the Florida Reef Tract (FRT) have undergone a dramatic decline since the 1980s. Since the 1997-98 El Niño event, coral cover on offshore reefs of the FRT has been ≤ 5% and continues to decline. Mortality of the framework-constructing coral in the Orbicella (formerly Montastraea) annularis species complex has driven this recent loss in overall coral cover. One exception to this decline occurred on the inshore patch reefs of the Florida Keys, where coral cover has remained relatively high. We examined the growth and calcification of Orbicella faveolata, an ecologically important subspecies of the O. annularis complex, at both an inshore and offshore reef site representing this dichotomy of present-day coral cover. The period examined (2004-2013) encompasses the Caribbean-wide 2005 mass coral bleaching, the 2009-10 catastrophic cold-water bleaching, and a warm-water bleaching event in 2011. Extension and calcification rates were higher inshore every year from 2004-2013 except when there were thermal stress events that solely impacted inshore reefs (2009-10, 2011-12). Inshore growth rates recovered quickly from cold and warm-water stress. These higher calcification rates and their quick recovery after thermal stress are likely important factors in the persistence of high coral cover inshore.

  15. Towle, E.K., I.C. Enochs, and C. Landon. Threatened Caribbean coral is able to mitigate the adverse effects of ocean acidification on calcification by increasing feeding rate. PLoS ONE, 10(4):e0123394, doi:10.1371/journal.pone.0123394 2015

    Abstract:

    Global climate change threatens coral growth and reef ecosystem health via ocean warming and ocean acidification (OA). Whereas the negative impacts of these stressors are increasingly well-documented, studies identifying pathways to resilience are still poorly understood. Heterotrophy has been shown to help corals experiencing decreases in growth due to either thermal or OA stress; however, the mechanism by which it mitigates these decreases remains unclear. This study tested the ability of coral heterotrophy to mitigate reductions in growth due to climate change stress in the critically endangered Caribbean coral Acropora cervicornis via changes in feeding rate and lipid content. Corals were either fed or unfed and exposed to elevated temperature (30°C), enriched pCO2 (800 ppm), or both (30°C/800 ppm) as compared to a control (26°C/390 ppm) for 8 weeks. Feeding rate and lipid content both increased in corals experiencing OA vs. present-day conditions, and were significantly correlated. Fed corals were able to maintain ambient growth rates at both elevated temperature and elevated CO2, while unfed corals experienced significant decreases in growth with respect to fed conspecifics. Our results show for the first time that a threatened coral species can buffer OA-reduced calcification by increasing feeding rates and lipid content.

  16. Enochs, I.C., D.P. Manzello, R. Carlton, S. Schopmeyer, R. van Hooidonk, and D. Lirman. Effects of light and elevated pCO2 on the growth and photochemical efficiency of Acropora cervicornis. Coral Reefs, 33(2):477-485, doi:10.1007/s00338-014-1132-7 2014

    Abstract:

    The effects of light and elevated pCO2 on the growth and photochemical efficiency of the critically endangered staghorn coral, Acropora cervicornis, were examined experimentally. Corals were subjected to high and low treatments of CO2 and light in a fully crossed design and monitored using 3D scanning and buoyant weight methodologies. Calcification rates, linear extension, as well as colony surface area and volume of A. cervicornis were highly dependent on light intensity. At pCO2 levels projected to occur by the end of the century from ocean acidification (OA), A. cervicornis exhibited depressed calcification, but no change in linear extension. Photochemical efficiency (F v/F m) was higher at low light, but unaffected by CO2. Amelioration of OA-depressed calcification under high-light treatments was not observed, and we suggest that the high-light intensity necessary to reach saturation of photosynthesis and calcification in A. cervicornis may limit the effectiveness of this potentially protective mechanism in this species. High CO2 causes depressed skeletal density, but not linear extension, illustrating that the measurement of extension by itself is inadequate to detect CO2 impacts. The skeletal integrity of A. cervicornis will be impaired by OA, which may further reduce the resilience of the already diminished populations of this endangered species.

  17. Glynn, P.W., I.C. Enochs, J.A. Afflerbach, V.W. Brandtneris, and J.E. Serafy. Eastern Pacific reef fish responses to coral recovery following El Niño disturbances. Marine Ecology Progress Series, 495:233-247, doi:10.3354/meps10594 2014

    Abstract:

    This study examines fluctuations in an eastern Pacific reef fish assemblage as it varies with coral recovery over 30 years. Concurrent fish and coral monitoring were conducted at Uva Island reef, which lies within the boundaries of Coiba National Park, Panama in an area that has received virtually no fishing pressure or watershed development over the past 80 years. Coral and fish monitoring spanned the 1982-83 and 1997-98 El Niño (ENSO) disturbances, anomalous warming events that selectively killed reef-building corals. While no fish mortalities were observed during the 1982-83 El Niño event, live coral cover was reduced to nearly 0% at the study reef. From 1984 to 1990, live coral (Pocillopora spp.) cover was extremely low (< 5%), but demonstrated steady recovery to ~35% by 2010. By quantifying disturbance-related, long-term changes in coral reef resources and relating these to fish trophic group responses, several functional relationships emerged. A total of 63 fish taxa were observed and reef fish density (all taxa combined) remained relatively stable. Multivariate analysis of species abundances revealed strong overlap between seasons and a clustering of community composition in the years following bleaching. Fish species richness increased significantly as live coral cover rose from near 0% to 15-20% then demonstrated a decreasing trend to 35% cover. Benthic invertivores showed a significant parabolic increase in density peaking at about 20% live coral cover. A pattern of decline was apparent for the mixed diet feeders guild as coral cover increased, whereas an asymptotic relationship with coral cover emerged for the facultative corallivore guild. No clear patterns in herbivore, piscivore and planktivore abundance were apparent with increasing coral cover. The varying responses of invertivore, corallivore and mixed diet feeding guilds demonstrated strong associations with coral cover, probably reflecting changes in availability of their respective trophic resources during reef recovery. Thus, variations in coral cover likely influence fish communities through trophic pathways involving invertebrate food sources.

  18. Manzello, D.P., I.C. Enochs, A. Bruckner, P.G. Renaud, G. Kolodziej, D.A. Budd, R. Carlton, and P.W. Glynn. Galapagos coral reef persistence after ENSO warming across an acidification gradient. Geophysical Research Letters, 41(24):9001-9008, doi:10.1002/2014GL062501 2014

    Abstract:

    Anthropogenic CO2 is causing warming and ocean acidification. Coral reefs are being severely impacted, yet confusion lingers regarding how reefs will respond to these stressors over this century. Since the 1982–1983 El Niño–Southern Oscillation warming event, the persistence of reefs around the Galápagos Islands has differed across an acidification gradient. Reefs disappeared where pH  < 8.0 and aragonite saturation state (Ωarag)  ≤ 3 and have not recovered, whereas one reef has persisted where pH  > 8.0 and Ωarag  > 3. Where upwelling is greatest, calcification by massive Porites is higher than predicted by a published relationship with temperature despite high CO2, possibly due to elevated nutrients. However, skeletal P/Ca, a proxy for phosphate exposure, negatively correlates with density (R = −0.822, p < 0.0001). We propose that elevated nutrients have the potential to exacerbate acidification by depressing coral skeletal densities and further increasing bioerosion already accelerated by low pH.

  19. Bignami, S., I.C. Enochs, D.P. Manzello, S. Sponaugle, and R.K. Cowen. Ocean acidification alters the otoliths of a pan-tropical fish species with implications for sensory function. Proceedings of the National Academy of Sciences USA, 110(18):7366-7370, doi:10.1073/pnas.1301365110 2013

    Abstract:

    Ocean acidification affects a wide diversity of marine organisms and is of particular concern for vulnerable larval stages critical to population replenishment and connectivity. Whereas it is well known that ocean acidification will negatively affect a range of calcareous taxa, the study of fishes is more limited in both depth of understanding and diversity of study species. We used new 3D microcomputed tomography to conduct in situ analysis of the impact of ocean acidification on otolith (ear stone) size and density of larval cobia (Rachycentron canadum), a large, economically important, pantropical fish species that shares many life history traits with a diversity of high-value, tropical pelagic fishes. We show that 2,100 μatm partial pressure of carbon dioxide (pCO2) significantly increased not only otolith size (up to 49% greater volume and 58% greater relative mass) but also otolith density (6% higher). Estimated relative mass in 800 μatm pCO2 treatments was 14% greater, and there was a similar but nonsignificant trend for otolith size. Using a modeling approach, we demonstrate that these changes could affect auditory sensitivity including a ∼50% increase in hearing range at 2,100 μatm pCO2, which may alter the perception of auditory information by larval cobia in a high-CO2 ocean. Our results indicate that ocean acidification has a graded effect on cobia otoliths, with the potential to substantially influence the dispersal, survival, and recruitment of a pelagic fish species. These results have important implications for population maintenance/replenishment, connectivity, and conservation efforts for other valuable fish stocks that are already being deleteriously impacted by overfishing.

  20. Manzello, D.P., I.C. Enochs, S. Musielewicz, R. Carlton, and D. Gledhill. Tropical cyclones cause CaCO3 undersaturation of coral reef seawater in a high-CO2 world. Journal of Geophysical Research, 118(C10):5312-5321, doi:10.1002/jgrc.20378 2013

    Abstract:

    Ocean acidification is the global decline in seawater pH and calcium carbonate (CaCO3) saturation state (Ω) due to the uptake of anthropogenic CO2 by the world's oceans. Acidification impairs CaCO3 shell and skeleton construction by marine organisms. Coral reefs are particularly vulnerable, as they are constructed by the CaCO3 skeletons of corals and other calcifiers. We understand relatively little about how coral reefs will respond to ocean acidification in combination with other disturbances, such as tropical cyclones. Seawater carbonate chemistry data collected from two reefs in the Florida Keys before, during, and after Tropical Storm Isaac provide the most thorough data to-date on how tropical cyclones affect the seawater CO2-system of coral reefs. Tropical Storm Isaac caused both an immediate and prolonged decline in seawater pH. Aragonite saturation state was depressed by 1.0 for a full week after the storm impact. Based on current 'business-as-usual' CO2 emissions scenarios, we show that tropical cyclones with high rainfall and runoff can cause periods of undersaturation (Ω < 1.0) for high-Mg calcite and aragonite mineral phases at acidification levels before the end of this century. Week-long periods of undersaturation occur for 18 mol% high-Mg calcite after storms by the end of the century. In a high-CO2 world, CaCO3 undersaturation of coral reef seawater will occur as a result of even modest tropical cyclones. The expected increase in the strength, frequency, and rainfall of the most severe tropical cyclones with climate change in combination with ocean acidification will negatively impact the structural persistence of coral reefs over this century.

  21. Enochs, I.C. Motile cryptofauna associated with live and dead coral substrates: Implications for coral mortality and framework erosion. Marine Biology, 159(4):709-722, doi:10.1007/s00227-011-1848-7 2012

    Abstract: Coral reef cryptofauna are a diverse group of metazoan taxa that live within intra- and inter-skeletal voids formed by framework structures. Despite a hypothesized high biomass and numerous trophic roles, they remain uncharacterized relative to exposed reef communities. Motile cryptofauna were sampled from live coral colonies and dead frameworks typifying four successive levels of degradation on an eastern Pacific pocilloporid reef. Abundances and biomass were higher on live versus dead corals habitats. The density of cryptofauna per volume substrate was highest on dead coral frameworks of intermediate degradation, where complex eroded substrates provide abundant shelters. These data have important and far-reaching ramifications for how the diverse multispecies assemblages that are reef ecosystems will respond to anthropogenic stressors such as those associated with climate change. Extreme levels of coral mortality, bioerosion, and habitat destruction will lead to impairment and eventually loss of ecosystem functions.

  22. Enochs, I.C., and D.P. Manzello. Responses of cryptofaunal species richness and trophic potential to coral reef habitat degradation. Diversity, 4(1):94-104, doi:10.3390/d4010094 2012

    Abstract:

    Coral reefs are declining worldwide as a result of many anthropogenic disturbances. This trend is alarming because coral reefs are hotspots of marine biodiversity and considered the 'rainforests of the sea. As in the rainforest, much of the diversity on a coral reef is cryptic, remaining hidden among the cracks and crevices of structural taxa. Although the cryptofauna make up the majority of a reef's metazoan biodiversity, we know little about their basic ecology or how these communities respond to reef degradation. Emerging research shows that the species richness of the motile cryptofauna is higher among dead (framework) vs. live coral substrates and, surprisingly, increases within successively more eroded reef framework structures, ultimately reaching a maximum in dead coral rubble. Consequently, the paradigm that abundant live coral is the apex of reef diversity needs to be clarified. This provides guarded optimism amidst alarming reports of declines in live coral cover and the impending doom of coral reefs, as motile cryptic biodiversity should persist independent of live coral cover. Granted, the maintenance of this high species richness is contingent on the presence of reef rubble, which will eventually be lost due to physical, chemical, and biological erosion if not replenished by live coral calcification and mortality. The trophic potential of a reef, as inferred from the abundance of cryptic organisms, is highest on live coral. Among dead framework substrates, however, the density of cryptofauna reaches a peak at intermediate levels of degradation. In summary, the response of the motile cryptofauna, and thus a large fraction of the reef's biodiversity, to reef degradation is more complex and nuanced than currently thought; such that species richness may be less sensitive than overall trophic function.

  23. Enochs, I.C., and D.P. Manzello. Species richness of motile cryptofauna across a gradient of reef framework erosion. Coral Reefs, 31(3):653-661, doi:10.1007/s00338-012-0886-z 2012

    Abstract: Coral reef ecosystems contain exceptionally high concentrations of marine biodiversity, potentially encompassing millions of species. Similar to tropical rainforests and their insects, the majority of reef animal species are small and cryptic, living in the cracks and crevices of structural taxa (trees and corals). Although the cryptofauna make up the majority of a reef's metazoan biodiversity, we know little about their basic ecology. We sampled motile cryptofaunal communities from both live corals and dead carbonate reef framework across a gradient of increasing erosion on a reef in Pacific Panama. A total of 289 Operational Taxonomic Units (OTUs) from six phyla were identified. We used species-accumulation models fitted to individual- and sample-based rarefaction curves, as well as seven nonparametric richness estimators to estimate species richness among the different framework types. All procedures predicted the same trends in species richness across the differing framework types. Estimated species richness was higher in dead framework (261-370 OTUs) than in live coral substrates (112-219 OTUs). Surprisingly, richness increased as framework structure was eroded: coral rubble contained the greatest number of species (227-320 OTUs) and the lowest estimated richness of 47-115 OTUs was found in the zone where the reef framework had the greatest vertical relief. This contradicts the paradigm that abundant live coral indicates the apex of reef diversity.

  24. Manzello, D.P., I.C. Enochs, N. Melo, D.K. Gledhill, and E.M. Johns. Ocean acidification refugia of the Florida Reef track. PLoS ONE, 7(7):e41715, 10 pp., doi:10.1371/journal.pone.0041 2012

    Abstract: Ocean acidification (OA) is expected to reduce the calcification rates of marine organisms, yet we have little understanding of how OA will manifest within dynamic, real-world systems. Natural CO2, alkalinity, and salinity gradients can significantly alter local carbonate chemistry, and thereby create a range of susceptibility for different ecosystems to OA. As such, there is a need to characterize this natural variability of seawater carbonate chemistry, especially within coastal ecosystems. Since 2009, carbonate chemistry data have been collected on the Florida Reef Tract (FRT). During periods of heightened productivity, there is a net uptake of total CO2 (T CO2) which increases aragonite saturation state (Varag) values on inshore patch reefs of the upper FRT. These waters can exhibit greater Varag than what has been modeled for the tropical surface ocean during preindustrial times, with mean (6 std. error) Varag-values in spring = 4.69 (60.101). Conversely, Varag-values on offshore reefs generally represent oceanic carbonate chemistries consistent with present day tropical surface ocean conditions. This gradient is opposite from what has been reported for other reef environments. We hypothesize this pattern is caused by the photosynthetic uptake of TCO2 mainly by seagrasses and, to a lesser extent, macroalgae in the inshore waters of the FRT. These inshore reef habitats are therefore potential acidification refugia that are defined not only in a spatial sense, but also in time; coinciding with seasonal productivity dynamics. Coral reefs located within or immediately downstream of seagrass beds may find refuge from OA.

  25. Toth, L.T., R.B. Aronson, S.V. Vollmer, J.W. Hobbs, D.H. Urrego, H. Cheng, I.C. Enochs, D.J. Combosch, R. van Woesik, and I.G. Macintyre. ENSO drove 2500-year collapse of eastern Pacific coral reefs. Science, 337(6090):81-84, doi:10.1126/science.1221168 2012

    Abstract: Cores of coral reef frameworks along an upwelling gradient in Panama show that reef ecosystems in the tropical eastern Pacific collapsed for 2500 years, representing as much as 40% of their history, beginning about 4000 years ago. The principal cause of this millennial-scale hiatus in reef growth was increased variability of the El Niño-Southern Oscillation (ENSO) and its coupling with the Intertropical Convergence Zone. The hiatus was a Pacific-wide phenomenon with an underlying climatology similar to probable scenarios for the next century. Global climate change is probably driving eastern Pacific reefs toward another regional collapse.

  26. Enochs, I.C., L.T. Toth, V.W. Brandtneris, J.C. Afflerbach, and D.P. Manzello. Environmental determinants of motile cryptofauna on an eastern Pacific reef. Marine Ecology Progress Series, 438:105-118, doi:10.3354/meps09259 2011

    Abstract: Coral reef cryptofauna, which live hidden within reef framework structures, are considered to be the most diverse group of coral reef metazoans. They likely comprise more biomass than all surface fauna, providing important food sources for fishes and playing important roles as predators, herbivores, detritivores, filter feeders, and scavengers. In an era of global change, it is important to determine how these communities are structured across reef habitats as well as to understand how reef framework degradation will impact the cryptofauna and, by extension, ecosystem function. Artificial reef framework (ARF) units were constructed from coral rubble to approximate framework substrates. Forty replicates were subjected to treatments of differing porosity, flow, and coral cover in a fully-crossed ANOVA design. After two months in situ, all motile cryptofauna (>2 mm) were counted, weighed, and identified to the lowest possible level. A total of 11,309 specimens were collected, comprising more than 121 species from six separate phyla. Cryptofaunal abundances and biomass were higher in low porosity crypts and biomass was greater in slow flow environments, highlighting the importance of sheltered low porosity habitats, such as backreef rubble plains. The presence of live coral was not found to have a significant effect on the motile cryptofauna occupying the dead coral framework below it, suggesting a high degree of resilience in how framework-dwelling fauna respond to coral mortality. These data support the assertion that artificial reefs are capable of facilitating the accumulation of a diverse cryptic community, independent of live coral, provided they contain suitably porous crypts.

  27. Glynn, P.W., S.B. Colley, H.M. Guzman, I.C. Enochs, J. Cortes, J.L. Mate, and J.S. Feingold. Reef coral reproduction in the eastern Pacific: Costa Rica, Panama, and the Galapagos Islands (Ecuador). VI. Agariciidae, Pavona clavus. Marine Biology, 158(7):1601-1617, doi:10.1007/s00227-011-1673-z 2011

    Abstract:

    The reproductive ecology of the zooxanthellate reef coral Pavona clavus was investigated at several sites in Costa Rica, Panama, and the Galapagos Islands (Ecuador) over the period 1985-2009. Pavona clavus displayed stable gonochorism as only five hermaphrodites were found in 590 samples. At four of five locations, sex ratios were skewed toward female dominance; however, at Saboga Island (Panama) male colonies predominated. In Panama, sexual maturity was observed in an estimated eight-year-old female colony, and several colonies of 10-20 years of age demonstrated gametogenesis. Sexual activity was observed at all study sites, but gamete development occurred in only 14-31% of colonies sampled sporadically. Seasonality of gametogenic activity occurred predominantly during the warm/wet season, June to August, at mainland sites (Ca'o Island, Costa Rica, and Gulfs of Chiriqui and Panama, Panama). This pattern was repeated in the Galapagos Islands, but mainly from March to May when seasonally high sea temperatures and rainfall prevailed there. Histological sampling and field observations indicated that spawning was centered around the full moon, most frequently on lunar day 17, and near sunset (1,800 h). Mean fecundity (mature ova cm-2 live tissue) estimates were significantly different for two sites and ranged from ~1,780 (Saboga Island, Gulf of Panama, seasonally upwelling) to ~4,280 (Uva Island, Gulf of Chiriqui, non-upwelling). Assuming three annual spawning events colony-1 (August, September, October), extrapolation of minimum and maximum fecundities yield 5,340 and 12,840 ova cm-2 year-1. Seasonal, lunar, and diel spawning patterns in nine zooxanthellate species at Uva Island indicate asynchronous coral community spawning.

  28. Glynn, P.W., and I.C. Enochs. Invertebrates and their roles in coral reef ecosystems. In Coral Reefs: An Ecosystem in Transition, Z. Dubinsky and N. Stambler (eds.) Springer, 273-326, 2010

    Abstract: No abstract.