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Dr Ross Hill

Biography

Dr Ross Hill is an Associate of the Faculty of Science and an Honorary Member of the Plant Functional Biology & Climate Change Cluster.

Ross currently holds a highly competitive Vice-Chancellor's Postdoctoral Research Fellowship at The University of New South Wales.

Ross’s research primarily concentrates on the impacts of climate change to a range of photosynthetic marine organisms which produce calcium carbonate skeletons. Of primary concern is how these vulnerable species will respond to warmer and more acidic conditions and how climate change will affect their interaction with natural enemies, such as herbivory and disease. Experiments being conducted at the Sydney Institute of Marine Science (SIMS) are simulating a range of future climate change scenarios to determine the likely impacts for these important species.

Another focus of Ross’s research is exploring the photosynthetic mechanisms that lead to coral bleaching. Thermal stress is known to cause the expulsion of algal symbionts from corals, but the photosynthetic trigger of bleaching, the capacity for photoprotection and protein repair mechanisms remain unresolved. Ross's research also extends to Antarctica where he investigates the impacts of climate change on pack ice algae.

These algae live in an extreme environment yet form the base of the Antarctic food chain. This research is of high importance as it is critical that we understand what impacts climate change will have on such a unique and valuable ecosystem.

In 2003, Ross completed his undergraduate degree in Environmental Biology with First Class Honours and the University Medal. He subsequently completed his PhD at the University of Technology, Sydney on the photosynthetic impacts to symbiotic dinoflagellates in corals during bleaching events, and graduated in 2008. Ross then completed a five month, ARC-funded, Research Fellowship, involving a 6 week voyage to Antarctica.

From 2008-2012, Ross was a Lecturer and Chancellor’s Postdoctoral Research Fellow at the University of Technology, Sydney.

Professional

Professional Associations:

  • Councillor and webmanager for the Australian Coral Reef Society.
  • Member of the Sydney Institute of Marine Science
  • Invited speaker at the Coral Reef Targeted Research and Capacity Building for Management Workshop, Puerto Morelos, Mexico (2005)

Professional Memberships:
  • American Society of Limnology and Oceanography (ASLO)
  • Australasian Society for Phycology and Aquatic Botany (ASPAB)
  • Australian Coral Reef Society (ACRS)
  • Australian Marine Science Association (AMSA)
  • International Society for Reef Studies (ISRS)
  • International Symbiosis Society (ISS)

Collaborations:
  • Professor David Kramer, Michigan State University. Photosynthetic antenna systems of Symbiodinium.
  • Associate Professor Douglas Campbell, Mt Allison University (Canada). Microalgal photosynthetic protein analyses, specifically D1 and Rubisco.
  • Emeritus Professor Anthony Larkum, The University of Sydney and University of Technology, Sydney. Photosynthesis, photoprotection and calcification in marine phototrophs.
  • Professor Michael Kühl, University of Copenhagen. Optical properties of corals and other tropical benthic marine calcifiers.
  • Dr Shunichi Takahashi, Australian National University. Mechanisms of photoinactivation and repair in Symbiodinium and the influence of thermal stress in promoting photoinhibition.
  • Professor Alfred Holzwarth and Dr Chavdar Slavov, Max-Planck-Institut für Bioanorganische Chemie. Characterising the potential of excess energy dissipation in the antennae of Symbiodinium.
  • Dr Björn Rost, Alfred Wegener Institute for Polar and Marine Research. Evaluating the vulnerability of temperate photosynthetic marine calcifiers to climate change.
  • Professor Ond?ej Prášil, Laboratory of Photosynthesis, Institute of Microbiology, Czech Academy of Sciences. Interpreting low-temperature fluorescence spectrum of dinoflagellate algae to reveal shifts in light harvesting antenna complexes.
  • Dr Christine Ferrier-Pagès, Centre Scientifique de Monaco. Research on coral calcification, growth and feeding.
  • Associate Professor Simon Davy, Dr Ken Ryan and Dr Laura Wicks, Victoria University of Wellington (New Zealand). Coral and anemone photobiology in high-latitude reefs.
  • Dr Imre Vass, Biological Research Centre, Hungarian Academy of Sciences. Sensitivity of photosynthetic processes in coral symbionts under thermal stress.
  • Dr Peter Scanes, Head of the Coastal Waters Unit at the NSW Department of Environment, Climate Change and Water. Building an understanding of seagrass resilience into estuarine management.
  • Associate Professor Dee Carter, The University of Sydney. Molecular ecology and photobiology of Symbiodinium and Chromera.
  • Dr Jane Williamson, Macquarie University. Impacts of ocean acidification to marine bivalves.
  • Dr Selina Ward, The University of Queensland. Climate change impacts on coral reproduction.
  • Dr Anna Scott, Southern Cross University. Climate change impacts on sea anemone reproduction, bleaching thresholds of adult anemones and recovery strategies.
  • Adrian Lutz, James Cook University and the Australian Institute of Marine Science. The biochemistry of electron carriers in the photosynthetic machinery of coral symbionts.
  • Professor Peter Steinberg and Dr Tilmann Harder, University of New South Wales. Calcification and herbivore avoidance in temperate photosynthetic marine calcifiers.

Ross Hill - Marine Climate Change video

Image of Ross Hill
Associate of the Faculty, Plant Functional Biology & Climate Change
B. Sc in Env. Sci (1st Class Hons & Univ. Medal), B.Env.Biol. (UTS), Doctor of Philosophy
 

Research Interests

  • Coral bleaching
  • Ocean acidification
  • Antarctic algae
  • Desalination
  • Climate change

Seagrass Inc
Ross Hill - Marine Climate Change video

Since 2004, Ross has taught the following subjects:

  • Biocomplexity
  • The Biosphere
  • Plant Physiology and Ecophysiology
  • Marine Primary Producers
  • Mapping and Remote Sensing
  • Environmental Management
  • Animal Function and Diversity
  • Cells, Genetics and Evolution

Books

Hill, R. 2008, Coral Bleaching: photosynthetic impacts on symbiotic dinoflagellates. Coral Reefs and Climate Change, VDM Publishing House Ltd, Germany.

Conference Papers

Sinutok, S., Hill, R., Doblin, M.A. & Ralph, P.J. 2010, 'Rising ocean temperature and ocean acidification will reduce productivity and calcification in Halimeda sp. and benthic foraminifera from the Great Barrier Reef', Wageningen, The Netherlands, December 2010 in Euro ISRS Symposium 2010, ed J. Kaandorp, E. Meesters, R. Osinga, J. Verreth, T. Wijgerde, Grafisch Service Center, Wageningen, The Netherlands, pp. 191-191.
Schrameyer, V., Kraemer, W., Hill, R., Doblin, M.A., Kai, B. & Ralph, P.J. 2010, 'Nutritional status of hard and soft corals influences photosynthesis capacity of Symbiodinium sp. and vitality of the holobiont', Wageningen, The Netherlands, December 2010 in Euro ISRS Symposium 2010, ed J. Kaandorp, E. Meesters, R. Osinga, J. Verreth, T. Wijgerde, Grafisch Service Center, Wageningen, The Netherlands, pp. 108-108.
Hill, R., Brown, C., DeZeeuw, K., Campbell, D. & Ralph, P.J. 2010, 'Increased rate of D1 repair in coral symbionts during bleaching is insufficient to counter accelerated photoinactivation', Wageningen, The Netherlands, December 2010 in Euro ISRS Symposium 2010, ed J. Kaandorp, E. Meesters, R. Osinga, J. Verreth, T. Wijgerde, Grafisch Service Center, Wageningen, The Netherlands, pp. 87-87.
Sinutok, S., Hill, R. & Ralph, P.J. 2009, 'The effect of light intensity on photosynthetic efficiency and calcification in three reef building species of Halimeda', ASPAB 2009 Conference, Townsville, Australia, November 2009.
Calcareous green algae from the genus Halimeda are widely distributed in tropical and subtropical marine environments. Halimeda is important as a carbonate sediment producer, as a source of food for herbivores, as a phototroph, and as a provider of shelter and nursery ground for invertebrates on coral reefs. Halimeda cylindracea, H. macroloba, and H. opuntia collected from the intertidal zone at Heron Island reef in the southern Great Barrier Reef of Australia were maintained in flow-through seawater tanks under three different irradiances (50, 400 and 900 -mol photon m-2 s-1) for a 4 day period. Measures of photosynthetic efficiency were investigated using Pulse Amplitude Modulated (PAM) fluorometry and chlorophyll concentrations (a and b) were determined after 4 days on an apical lobe of the thallus. Growth and calcification were examined by staining the thallus with Alizarin Red-S solution. Pigmentation, growth, and calcification were found to be independent of irradiance, remaining constant over time between treatments, except for chlorophyll a in H. cylindracea which was higher in low light than in higher light treatments. The results indicate that each species responded differently under the high light treatment at midday, with H. cylindracea and H. macroloba showing a reduction in photochemical quenching (Y(II)), indicating downregulation in photosynthetic efficiency. This was mirrored by an increase in non-regulated energy dissipation yield of PSII (Y(NO)), suggesting that photoinhibition was occurring. In comparison to this species, H. opuntia showed no changes in Y(II) and Y(NO) while H. macroloba showed higher Y(II) and lower Y(NO) only in the morning and the evening. Non-photochemical quenching yield (Y(NPQ)) was low in all treatments and in all three species which may indicate a low potential for photoprotection mechanisms in these algae. However, further investigation is required which run over an extended period of time and between seasons.

Journal Articles

Jeans, J., Szabo, M., Campbell, D.A., Larkum, A., Ralph, P.J. & Hill, R. 2014, 'Thermal bleaching induced changes in photosystem II function not reflected by changes in photosystem II protein content of Stylophora pistillata', Coral Reefs, vol. 33, no. 1, pp. 131-139.
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Scleractinian corals exist in a symbiosis with marine dinoflagellates of the genus Symbiodinium that is easily disrupted by changes in the external environment. Increasing seawater temperatures cause loss of pigments and expulsion of the symbionts from the host in a process known as coral bleaching; though, the exact mechanism and trigger of this process has yet to be elucidated. We exposed nubbins of the coral Stylophora pistillata to bleaching temperatures over a period of 14 daylight hours. Fifty-nine percent of the symbiont population was expelled over the course of this short-term treatment. Maximum quantum yield (F V/F M) of photosystem (PS) II for the in hospite symbiont population did not change significantly over the treatment period, but there was a significant decline in the quantity of PSII core proteins (PsbA and PsbD) at the onset of the experimental increase in temperature. F V/F M from populations of expelled symbionts dropped sharply over the first 6 h of temperature treatment, and then toward the end of the experiment, it increased to an F V/F M value similar to that of the in hospite population. This suggests that the symbionts were likely damaged prior to expulsion from the host, and the most damaged symbionts were expelled earlier in the bleaching. The quantity of PSII core proteins, PsbA and PsbD, per cell was significantly higher in the expelled symbionts than in the remaining in hospite population over 6+10 h of temperature treatment. We attribute this to a buildup of inactive PSII reaction centers, likely caused by a breakdown in the PSII repair cycle. Thus, thermal bleaching of the coral S. pistillata induces changes in PSII content that do not follow the pattern that would be expected based on the results of PSII function
Jeans, J., Szabo, M., Campbell, D.A., Larkum, A., Ralph, P.J. & Hill, R. 2014, 'Thermal bleaching induced changes in photosystem II function not reflected by changes in photosystem II protein content of Stylophora pistillata', Coral Reefs, vol. 33, pp. 131-139.
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Sinutok, S., Hill, R., Kuhl, M., Doblin, M.A. & Ralph, P.J. 2014, 'Ocean acidification and warming alter photosynthesis and calcification of the symbiont-bearing foraminifera Marginopora vertebralis', Marine Biology, vol. 161, pp. 2143-2154.
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Sinutok, S., Hill, R., Doblin, M.A. & Ralph, P.J. 2013, 'Diurnal photosynthetic response of the motile symbiotic benthic foraminiferan Marginopora vertebralis', Marine Ecology Progress Series, vol. 478, pp. 127-138.
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Movement of the symbiont-bearing foraminiferan Marginopora vertebralis and photo physiological response to diurnal fluctuations in irradiance were investigated in field and laboratory experiments. The abundance of M. vertebralis from both light-exposed and sheltered habitats was determined 5 times during the day, from pre-dawn to post-dusk. M. vertebralis abundance was significantly higher in sheltered compared to exposed habitats at midday under high irradiance, and this movement enabled the algal symbionts to avoid excessive photoinhibition. The diurnal changes in photosynthetic efficiency were not consistent with the typical midday solar maximum downregulation of photosystem II observed in other photoautotrophs and was likely due to the negatively phototactic capacity of the foraminifera. To confirm the light-dependent movement of foraminifera, individuals in exposed and sheltered habitats were exposed to the photosynthetic inhibitor 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) in the laboratory. The lack of movement in DCMU-exposed specimens confirmed light-dependent movement and subsequent disruption of signalling between the host foraminiferan and the algal symbionts. Analysis of chlorophyll and xanthophyll pigments, as well as symbiont density, indicated that under high irradiance, foraminiferal symbionts have the capacity to reduce light stress by activating photo-protective mechanisms. The negatively phototactic behaviour prevented chlorophyll degradation, symbiont loss and bleaching, suggesting that it is the primary mechanism for controlling light exposure in these foraminifera. This behaviour provides a competitive advantage over other sessile organisms in avoiding photoinhibition and bleaching by moving away from over-saturating irradiance, towards less damaging light fields.
Kramer, W., Schrameyer, V., Hill, R., Ralph, P.J. & Bischof, K. 2013, 'PSII Activity And Pigment Dynamics Of Symbiodinium In Two Indo-pacific Corals Exposed To Short-term High-light Stress', Marine Biology, vol. 160, no. 3, pp. 563-577.
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This study examined the capacity for photoprotection and repair of photo-inactivated photosystem II in the same Symbiodinium clade associated with two coexisting coral species during high-light stress in order to test for the modulation of the symbiont+s photobiological response by the coral host. After 4 days exposure to in situ irradiance, symbionts of the bleaching-sensitive Pocillopora damicornis showed rapid synthesis of photoprotective pigments (by 44 %) and strongly enhanced rates of xanthophyll cycling (by 446 %) while being insufficient to prevent photoinhibition (sustained loss in F v/F m at night) and loss of symbionts after 4 days. By contrast, Pavona decussata showed no significant changes in F v/F m, symbiont density or xanthophyll cycling. Given the association with the same Symbiodinium clade in both coral species, our findings suggest that symbionts in the two species examined may experience different in hospite light conditions as a result of different biometric properties of the coral host.
York, P.H., Gruber, R.K., Hill, R., Ralph, P.J., Booth, D.J. & Macreadie, P.I. 2013, 'Physiological and Morphological Responses of the Temperate Seagrass Zostera muelleri to Multiple Stressors: Investigating the Interactive Effects of Light and Temperature', PLoS One, vol. 8, no. 10, pp. e76377-e76377.
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Understanding how multiple environmental stressors interact to affect seagrass health (measured as morphological and physiological responses) is important for responding to global declines in seagrass populations. We investigated the interactive effects of temperature stress (24, 27, 30 and 32C) and shading stress (75, 50, 25 and 0% shade treatments) on the seagrass Zostera muelleri over a 3-month period in laboratory mesocosms. Z. muelleri is widely distributed throughout the temperate and tropical waters of south and east coasts of Australia, and is regarded as a regionally significant species. Optimal growth was observed at 27C, whereas rapid loss of living shoots and leaf mass occurred at 32C. We found no difference in the concentration of photosynthetic pigments among temperature treatments by the end of the experiment; however, up-regulation of photoprotective pigments was observed at 30C. Greater levels of shade resulting in high photochemical efficiencies, while elevated irradiance suppressed effective quantum yield (?F/FM+). Chlorophyll fluorescence fast induction curves (FIC) revealed that the J step amplitude was significantly higher in the 0% shade treatment after 8 weeks, indicating a closure of PSII reaction centres, which likely contributed to the decline in ?F/FM+ and photoinhibition under higher irradiance. Effective quantum yield of PSII (delta F/FM+) declined steadily in 32C treatments, indicating thermal damage
Sackett, O.E., Petrou, K., Reedy, B.J., De Grazia, A., Hill, R., Doblin, M.A., Beardall, J., Ralph, P.J. & Heraud, P. 2013, 'Phenotypic plasticity of Southern Ocean diatoms: Key to success in the sea ice habitat?', PLoS One, vol. 8, no. 11, pp. e81185-1-e81185-12.
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Diatoms are the primary source of nutrition and energy for the Southern Ocean ecosystem. Microalgae, including diatoms, synthesise biological macromolecules such as lipids, proteins and carbohydrates for growth, reproduction and acclimation to prevailing environmental conditions. Here we show that three key species of Southern Ocean diatom (Fragilariopsis cylindrus, Chaetoceros simplex and Pseudo-nitzschia subcurvata) exhibited phenotypic plasticity in response to salinity and temperature regimes experienced during the seasonal formation and decay of sea ice. The degree of phenotypic plasticity, in terms of changes in macromolecular composition, was highly species-specific and consistent with each species+ known distribution and abundance throughout sea ice, meltwater and pelagic habitats, suggesting that phenotypic plasticity may have been selected for by the extreme variability of the polar marine environment. We argue that changes in diatom macromolecular composition and shifts in species dominance in response to a changing climate have the potential to alter nutrient and energy fluxes throughout the Southern Ocean ecosystem.
Buxton, L.J., Takahashi, S., Hill, R. & Ralph, P.J. 2012, 'Variability in the primary site of photosynthetic damage in Symbiodinium sp. (Dinophyceae) exposed to thermal stress', Journal of Phycology, vol. 48, no. 1, pp. 117-126.
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Exposure to elevated temperature is known to cause photosynthetic inhibition in the coral symbiont Symbiodinium sp. Through the use of the artificial electron acceptor, methyl viologen, this study identified how reduced photosynthetic capacity occurs as a result of inhibition up- and/or downstream of ferredoxin in Symbiodinium sp. in hospite and in culture. Heterogeneity between coral species and symbiont clades was identified in the thermal sensitivity of photosynthesis in the symbionts of the scleractinian corals Stylophora pistillata and Pocillopora damicornis, as well as among Symbiodinium cultures of clades A, B, and C. The in hospite symbionts of S. pistillata and the cultured clade C Symbiodinium both exhibited similar patterns in that their primary site of thermal inhibition occurred downstream of ferredoxin at 32 degrees C. In contrast, the primary site of thermal inhibition occurred upstream of ferredoxin in clades A and B at 32 degrees C, while at 34 degrees C, all samples showed combined up- and downstream inhibition. Although clade C is common to both P. damicornis and S. pistillata, the manner of thermal inhibition was not consistent when observed in hospite. Results showed that there is heterogeneity in the primal site of thermal damage in Symbiodinium among coral species and symbiont clades.
Hill, R. & Scott, A. 2012, 'The influence of irradiance on the severity of thermal bleaching in sea anemones that host anemonefish', Coral Reefs, vol. 31, no. 1, pp. 273-284.
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Entacmaea quadricolor is a geographically widespread species of sea anemone that forms a three-way symbiosis with anemonefish and Symbiodinium. This species dominates the reef substrata at North Solitary Island, Australia, which is located in a region identified as a climate change hot spot. Their geographic location places these anemones under significant threat from rising ocean temperatures, although their upper thermal limit and risk of bleaching are unknown. To address this knowledge gap, anemones were exposed to one of four temperatures (23, 25, 27, or 29 degrees C) and one of two irradiance treatments (high or low light) over 6 days. At moderate temperatures (27 degrees C, 1 degrees C above summer average), anemone bleaching was characterised by symbiont expulsion, while extreme temperatures (29 degrees C) resulted in an additional loss of photosynthetic pigments from within symbionts, and in some cases, host mortality. Irradiance influenced the susceptibility to thermal stress with high light promoting the bleaching response, along with significant reductions in the effective quantum yield of anemone symbionts. The long-term loss of photosystem II photochemical efficiency within in hospite symbionts was observed during exposure to temperatures exceeding the summer average, indicating photosynthetic damage. The resident Symbiodinium, identified as clade C using 28S rRNA gene sequences, therefore represents the partner within the symbiosis that is likely to be most vulnerable to rising seawater temperatures. Results suggest that E. quadricolor is living within approximately 1 degrees C of the upper thermal maximum at the Solitary Islands, and given the predictions for rising seawater temperature on Australia's east coast, the thermal threshold at which bleaching will occur is expected to be reached and exceeded more frequently in the future.
Gilbert, J.A., Hill, R., Doblin, M.A. & Ralph, P.J. 2012, 'Microbial consortia increase thermal tolerance of corals', Marine Biology, vol. 159, pp. 1763-1771.
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This study examined the response of a coral holobiont to thermal stress when the bacterial community was treated with antibiotics. Colonies of Pocillopora damicornis were exposed to broad and narrow-spectrum antibiotics targeting coral-associated a and c-Proteobacteria. Corals were gradually heated from the control temperature of 26 to 31 C, and measurements were made of host, zooxanthellar and microbial condition. Antibiotics artificially reduced the abundance and activity of bacteria, but had minimal effect on zooxanthellae photosynthetic efficiency or host tissue protein content. Heated corals without antibiotics showed significant declines in FV/FM, typical of thermal stress. However, heated corals treated with antibiotics showed severe tissue loss in addition to a decline in FV/ FM. This study demonstrated that a disruption to the microbial consortium diminished the resilience of the holobiont. Corals exposed to antibiotics under control temperature did not bleach, suggesting that temperature may be an important factor influencing the activity, diversity and ecological function of the holobiont bacterial community.
Sinutok, S., Hill, R., Doblin, M.A., Kuhl, M. & Ralph, P.J. 2012, 'Microenvironmental changes support evidence of photosynthesis and calcification inhibition in Halimeda under ocean acidification and warming', Coral Reefs, vol. 31, pp. 1201-1213.
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The effects of elevated CO 2 and temperature on photosynthesis and calcification of two important calcifying reef algae (Halimedamacroloba and Halimeda cylindracea) were investigated with O 2 microsensors and chlorophyll a fluorometry through a combination of two pCO 2 (400 and 1,200 atm) and two temperature treatments (28 and 32 C) equivalent to the present and predicted conditions during the 2100 austral summer. Combined exposure to pCO 2 and elevated temperature impaired calcification and photosynthesis in the two Halimeda species due to changes in the microenvironment around the algal segments and a reduction in physiological performance. There were no significant changes in controls over the 5-week experiment, but there was a 50-70 % decrease in photochemical efficiency (maximum quantum yield), a 70-80 % decrease in O 2 production and a threefold reduction in calcification rate in the elevated CO 2 and high temperature treatment. Calcification in these species is closely coupled with photosynthesis, such that a decrease in photosynthetic efficiency leads to a decrease in calcification. Although pH seems to be the main factor affecting Halimeda species, heat stress also has an impact on their photosystem II photochemical efficiency. There was a strong combined effect of elevated CO 2 and temperature in both species, where exposure to elevated CO 2 or temperature alone decreased photosynthesis and calcification, but exposure to both elevated CO 2 and temperature caused a greater decline in photosynthesis and calcification than in each stress individually. Our study shows that ocean acidification and ocean warming are drivers of calcification and photosynthesis inhibition in Halimeda. Predicted climate change scenarios for 2100 would therefore severely affect the fitness of Halimeda, which can result in a strongly reduced production of carbonate sediments on coral reefs under such changed climate conditions.
Hill, R., Larkum, A., Prasil, O., Kramer, D.M., Szabo, M., Kumar, V. & Ralph, P.J. 2012, 'Light-induced dissociation of antenna complexes in the symbionts of scleractinian corals correlates with sensitivity to coral bleaching', Coral Reefs, vol. 31, pp. 963-975.
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Elevated temperatures in combination with moderate to high irradiance are known to cause bleaching events in scleractinian corals, characterised by damage to photosystem II (PSII). Photoprotective mechanisms of the symbiont can reduce the excitation pressure impinging upon PSII. In the bleaching sensitive species, Acropora millepora and Pocillopora damicornis, high light alone induced photoprotection through the xanthophyll cycle, increased content of the antioxidant carotenoid, -carotene, as well as the dissociation of the light-harvesting chlorophyll complexes. The evidence is compatible with either the membrane-bound chlorophyll a-chlorophyll c 2-peridinin-protein (acpPC) complex or the peripheral peridinin-chlorophyll-protein complex, or both, disconnecting from PSII under high light. The acpPC complex potentially showed a state transition response with redistribution towards photosystem I to reduce PSII over-excitation. This apparent acpPC dissociation/reassociation was promoted by the addition of the xanthophyll cycle inhibitor, dithiothreitol, under high irradiance. Exposure to thermal stress as well as high light promoted xanthophyll de-epoxidation and increased -carotene content, although it did not influence light-harvesting chlorophyll complex (LHC) dissociation, indicating light, rather than temperature, controls LHC dissociation. Photoinhibition was avoided in the bleaching tolerant species, Pavona decussata, suggesting xanthophyll cycling along with LHC dissociation may have been sufficient to prevent photodamage to PSII. Symbionts of P. decussata also displayed the greatest detachment of antenna complexes, while the more thermally sensitive species, Pocillopora damicornis and A. millepora, showed less LHC dissociation, suggesting antenna movement influences bleaching susceptibility.
Hill, R., Brown, C.M., DeZeeuw, K., Campbell, D.A. & Ralph, P.J. 2011, 'Increased rate of D1 repair in coral symbionts during bleaching is insufficient to counter accelerated photo-inactivation', Limnology and Oceanography, vol. 56, no. 1, pp. 139-146.
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We dissect the primary photo-inactivation and the counteracting metabolic repair rates in fragments of the scleractinian coral, Pocillopora damicornis, subjected to a combined stress of a shift to elevated temperature (from 26 degrees C to 32 degrees C) and increased light (from 200 mu mol photons m(-2) s(-1) to 400 mmol photons m(-2) s(-1)) to induce bleaching. During the bleaching treatment the dinoflagellate symbionts showed a 5.5-fold acceleration in their photosystem II (PSII) repair rate constant, demonstrating that they maintain strong metabolic capacity to clear and replace photo-damaged D1 protein at the elevated temperature and light conditions. Nevertheless, the symbionts concurrently suffered a seven-fold increase in the rate constant for PSII photo-inactivation. This rapid photo-inactivation exceeded the PSII repair capacity, therefore tipping the symbionts, and by implication the symbiosis, into net photo-inhibition. Increased photo-inactivation in hospite, rather than an inhibition of PSII repair, is the principle trigger for net photo-inhibition under bleaching conditions.
Petrou, K., Hill, R., Doblin, M.A., McMinn, A., Johnson, R., Wright, S.W. & Ralph, P.J. 2011, 'Photoprotection of sea-ice microalgal communities from the east Antarctic pack ice', Journal of Phycology, vol. 47, no. 1, pp. 77-86.
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All photosynthetic organisms endeavor to balance energy supply with demand. For sea-ice diatoms, as with all marine photoautotrophs, light is the most important factor for determining growth and carbonfixation rates. Light varies from extremely low to often relatively high irradiances within the sea-ice environment, meaning that sea-ice algae require moderate physiological plasticity that is necessary for rapid light acclimation and photoprotection. This study investigated photoprotective mechanisms employed by bottom Antarctic sea-ice algae in response to relatively high irradiances to understand how they acclimate to the environmental conditions presented during early spring, as the light climate begins to intensify and snow and sea-ice thinning commences.
Sinutok, S., Hill, R., Doblin, M.A., Wuhrer, R. & Ralph, P.J. 2011, 'Warmer more acidic conditions cause decreased productivity and calcification in subtropical coral reef sediment-dwelling calcifiers', Limnology and Oceanography, vol. 56, no. 4, pp. 1200-1212.
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The effects of elevated CO(2) and temperature on photosynthesis and calcification in the calcifying algae Halimeda macroloba and Halimeda cylindracea and the symbiont-bearing benthic foraminifera Marginopora vertebralis were investigated through exposure to a combination of four temperatures (28 degrees C, 30 degrees C, 32 degrees C, and 34 degrees C) and four CO(2) levels (39, 61, 101, and 203 Pa; pH 8.1, 7.9, 7.7, and 7.4, respectively). Elevated CO(2) caused a profound decline in photosynthetic efficiency (F(V) : F(M)), calcification, and growth in all species. After five weeks at 34 degrees C under all CO(2) levels, all species died. Chlorophyll (Chl) a and b concentration in Halimeda spp. significantly decreased in 203 Pa, 32 degrees C and 34 degrees C treatments, but Chl a and Chl c(2) concentration in M. vertebralis was not affected by temperature alone, with significant declines in the 61, 101, and 203 Pa treatments at 28 degrees C. Significant decreases in F(V) : F(M) in all species were found after 5 weeks of exposure to elevated CO(2) (203 Pa in all temperature treatments) and temperature (32 degrees C and 34 degrees C in all pH treatments). The rate of oxygen production declined at 61, 101, and 203 Pa in all temperature treatments for all species. The elevated CO(2) and temperature treatments greatly reduced calcification (growth and crystal size) in M. vertebralis and, to a lesser extent, in Halimeda spp. These findings indicate that 32 degrees C and 101 Pa CO(2), are the upper limits for survival of these species on Heron Island reef, and we conclude that these species will be highly vulnerable to the predicted future climate change scenarios of elevated temperature and ocean acidification.
Petrou, K., Hill, R., Brown, C.M., Campbell, D.A., Doblin, M.A. & Ralph, P.J. 2010, 'Rapid photoprotection in sea-ice diatoms from the East Antarctic pack ice', Limnology and Oceanography, vol. 55, no. 3, pp. 1400-1407.
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Photoinhibition and D1 protein re-synthesis were investigated in bottom-dwelling sea-ice microalgal communities from the East Antarctic pack ice during early spring. Bottom-dwelling sea-ice microalgal communities were dominated by diatoms that exhibited rapid photoprotection when exposed to a range of different light levels (10 mol photons m-2 s-1, 50 mol photons m-2 s-1, 100 mol photons m-2 s-1, and 200 mol photons m-2 s-1). Photosynthetic capacity of photosystem II (PSII) dropped significantly over 3 h under 200 mol photons m-2 s-1, but largely recovered when placed in a low-light environment (10 mol photons m-2 s-1) for an additional 3 h. PSII repair rates increased with increasing irradiance, and the D1-protein pool remained steady even under high light (200 mol photons m-2 s-1). Sea-ice diatoms showed a low intrinsic susceptibility to photoinactivation of PSII across all the light treatments, and a strong and irradiance-dependent induction of nonphotochemical quenching, which did not depend upon chloroplast protein synthesis, was also seen. These highly plastic organisms, once thought to be adapted to shade, are in fact well equipped to withstand rapid and relatively large changes in light at low temperatures with minimal long-term effect on their photosynthetic machinery.
Wicks, L.C., Hill, R. & Davy, S.K. 2010, 'The influence of irradiance on tolerance to high and low temperature stress exhibited by Symbiodinium in the coral, Pocillopora damicornis, from the high-latitude reef of Lord Howe Island', Limnology and Oceanography, vol. 55, no. 6, pp. 2476-2486.
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The coral Pocillopora damicornis hosts genetically distinct and novel types of dinoflagellate symbionts at the high-latitude site of Lord Howe Island (LHI), yet why these novel types exist at this marginal site is unknown. In this study, it was detennined whether one of the novel Symbiodinium types at LHI is phy~iologically adapted for this high-latitude site, where water temperatures annually range from 18C to 26e. Low and high short-tenn thennal bleaching thresholds of the coral-symbiont partnership were measured as 14C and 30e. PhotochEmical sensitivity to temperature (15C and 29C) and light treatments (100% and 40% of sunlight), measured as effective_ quantum yie1d and fast induction curves, were detennined over a 72-h period. A greater effect on the photochemical reactions of LHI P. damicornis symbionts was recorded in response to a 3e temperature increase from annual maxima than a 3e temperature decrease from annual minima. Corals did not bleach when temperature was reduced to 15e for 72 h; in contrast, a 92% decline in photochemical efficiency was recorded in the 29C treatment (AF: F~ < 0.05), compared to 35% loss in the control (20C). For the first time, a Pulse Efficiency Analyser fluorometer was used to assess the effect of reduced temperature on symbionts, showing a reduced rate of QA reduction, further enhanced by high light levels. This type of Symbiodinium at LHI may be specialized for cooler and more variable temperatures, so contributing to the success of corals at this marginal location.
Hill, R., Ulstrup, K. & Ralph, P.J. 2009, 'Temperature Induced Changes In Thylakoid Membrane Thermostability Of Cultured, Freshly Isolated, And Expelled Zooxanthellae From Scleractinian Corals', Bulletin of Marine Science, vol. 85, no. 3, pp. 223-244.
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Coral bleaching events are characterized by a dysfunction between the cnidarian coral host and the symbiotic dinoflagellate algae, known as zooxanthellae (genus Symbiodinium). Elevated temperature and intense light induce coral bleaching, where zooxanthellae are expelled from the host tissue. The primary cellular process in zooxanthellae which leads to coral bleaching is unresolved, and here, we investigated the sensitivity of the thylakoid membrane in a Symbiodinium culture and in genetically identified freshly isolated and expelled Symbiodinium cells. The fluorescence-temperature curve technique was used to measure the critical temperature (Tc) at which irreversible damage to the thylakoid membrane occurred. The accuracy of this technique was confirmed through the collection of scanning transmission electron micrographs which demonstrated the clear relationship between Tc and thylakoid membrane degradation. Analysis of 10 coral species with a diverse range of genetically distinct Symbiodinium communities showed a decline in Tc from summer to winter. A Symbiodinium culture and fragments of Pocillopora damicornis (Linnaeus, 1758) were exposed to a series of light and temperature treatments, where Tc increased from approximately 37 -C to 42 -C upon exposure to elevated temperature. Under bleaching conditions, the thermostability of the thylakoid membrane increased within 4 hrs by 5.1 -C, to a temperature far above bleaching thresholds, in both freshly isolated and photosynthetically competent zooxanthellae expelled from P. damicornis under these conditions. It is demonstrated that the thermostability of the thylakoid membrane increases in cultured, freshly isolated, and expelled zooxanthellae exposed to bleaching stress, suggesting it is not the primary site of impact during coral bleaching events.
Ulstrup, K.E., Hill, R., van Oppen, M.J., Larkum, A. & Ralph, P.J. 2008, 'Seasonal variation in the photo-physiology of homogeneous and heterogeneous Symbiodinium consortia in two scleractinian corals', Marine Ecology Progress Series, vol. 361, pp. 139-150.
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Seasonal variation in the composition of the algal endosymbiont community and photophysiology was determined in the corals Pocillopora damicornis,w hich show high local fidelity to one symbiont type (Symbiodinium C1) and Acropora valida, with a mixed Symbiodinium synbiont community, compromising members of both clades A and C. The relative abundances of Symbiodinium types varied overtime. A significant decline in symbiont densities in both coral species during the summer of 2005 coincided with a NOAA 'hotspot' warning for Heron Island. This also coincided with a relayiove increase in the presence and dominance of clade A in A. valida particularl in sun-adapted surfaces.
Hill, R. & Ralph, P.J. 2008, 'Dark-induced reduction of the plastoquinone pool in zooxanthellae of scleractinian corals and implications for measurements of chlorophyll a fluorescence', Symbiosis, vol. 46, pp. 45-56.
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Fluorometric measurements of maximum quantum yield (Fv/Fm) and fast induction curves (FICs) require coral samples to be dark-adapted (DA). Pathways causing dark-reduction of the plastoquinone (PQ) pool are shown here to be active in corals. Early morning sunlight and far-red light successfully increased Fv/Fm and lowered the O and J steps of FICs in corals that were darkened overnight. The thick-tissued massive coral, Cyphastrea serailia, was shown to be more prone to reduction of the PQ pool, with significant reductions in Fv/Fm occurring after 10 min of DA, and elevated J steps occurring within 200 s following a far-red flash. In thinner-tissued branching species, Pocillopora damicornis and Acropora nobilis, elevation of the J step also occurred within 200 s of DA, but a drop in Fv/Fm was only manifested after 30 min. Pre-exposure to far-red light is an effective and simple procedure to ensure determination of the true maximum quantum yield of Photosystem II (PSII) and accurate FICs which require a fully oxidised inter-system electron transport chain and open PSII reaction centres.
Hill, R. & Ralph, P.J. 2008, 'Impact of bleaching stress on the function of the oxygen evolving complex of zooxanthellae from scleractinian corals', Journal of Phycology, vol. 44, no. 2, pp. 299-310.
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Global climate change is leading to the rise of ocean temperatures and is triggering mass coral bleaching events on reefs around the world. The expulsion of the symbiotic dinoflagellate algae is believed to occur as a result of damage to the photosynthetic apparatus of these symbionts, although the specific site of initial impact is yet to be conclusively resolved. Here, the sensitivity of the oxygen evolving complex (OEC) to bleaching stress was studied as well as its natural variation between seasons. The artificial electron donor, diphenyl carbazide (DPC), was added to cultured, freshly isolated and expelled (bleaching treatments only) zooxanthellae suspensions. Chl a fluorescence and oxygen production measurements showed that upon addition of DPC, no restoration of diminished photochemical efficiency occurred under control or bleaching conditions. This result was consistent between 12h and 5d bleaching treatments on Pocilloporadamicornis, indicating that the OEC is not the primary site of damage, and that zooxanthellae expulsion from the host is a nonselective process with respect to the functioning of the OEC. Further experiments measuring fast induction curves (FICs) revealed that in both summer and winter, the temperature when OEC function was lost occurred between 7C and 14C above the sea surface temperature. FIC and oxygen production measurements of P. damicornis during exposure to bleaching stress demonstrated that the thermotolerance of the OEC increased above the temperature of the bleaching treatment over a 4h period. This finding indicates that the OEC has the capacity to acclimate between seasons and remains functional at temperatures well above bleaching thresholds.
Hill, R. & Ralph, P.J. 2007, 'Post-bleaching viability of expelled zooxanthellae from the scleractinian coral Pocillopora damicornis', Marine Ecology Progress Series, vol. 352, pp. 137-144.
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Coral bleaching events have been linked to elevated seawater temperatures in combination with intense light and can be characterised by the loss of symbionts (zooxanthellae, genus Symbiodinium) from the host tissue, as well as a reduction in photosynthetic pigments in these zooxanthellae. The long-term (days) viability of expelled zooxanthellae in the water column from the scleractiman coral Pocillopora damicornis was explored in this study through measurements of photosynthetic health and morphological condition. After initial expulsion, zooxanthellae were found to be photosynthetically competent and structurally intact. However, within 6 to 12 h following this time, photosystem II photochemical efficiency dramatically declined in these cells and photosynthetic damage was gradually manifested in the loss of structural integrity of the cell. The time of expulsion during bleaching exposure, as well as ambient water temperature, greatly influenced survivorship. Expelled zooxanthellae were collected at 4 different time intervals (0-6, 6-12, 12-24 and 24-36 h) following the onset of exposure to bleaching conditions (32 degrees C and 400 mu mol photons m(-2) s(-1)) and then maintained at 28, 30 or 32 degrees C and 100 mu mol photons m(-2) s(-1) for up to 96 h. Those cells expelled within the first 6 h of bleaching and held at 28 degrees C (lagoon temperature) had the greatest longevity, although even in this treatment, long-term photosynthetic viability was restricted to 5 d in the water column. This suggests that unless expelled zooxanthellae inhabit other environments of coral reefs (such as sediments) which may be more favourable for survival, their capacity for persistence in the environment is extremely limited.
Scanes, P., Coade, G., Doherty, M. & Hill, R. 2007, 'Evaluation of the utility of water quality based indicators of estuarine condition in NSW, Australia', Estuarine, Coastal And Shelf Science, vol. 74, no. 1-2, pp. 306-319.
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Environmental indicators must have a predictable relationship with stressors to be of value in ecological assessments. We evaluated the information provided by commonly implemented monitoring indictaors as a means of assessing of the level of ecological impact experienced by coastal lagoons in NSW, Australia. Existing data for environemtal variables in coastal lagoons were correlated with independent estimates of catchment disturbance.
Hill, R. & Ralph, P.J. 2006, 'Photosystem II Heterogeneity of in hospite Zooxanthellae in Scleractinian Corals Exposed to Bleaching Conditions', Photochemistry and Photobiology, vol. 82, no. 6, pp. 1577-1585.
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Increased ocean temperatures are thought to be triggering mass coral bleaching events around the world. The intracellular symbiotic zooxanthellae (genus Symbiodinium) are expelled from the coral host, which is believed to be a response to photosynthetic damage within these symbionts. Several sites of impact have been proposed, and here we probe the functional heterogeneity of Photosystem II (PSII) in three coral species exposed to bleaching conditions. As length of exposure to bleaching conditions (32 degrees C and 350 mu mol photons m(-2) s(-1)) increased, the Q(A)(-) reoxidation kinetics showed a rise in the proportion of inactive PSII centers (PSIIX), where Q(B) was unable to accept electrons. PSIIX contributed up to 20% of the total PSII centers in Pocillopora damicornis, 35% in Acropora nobilis and 14% in Cyphastrea serailia. Changes in F-V/F-M and amplitude of the J step along fast induction curves were found to be highly dependent upon the proportion of PSIIx centers within the total pool of PSII reaction centers. Determination of PSII antenna size revealed that under control conditions in the three coral species up to 60% of PSII centers were lacking peripheral light-harvesting complexes (PSII beta). In P. damicornis, the proportion of PSII beta increased under bleaching conditions and this could be a photoprotective mechanism in response to excess light. The rapid increases in PSIIX and PSII beta observed in these corals under bleaching conditions indicates these physiological processes are involved in the initial photochemical damage to zooxanthellae.
Hill, R., Frankart, C. & Ralph, P.J. 2005, 'Impact of bleaching conditions on the components of non-photochemical quenching in the zooxanthellae of a coral', Journal Of Experimental Marine Biology And Ecology, vol. 322, no. 1, pp. 83-92.
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Mass coral bleaching events are a worldwide phenomenon, which generally occur during periods of elevated sea surface temperature and intense sunlight. These conditions result in a decline in photochemical efficiency of symbiotic microalgae (zooxanthellae
Hill, R. & Ralph, P.J. 2005, 'Diel and seasonal changes in fluorescence rise kinetics of three scleractinian corals', Functional Plant Biology, vol. 32, no. 6, pp. 549-559.
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The effect of diel oscillations in light on the photosynthetic response of three coral species during summer and winter was studied. Fast induction curves revealed detailed information on primary photochemistry as well as redox states of electron accepto
Ulstrup, K.E., Hill, R. & Ralph, P.J. 2005, 'Photosynthetic impact of hypoxia on in hospite zooxanthellae in the scleractinian coral Pocillopora damicornis', Marine Ecology-Progress Series, vol. 286, pp. 125-132.
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Shallow water coral reefs may experience hypoxia under conditions of calm weather doldrums. Anaerobic responses of endosymbionts (i.e. zooxanthellae) within Pocillopora damicornis coral colonies were tested using both slow and fast chlorophyll a fluoresc
Hill, R., Larkum, A., Frankart, C., Kuehl, M. & Ralph, P.J. 2004, 'Loss of functional Photosystem II reaction centres in zooxanthellae of corals exposed to bleaching conditions: using fluorescence rise kinetics', Photosynthesis Research, vol. 82, pp. 59-72.
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Hill, R., Schreiber, U., Gademann, R., Larkum, A., Kuehl, M. & Ralph, P.J. 2004, 'Spatial heterogeneity of photosynthesis and the effect of temperature-induced bleaching condition in three species of corals', Marine Biology, vol. 144, pp. 633-640.
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Major, R., Pyke, G.H., Christy, M., Gowing, G. & Hill, R. 1994, 'Can Nest Predation Explain The Timing Of The Breeding-Season And The Pattern Of Nest Dispersion Of New-Holland Honeyeaters', OIKOS, vol. 69, no. 3, pp. 364-372.
We tested the following two predictions of the hypotheses that predation rate may select for nest spacing and winter breeding in New Holland honeyeaters: (a) the level of nest predation should be lower during the breeding season than outside it, and (b)

Reports

Ralph, P.J., Wilson, K., Hill, R. & Petrou, K. 2007, 'Effects of increased temperature pulses on temperate seagrass: progress reports 1-4', Institute for Water and Environmental Resource Management, and Department of Environmental Sciences,, Sydney, pp. 1-14.