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Professor Peter Ralph

Biography

As the Executive Director of The Plant Functional Biology and Climate Change Cluster (C3) I have the privilege of leading a dynamic, multidisciplinary team dedicated to improving our predictions about the impacts of climate change.

Over the past 20 years my research has examined seagrasses, freshwater macrophytes, macroalgae and terrestrial plants from the scale of whole organisms to cellular and biochemical processes.

Due to the expertise that I have developed in the measurement of photosynthetic processes in seagrasses I am a member of the Blue Carbon International Scientific Working Group, formed under the auspices of the International Union for the Conservation of Nature, United Nations Environmental Program and the Intergovernmental Oceanographic Commission. In addition I am also an invited member of the Integrated Marine Observing System National Bio-optical Working Group.

Within C3 I am also the Team Leader for the Aquatic Processes Group (APG): a team of both highly experienced and outstanding early career marine ecologists, biologists and oceanographers. The APG has developed major strengths in assessing the impact of human-induced change, as well as climate change, on ecologically important aquatic plant systems.

Within the APG I oversee specialist teams that support research into



UTS is the administering body for the newly established CSIRO Marine and Coastal Carbon Biogeochemistry Cluster of which I am the Co- Leader. This brings together the expertise of CSIRO and the research capabilities of eight Australian universities in Australia's largest ever coastal blue carbon accounting, mapping and measurement study.

Professional

Professional Activities
Review staff for Marine Ecology-Progress Series

Co-convener of ARC network meeting BEAM January 2004

Co-convened conference: International Workshop on Marine Applications of Chlorophyll a Fluorescence.
University of Sydney, 4-8 February, 2000.

Co-convened conference: International Workshop on Marine Applications of Chlorophyll a Fluorescence.
University of Sydney, 4-8 April, 1998.

Co-convener of ASPAB
University of Sydney, 13-15 February 2006


Recent Media Releases



Employment History
Current Position Professor
2001-2003 University Reader
1999-2002 Senior Lecturer
1997-1999 Lecturer and Program Director of Coastal Resource Management, UTS
1997-1998 Associate Lecturer, UTS

Image of Peter Ralph
Director, Plant Functional Biology & Climate Change
Professor, School of the Environment
Associate Member, Centre for Technology in Water and Wastewater
Director, Plant Functional Biology & Climate Change
Core Member, Plant Functional Biology & Climate Change
BAppSc (NSWIT), MAIBiol (UTS), PhD (UTS)
 
Phone
+61 2 9514 4070
Room
CB04.05.43B

Research Interests

Aquatic Processes Group

Can supervise: Yes

  • Marine Primary Producers
  • Coastal and Marine Ecosystems
  • Tropical Reef Ecosystems
  • GIS and Resource Assessments
  • Australian Biota
  • Biocomputing
  • Mapping and Remote Sensing
  • Biology and Ecology for Engineers

Book Chapters

Ralph, P.J., Wilhelm, C., Lavaud, J., Jakob, T., Petrou, K. & Kranz, S.A. 2011, 'Fluorescence as a Tool to Understand Changes in Photosynthetic Electron Flow Regulation' in David J Suggett, Michael A Borowitzka and Ondrej Prasil (eds), Chlorophyll a Fluorescence in Aquatic Sciences : Methods and Applications, Springer, United Kingdom, pp. 75-89.
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This chapter investigates the use of chlorophyll a fluorescence to better understand changes in the regulation of photosynthetic electron transport. It describes the different electron pathways utilised by photosynthetic organisms, including pathways used in photosynthesis as well as alternative electron cycling (AEC). The major photoprotective processes are described, in particular, non-photochemical quenching (NPQ) and its three components, energy-dependent quenching (qE), state-transition quenching (qT), and photoinhibition (qI). Fluorescence and NPQ responses to light stress are compared across a higher plant, diatom and cyanobacteria. Photosynthesis is a complex interaction of complementary processes making the identification and isolation of a particular photosynthetic pathway or process inherently difficult. Therefore, we describe the use of chemicals which allow for the differentiation of mechanistic photosynthetic processes, such as electron transport pathways, CO2 fixation and the use of trans-thylakoid proton gradients, which can be effectively understood and quantified using chlorophyll fluorescence detection techniques.
Warner, M.E., Lesser, M.P. & Ralph, P.J. 2011, 'Chlorophyll fluorescence in reef building corals' in David J Suggett, Michael A Borowitzka and Ondrej Prasil (eds), Chlorophyll a Fluorescence in Aquatic Sciences : Methods and Applications, Springer, UK, pp. 209-221.
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The ecological success of reef-building corals throughout the tropics is due in large part to the endosymbiotic dinoflagellates that reside within the gastrodermal cells of these cnidarian hosts. These algae, belonging to the genus Symbiodinium, are often referred to by the common term of +zooxanthellae.+ This mutualism between Symbiodinium spp. and tropical and sub-tropical coral species has been a key component to the evolutionary persistence of reef-building corals since the Triassic (Stanely 2003). The importance of these algae in the long-term success of reef-building corals cannot be over emphasized, as they can contribute a significant portion of photosynthetically derived carbon to the host via translocation. The coral metabolizes this carbon, thereby meeting up to 90 percent or more of the animal+s daily metabolic demand from the byproducts of photosynthesis by the symbionts (Muscatine 1990).
Larkum, A., Drew, E.A. & Ralph, P.J. 2006, 'Photosynthesis and Metabolism in Seagrasses at the Cellular Level' in Larkum AWD; Orth RJ; Dyarte CM (eds), Seagrasses:Biology, Ecology and Conservation, Springer, Dordrecht, The Netherlands, pp. 323-345.
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Ralph, P.J., Tomasko, D., Moore, K.A., Seddon, S. & Macinnis-Ng, C.M. 2006, 'Human impacts on seagrasses: Eutrophication, sedimentation and contamination' in Larkum AWD; Orth RJ; Duarte CM (eds), Seagrasses: Biology, Ecology and Conservation, Springer, The Netherlands, pp. 567-593.
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Beer, S., Bjork, M., Gademann, R. & Ralph, P.J. 2001, 'Measurements of Photosynthetic Rates in Seagrasses' in Short FT; Coles RG (eds), Global Seagrass Research Methods, Elsevier Science, Netherlands, pp. 183-198.
Ralph, P.J., Brown, K., Wearing, S.L. & Nudd, B. 1998, 'GIS - A tool for integrating tourism and mariculture in Wallis Lakes' in Wearing, Stephen (eds), Planning Recreation and Tourism with Australian Communities, HM Leisure Planning Pty Ltd, Melbourne, pp. 95-102.

Conference Papers

Howes, J.M., Stuart, B.H. & Ralph, P.J. 2013, 'Assessing metabolic variation of endosymbiotic and cultured Symbiodinium microadriaticum using synchrotron imaging FTIR spectroscopy', 7th International Workshop on Infrared Microscopy and Spectroscopy with Accelerator-Based Sources in 7th International Workshop on Infrared Microscopy and Spectroscopy with Accelerator-Based Sources Abstracts.
Howes, J.M., Stuart, B.H. & Ralph, P.J. 2013, 'Macromolecular composition varies significantly between genetic clades of Symbiodinium microadriaticum', 10th International Phycological Congress in 10th International Phycological Congress Abstracts.
Chartrand, K.M., Rasheed, M., Petrou, K. & Ralph, P.J. 2012, 'Establishing tropical seagrass light requirements in a dynamic port environment', Cairns, July 2012 in Proceedings of the 12th International Coral Reef Symposium, Cairns, Australia, 9-13 July 2012, ed -, ReefBase, Australia.
Tropical seagrasses inhabit naturally turbid waters with dynamic light environments and variable water quality in coastal waters adjacent to the Great Barrier Reef. Large tidal fluxes amplify the magnitude of these conditions with extreme high and low light over relatively short time scales (i.e. hours). Large port developments in the region have the potential to confound the complex relationships between seagrass physiology and this dynamic light field with the onset of dredging and their associated turbid plumes. Understanding the capacity for seagrasses to respond to changes in the quantity and quality of the light environment will allow for prediction of how seagrass species and populations will tolerate changes in light attenuation that may occur during dredging. We present a strategy for determining seasonal-specific light requirements for an intertidal tropical seagrass community in a port environment. Locally relevant light requirements are established by describing the relationships among photosynthetic inputs and losses, tidal exposure, shifts in spectral light quality, seasonality and the capacity to utilise below ground carbon reserves. The outcomes of the study provide guidelines for a mitigation strategy that is focused on maintaining critical windows of light to support seagrass growth and the longer term survival of these productive coastal ecosystems.
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.
Petrou, K., Doblin, M.A., Hassler, C.S. & Ralph, P.J. 2009, 'Multiple stressors on the sea ice diatom Fragilariopsis cylindrus - photophysiological impacts of seasonal freezing and melting of sea ice', Japan, August 2009.
Doblin, M.A., Ralph, P.J., Oubelkheir, K., Hassler, C.S., Suthers, I. & Thompson, P. 2009, 'Using IMOS to bridge the gap between direct measurements of marine primary production and models', Adelaide, Australia, July 2009.
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.
Petrou, K., Shelly, K., Hassler, C.S., Schoemann, V., Doblin, M.A. & Ralph, P.J. 2007, 'Ocean productivity in a changing world: Iron-limitation of Southern Ocean phytoplankton and implication for Antarctic meltwater productivity', Australia, July 2007.

Journal Articles

Macreadie, P.I., Schliep, M.T., Rasheed, M., Chartrand, K.M. & Ralph, P.J. 2014, 'Molecular indicators of chronic seagrass stress: A new era in the management of seagrass ecosystems?', Ecological Indicators, vol. 38, pp. 279-281.
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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
Tamburic, B., Guruprasad, S., Radford, D.T., Szabo, M., Lilley, R., Larkum, A., Franklin, J.B., Kramer, D., Blackburn, S.I., Raven, J., Schliep, M.T. & Ralph, P.J. 2014, 'The effect of diel temperature and light cycles on the growth of Nannochloropsis oculata in a photobioreactor matrix', PLoS One, vol. 9, no. 1, p. e86047.
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Wangpraseurt, D., Larkum, A., Franklin, J.B., Szabo, M., Ralph, P.J. & Kuhl, M. 2014, 'Lateral light transfer ensures efficient resource distribution in symbiont-bearing corals', Journal of Experimental Biology, vol. 217, pp. 489-498.
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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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Brodersen, K.E., Lichtenberg, M., Ralph, P.J., Kuhl, M. & Wangpraseurt, D. 2014, 'Radiative energy budget reveals high photosynthetic efficiency in symbiont-bearing corals', Journal of the Royal Society Interface, vol. 11, p. 20130997.
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Petrou, K., Trimborn, S., Rost, B., Ralph, P.J. & Hassler, C.S. 2014, 'The impact of iron limitation on the physiology of the Antarctic diatom Chaetoceros simplex', Marine Biology, vol. 161, pp. 925-937.
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Iron availability strongly governs the growth of Southern Ocean phytoplankton. To investigate how iron limitation affects photosynthesis as well as the uptake of carbon and iron in the Antarctic diatom Chaetoceros simplex, a combination of chlorophyll a fluorescence measurements and radiotracer incubations in the presence and absence of chemical inhibitors was conducted. Iron limitation in C. simplex led to a decline in growth rates, photochemical efficiency and structural changes in photosystem II (PSII), including a reorganisation of photosynthetic units in PSII and an increase in size of the functional absorption cross section of PSII. Iron-limited cells further exhibited a reduced plastoquinone pool and decreased photosynthetic electron transport rate, while non-photochemical quenching and relative xanthophyll pigment content were strongly increased, suggesting a photoprotective response. Additionally, iron limitation resulted in a strong decline in carbon fixation and thus the particulate organic carbon quotas. Inhibitor studies demonstrated that, independent of the iron supply, carbon fixation was dependent on internal, but not on extracellular carbonic anhydrase activity. Orthovanadate more strongly inhibited iron uptake in iron-limited cells, indicating that P-type ATPase transporters are involved in iron uptake. The stronger reduction in iron uptake by ascorbate in iron-limited cells suggests that the re-oxidation of iron is required before it can be taken up and further supports the presence of a high-affinity iron transport pathway. The measured changes to photosystem architecture and shifts in carbon and iron uptake strategies in C. simplex as a result of iron limitation provide evidence for a complex interaction of these processes to balance the iron requirements for photosynthesis and carbon demand for sustained growth in iron-limited waters.
Zhang, D., Glasby, T., Ralph, P.J. & Gribben, P.E. 2014, 'Mechanisms Influencing the Spread of a Native Marine Alga', PLoS One, vol. 9, no. 4, pp. e94647-e94647.
Like invasive macrophytes, some native macrophytes are spreading rapidly with consequences for community structure. There is evidence that the native alga Caulerpa filiformis is spreading along intertidal rocky shores in New South Wales, Australia, seemingly at the expense of native Sargassum spp. We experimentally investigated the role physical disturbance plays in the spread of C. filiformis and its possible consequences for Sargassum spp. Cleared patches within beds of C. filiformis (Caulerpa habitat) or Sargassum spp. (Sargassum habitat) at multiple sites showed that C. filiformis had significantly higher recruitment (via propagules) into its own habitat. The recruitment of Sargassum spp. to Caulerpa habitat was rare, possibly due in part to sediment accretion within Caulerpa habitat. Diversity of newly recruited epibiotic assemblages within Caulerpa habitat was significantly less than in Sargassum habitat. In addition, more C. filiformis than Sargassum spp. recruited to Sargassum habitat at some sites. On common boundaries between these two macroalgae, the vegetative growth of adjacent C. filiformis into cleared patches was significantly higher than for adjacent Sargassum spp. In both experiments, results were largely independent of the size of disturbance (clearing). Lastly, we used PAM fluorometry to show that the photosynthetic condition of Sargassum spp. fronds adjacent to C. filiformis was generally suppressed relative to those distant from C. filiformis. Thus, physical disturbance, combined with invasive traits (e.g. high levels of recruitment and vegetative growth) most likely facilitate the spread of C. filiformis, with the ramifications being lower epibiotic diversity and possibly reduced photosynthetic condition of co-occurring native macrophytes.
Wangpraseurt, D., Polerecky, L., Larkum, A., Ralph, P.J., Nielsen, D.A., Pernice, M. & Kuhl, M. 2014, 'The in situ light microenvironment of corals', Limnology and Oceanography, vol. 59, no. 3, pp. 917-926.
We used a novel diver-operated microsensor system to collect in situ spectrally resolved light fields on corals with a micrometer spatial resolution. The light microenvironment differed between polyp and coenosarc tissues with scalar irradiance (400+700 nm) over polyp tissue, attenuating between 5.1- and 7.8-fold from top to base of small hemispherical coral colonies, whereas attenuation was at most 1.5-fold for coenosarc tissue. Fluctuations in ambient solar irradiance induced changes in light and oxygen microenvironments, which were more pronounced and faster in coenosarc compared with polyp tissue. Backscattered light from the surrounding benthos contributed . 20% of total scalar irradiance at the coral tissue surface and enhanced symbiont photosynthesis and the local O2 concentration, indicating an important role of benthos optics for coral ecophysiology. Light fields on corals are species and tissue specific and exhibit pronounced variation on scales from micrometers to decimeters. Consequently, the distribution, genetic diversity, and physiology of coral symbionts must be coupled with the measurements of their actual light microenvironment to achieve a more comprehensive understanding of coral ecophysiology.
Tout, J.A., Jeffries, T.C., Webster, N.S., Stocker, R., Ralph, P.J. & Seymour, J.R. 2014, 'Variability in Microbial Community Composition and Function Between Different Niches Within a Coral Reef', Microbial Ecology, vol. 67, pp. 540-552.
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To explore how microbial community composition and function varies within a coral reef ecosystem, we performedmetagenomic sequencing of seawater fromfour niches across Heron Island Reef, within the Great Barrier Reef. Metagenomes were sequenced from seawater samples associated with (1) the surface of the coral species Acropora palifera, (2) the surface of the coral species Acropora aspera, (3) the sandy substrate within the reef lagoon and (4) open water, outside of the reef crest. Microbial composition and metabolic function differed substantially between the four niches. The taxonomic profile showed a clear shift from an oligotroph-dominated community (e.g. SAR11, Prochlorococcus, Synechococcus) in the open water and sandy substrate niches, to a community characterised by an increased frequency of copiotrophic bacteria (e.g. Vibrio, Pseudoalteromonas, Alteromonas) in the coral seawater niches. The metabolic potential of the four microbial assemblages also displayed significant differences, with the open water and sandy substrate niches dominated by genes associated with core house-keeping processes such as amino acid, carbohydrate and protein metabolism as well as DNA and RNA synthesis and metabolism. In contrast, the coral surface seawater metagenomes had an enhanced frequency of genes associated with dynamic processes including motility and chemotaxis, regulation and cell signalling. These findings demonstrate that the composition and function of microbial communities are highly variable between niches within coral reef ecosystems and that coral reefs host heterogeneous microbial communities that are likely shaped by habitat structure, presence of animal hosts and local biogeochemical conditions.
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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Gustafsson, M.S., Baird, M.E. & Ralph, P.J. 2013, 'The interchangeability of autotrophic and heterotrophic nitrogen sources in Scleractinian coral symbiotic relationships: A numerical study', Ecological Modelling, vol. 250, pp. 183-194.
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The success of corals in tropical oligotrophic waters depends largely on their symbiotic relationship with the dinoflagellate algae residing in their tissues. Understanding the dynamics of this symbiosis is essential to predict how corals respond to environmental stressors, such as changes in nutrients availability, water temperatures and irradiance. This study presents a numerical model of the symbiotic relationship between a heterotrophic coral (cnidarian) host and autotrophic symbiotic dinoflagellates, including the major metabolic and physical functions of the system, under non-bleaching conditions. The coral acquires nitrogen (N) through two processes, uptake of dissolved inorganic nitrogen (VH DIN) and heterotrophic feeding (ZN). Numerical experiments were used to highlight the importance of these different sources of N for coral survival and growth. The model was analyzed for four external nutrient supply scenarios, using combinations of two VH DIN rates (high and low) and two ZN rates (high and low), and for a range of light levels. The model outputs showed the importance of the algae symbionts to the coral host as a source of both N and C when the feeding rate was limited, with heterotrophic feeding providing only 14% of the N needed to sustain the host biomass for the low ZN + high VH DIN scenario. In contrast, with no light or low light, conditions under which the symbiont population dies, the host was able to survive if ZN was high. Living inside the host the symbiont population thrived as long as there was enough light, as well as, DIN and DIC in the host tissues, independent of whether N was supplied as ZN or VH DIN. Translocation and recycling of nutrient were two of the most important features of this model, emphasizing why it is essential to resolve host and symbiont in a coral model. The model highlights that the interchangeability of N sources, and the ability to exchange and recycle nutrients in the host-symbiont system, is the key to coral survival in nutrient poor environments.
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.
Baird, M.E., Ralph, P.J., Rizwi, F., Wild-Allen, K. & Steven, A. 2013, 'A dynamic model of the cellular carbon to chlorophyll ratio applied to a batch culture and a continental shelf ecosystem', Limnology and Oceanography, vol. 58, no. 4, pp. 1215-1226.
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A novel parameterization of the dynamical relationship between cellular carbon (C) and chlorophyll (Chl) is developed using a Chl synthesis term that includes the physiological status of the cell and the effect of packaging of pigments within cells. The geometric derivation highlights the non-linear relationship between Chl content and absorption due to the package effect. When parameterized for a generic 3 mm radius phytoplankton cell, the model reproduces the magnitude and daily variations of C: Chl and C: nitrogen ratios of the diatom Skeletonema costatum in published laboratory experiments. The parameterization is then applied in a three-dimensional biogeochemical model containing three phytoplankton classes in the coastal waters off southeast Tasmania, Australia, which demonstrates the behavior of the dynamic Chl parameterization over a range of light- and nutrient-limiting environments for phytoplankton of different sizes and growth rates. The model produces C: Chl ratios of , 12+20 (weight : weight) and , 60+80 for phytoplankton communities dominated by fast-growing small and fast-growing large cells, respectively, close to the ratios of 17 and 76 observed at two sampling stations during periods with diatom- and flagellate-dominated communities. Throughout the simulation, community C: Chl ratios generally vary between 12 and 200, which is similar to the range observed globally. In the new parameterization, C: Chl ratios are most influenced by the package effect for light-limited, slow-growing large microalgae, with physiological processes becoming important for smaller, nutrient-limited, fast-growing microalgae.
Petrou, K., Jimenez-denness, I., Chartrand, K.M., Mccormack, C., Rasheed, M. & Ralph, P.J. 2013, 'Seasonal heterogeneity in the photophysiological response to air exposure in two tropical intertidal seagrass species', Marine Ecology Progress Series, vol. 482, no. NA, pp. 93-106.
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Photosynthesis, chlorophyll a fluorescence, leaf bio-optical properties and pigments were measured in 2 tropical intertidal seagrass species, Zostera muelleri ssp. capricorni and Halophila ovalis before, during and after air-exposure over a tidal cycle.
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
Clark, J.S., Poore, A.G., Ralph, P.J. & Doblin, M.A. 2013, 'Potential for adaptation in response to thermal stress in an intertidal macroalga', Journal of Phycology, vol. 49, no. 4, pp. 630-639.
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Understanding responses of marine algae to changing ocean temperatures requires knowledge of the impacts of elevated temperatures and the likelihood of adaptation to thermal stress. The potential for rapid evolution of thermal tolerance is dependent on the levels of heritable genetic variation in response to thermal stress within a population. Here, we use a quantitative genetic breeding design to establish whether there is a heritable variation in thermal sensitivity in two populations of a habitat-forming intertidal macroalga, Hormosira banksii (Turner) Descaisne. Gametes from multiple parents were mixed and growth and photosynthetic performance were measured in the resulting embryos, which were incubated under control and elevated temperature (20C and 28C). Embryo growth was reduced at 28C, but significant interactions between male genotype and temperature in one population indicated the presence of genetic variation in thermal sensitivity. Selection for more tolerant genotypes thus has the ability to result in the evolution of increased thermal tolerance. Furthermore, genetic correlations between embryos grown in the two temperatures were positive, indicating that those genotypes that performed well in elevated temperature also performed well in control temperature. Chlorophyll a fluorescence measurements showed a marked decrease in maximum quantum yield of photosystem II (PSII) under elevated temperature. There was an increase in the proportion of energy directed to photoinhibition (nonregulated nonphotochemical quenching) and a concomitant decrease in energy used to drive photochemistry and xanthophyll cycling (regulated nonphotochemical quenching). However, PSII performance between genotypes was similar, suggesting that thermal sensitivity is related to processes other than photosynthesis.
Hong, Y., Burford, M.A., Ralph, P.J., Udy, J.W. & Doblin, M.A. 2013, 'The cyanobacterium Cylindrospermopsis raciborskii is facilitated by copepod selective grazing', Harmful Algae, vol. 29, no. 1, pp. 14-21.
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Blooms of the toxin-producing cyanobacterium Cylindrospermopsis raciborskii occur in tropical and subtropical lakes during spring-summer but the mechanisms behind bloom formation are unclear. This study tests the hypothesis that C. raciborskii accumulations in freshwater systems are facilitated by selective copepod grazing. Prey selection was examined in a series of experiments with C. raciborskii and the green alga, Chlamydomonas reinhardtii, as well as within natural phytoplankton assemblages. Clearance rates of the copepod Boeckella sp. on a C. raciborskii diet were 2+4 times lower than that of a common cladoceran Ceriodaphnia sp. when both grazers had prey choice. More C. raciborskii was cleared by Boeckella sp. when in mixed natural phytoplankton assemblages, but the clearance rate declined when nutrient replete C. reinhardtii was added, demonstrating that when alternate +high quality+ algae were present, so did C. raciborskii consumption. The clearance rates of Boeckella sp. on two toxic C. raciborskii strains were significantly lower than on a non-toxic strain, and on C. raciborskii with low cellular P content. When we tested the grazing preference of a copepod dominated mixed zooplankton community on C. raciborskii during the early bloom period, clearance rates were relatively low (0.05+0.20 ml individual-1 h-1), and decreased significantly as the proportion of C. raciborskii increased above 5%. These results suggest that C. raciborskii persistence could be promoted by copepods preferentially grazing on other algae, with significant loss of top-down control as C. raciborskii abundance increases.
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.
Macreadie, P.I., Allen, K., Kelaher, B.P., Ralph, P.J. & Skilbeck, C.G. 2012, 'Paleoreconstruction of estuarine sediments reveal human-induced weakening of coastal carbon sinks', Global Change Biology, vol. 18, no. 3, pp. 891-901.
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Human activities in coastal areas frequently cause loss of benthic macrophytes (e.g. seagrasses) and concomitant increases in microalgal production through eutrophication. Whether such changes translate into shifts in the composition of sediment detritus is largely unknown, yet such changes could impact the role these ecosystems play in sequestrating CO2. We reconstructed the sedimentary records of cores taken from two sites within Botany Bay, Sydney the site of European settlement of Australia to look for human-induced changes in dominant sources of detritus in this estuary. Cores covered a period from the present day back to the middle Holocene (6000years) according to 210Pb profiles and radiocarbon (14C) dating. Depositional histories at both sites could not be characterized by a linear sedimentation rate; sedimentation rates in the last 3050years were considerably higher than during the rest of the Holocene. C:N ratios declined and began to exhibit a microalgal source signature from around the time of European settlement, which could be explained by increased nutrient flows into the Bay caused by anthropogenic activity. Analysis of stable isotopic ratios of 12C/13C showed that the relative contribution of seagrass and C3 terrestrial plants (mangroves, saltmarsh) to detritus declined around the time of rapid industrial expansion (1950s), coinciding with an increase in the contribution of microalgal sources. We conclude that the relative contribution of microalgae to detritus has increased within Botany Bay, and that this shift is the sign of increased industrialization and concomitant eutrophication.
Petrou, K., Kranz, S.A., Doblin, M.A. & Ralph, P.J. 2012, 'Photophysiological responses of Fragilariopsis cylindrus (Bacillariophyceae) to nitrogen depletion at two temperatures', Journal of Phycology, vol. 48, no. 1, pp. 127-136.
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The photosynthetic efficiency and photoprotective capacity of the sea-ice diatom, Fragilariopsis cylindrus (Grunow) W. Krieg., grown in a matrix of nitrogen repletion and depletion at two different temperatures (-1 degrees C and +6 degrees C) was investigated. Temperature showed no significant effect on photosynthetic efficiency or photoprotection in F. cylindrus. Cultures under nitrogen depletion showed enhanced photoprotective capacity with an increase in nonphotochemical quenching (NPQ) when compared with nitrogen-replete cultures. This phenomenon was achieved at no apparent cost to the photosynthetic efficiency of PSII (FV/FM). Nitrogen depletion yielded a partially reduced electron transport chain in which maximum fluorescence (FM) could only be obtained by adding 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU). reoxidation curves showed the presence of QB nonreducing PSII centers under nitrogen depletion. Fast induction curves (FICs) and electron transport rates (ETRs) revealed slowing of the electrons transferred from the primary (QA) to the secondary (QB) quinone electron acceptors of PSII. The data presented show that nitrogen depletion in F. cylindrus leads to the formation of QB nonreducing PSII centers within the photosystem. On a physiological level, the formation of QB nonreducing PSII centers in F. cylindrus provides the cell with protection against photoinhibition by facilitating the rapid induction of NPQ. This strategy provides an important ecological advantage, especially during the Antarctic spring, maintaining photosynthetic efficiency under high light and nutrient-limiting conditions.
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.
Jimenez Denness, I.M., Larkum, A., Ralph, P.J. & Kuhl, M. 2012, 'In situ thermal dynamics of shallow water corals is affected by tidal patterns and irradiance', Marine Biology, vol. 159, pp. 1773-1782.
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We studied the diel variation of in situ coral temperature, irradiance and photosynthetic performance of hemispherical colonies of Porites lobata and branching colonies of Porites cylindrica during different bulk water temperature and tidal scenarios on the shallow reef flat of Heron Island, Great Barrier Reef, Australia. Our study presents in situ evidence that coral tissue surface temperatures can exceed that of the surrounding water under environmental conditions typically occurring during low tide in shallow reef or lagoon environments. Such heating may be a regular occurrence on shallow reef flats, triggered by the combined effects of high irradiance and low water flow characteristic of low Spring tides. At these times, solar heating of corals coincides with times of maximum water temperature and high irradiance, where the slow flow and consequent thick boundary layers impede heat exchange between corals and the surrounding water. Despite similar light-absorbing properties, the heating effect was more pronounced for the hemispherical P. lobata than for the branching P. cylindrica. This is consistent with previous laboratory experiments showing the evidence of interspecific variation in coral thermal environment and may result from morphologically influenced variation in convective heat transfer and/or thermal properties of the skeleton. Maximum coral surface warming did not coincide with maximum irradiance, but with maximum water temperature, well into the low-tide period with extremely low water flow in the partially drained reef flat, just prior to flushing by the rising tide. The timing of low tide thus influences the thermal exposure and photophysiological performance of corals, and the timing of tidally driven coral surface warming could potentially have different physiological impacts in the morning or in the afternoon.
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.
Wangpraseurt, D., Larkum, A., Ralph, P.J. & Kuhl, M. 2012, 'Light gradients and optical microniches in coral tissues', Frontiers in Microbiology, vol. 3, no. 316, pp. 1-9.
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Light quantity and quality are among the most important factors determining the physiology and stress response of zooxanthellate corals. Yet, almost nothing is known about the light ?eld that Symbiodinium experiences within their coral host, and the basic optical properties of coral tissue are unknown. We used scalar irradiance microprobes to characterize vertical and lateral light gradients within and across tissues of several coral species. Our results revealed the presence of steep light gradients with photosynthetically available radiation decreasing by about one order of magnitude from the tissue surface to the coral skeleton. Surface scalar irradiance was consistently higher over polyp tissue than over coenosarc tissue in faviid corals. Coral bleaching increased surface scalar irradiance by ~150% (between 500 and 700 nm) relative to a healthy coral. Photosynthesis peaked around 300 m within the tissue, which corresponded to a zone exhibiting strongest depletion of scalar irradiance. Deeper coral tissue layers, e.g., ~1000 m into aboral polyp tissues, harbor optical microniches, where only ~10% of the incident irradiance remains. We conclude that the optical microenvironment of corals exhibits strong lateral and vertical gradients of scalar irradiance, which are affected by both tissue and skeleton optical properties. Our results imply that zooxanthellae populations inhabit a strongly heterogeneous light environment and highlight the presence of different optical microniches in corals; an important ?nding for understanding the photobiology, stress response, as well as the phenotypic and genotypic plasticity of coral symbionts.
Wilson, K.G. & Ralph, P.J. 2012, 'Laboratory testing protocol for the impact of dispersed petrochemicals on seagrass', Marine Pollution Bulletin, vol. 64, no. 11, pp. 2421-2427.
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To improve the effectiveness of oil spill mitigation, we developed a rapid, logistically simple protocol to detect petrochemical stress on seagrass. Sections of leaf blades from Zostera muelleri subsp. capricorni were exposed to the water accommodated fraction (WAF) of non-dispersed and dispersed Tapis crude oil and fuel oil (IFO-380) for 5 h. Photosynthetic health was monitored by assessing changes in effective quantum yield of photosystem II () and chlorophyll a pigment concentrations. Loss of total petroleum hydrocarbons (TPH) was measured using an oil-in-water fluorometer, whilst GC+MS analyses quantified the hydrocarbon components within each treatment. Few significant differences were detected in the chlorophyll a pigment analyses; however, appeared sensitive to petrochemical exposure. Dispersing both types of oil resulted in a substantial increase in the TPH of the WAF and was generally correlated with a greater physiological impact to the seagrass health, compared with the oil alone.
Jimenez Denness, I.M., Larkum, A., Ralph, P.J. & Kuhl, M. 2012, 'Thermal effects of tissue optics in symbiont-bearing reef-building corals', Limnology and Oceanography, vol. 57, no. 6, pp. 1816-1825.
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Reflectance spectroscopy and microscale temperature measurements were used to investigate links between optical and thermal properties of corals. Coral tissue heating showed a species-specific linear correlation to the absorptance of incident irradiance. Heat budgets estimated from absorptance and thermal boundary layer measurements indicated differences in the relative contribution of convection and conduction to heat loss in Porites lobata and Stylophora pistillata, and a higher heat conduction into the skeleton of the thin-tissued branching S. pistillata as compared to the massive thick-tissued P. lobata. Decreasing absorptance associated with bleaching resulted in decreased surface warming of coral tissue. Action spectra of coral tissue heating showed elevated efficiency of heating at wavelengths corresponding to absorption maxima of major zooxanthellae photopigments. Generally, energy-rich radiation (, 500 nm) showed the highest heating efficiency. Speciesspecific relationships between coral tissue heating and absorptance can be strongly affected by differences in the thermal properties of the skeleton and/or tissue arrangement within the skeletal matrix, indicating a yet unresolved potential for coral shape, size, and tissue thickness to affect heat dissipation and especially the conduction of heat into the coral skeleton.
Seymour, J.R., Doblin, M.A., Jeffries, T.C., Brown, M.V., Newton, K., Ralph, P.J., Baird, M.E. & Mitchell, J.G. 2012, 'Contrasting microbial assemblages in adjacent water masses associated with the East Australian Current', Environmental Microbiology Reports, vol. 4, pp. 548-555.
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Different oceanographic provinces host discrete microbial assemblages that are adapted to local physicochemical conditions. We sequenced and compared the metagenomes of two microbial communities inhabiting adjacent water masses in the Tasman Sea, where the recent strengthening of the East Australian Current (EAC) has altered the ecology of coastal environments. Despite the comparable latitude of the samples, significant phylogenetic differences were apparent, including shifts in the relative frequency of matches to Cyanobacteria, Crenarchaeota and Euryarchaeota. Fine-scale variability in the structure of SAR11, Prochlorococcus and Synechococcus populations, with more matches to `warm-water+ ecotypes observed in the EAC, indicates the EAC may drive an intrusion of tropical microbes into temperate regions of the Tasman Sea. Furthermore, significant shifts in the relative importance of 17 metabolic categories indicate that the EAC prokaryotic community has different physiological properties than surrounding waters
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.
Verhoeven, M.P., Kelaher, B.P., Bishop, M.J. & Ralph, P.J. 2012, 'Epiphyte Grazing Enhances Productivity Of Remnant Seagrass Patches', Austral Ecology, vol. 37, no. 8, pp. 885-892.
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Anthropogenic nutrient enrichment is increasingly modifying community structure and ecosystem functioning in terrestrial and aquatic ecosystems. In marine ecosystems, the paradigm is that nutrient enrichment leads to a decline of seagrasses by stimulatin
McMinn, A., Ashworth, C., Bhagooli, R., Martin, A., Salleh, S., Ralph, P.J. & Ryan, K.G. 2012, 'Antarctic Coastal Microalgal Primary Production And Photosynthesis', Marine Biology, vol. 159, no. 12, pp. 2827-2837.
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Primary production in coastal Antarctica is primarily contributed from three sources: sea ice algae, phytoplankton, and microphytobenthos. Compared to other eastern Antarctic sites, the sea ice microalgal biomass at Casey Station, in spring 2005 was rela
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.
Petrou, K., Doblin, M.A. & Ralph, P.J. 2011, 'Heterogeneity in the photoprotective capacity of three Antarctic diatoms during short-term changes in salinity and temperature', Marine Biology, vol. 158, no. 5, pp. 1029-1041.
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The Antarctic marine ecosystem changes seasonally, forming a temporal continuum of specialised niche habitats including open ocean, sea ice and meltwater environments. The ability for phytoplankton to acclimate rapidly to the changed conditions of these environments depends on the species++ physiology and photosynthetic plasticity and may ultimately determine their long-term ecological niche adaptation. This study investigated the photophysiological plasticity and rapid acclimation response of three Antarctic diatoms++Fragilariopsis cylindrus, Pseudo-nitzschia subcurvata and Chaetoceros sp.++to a selected range of temperatures and salinities representative of the sea ice, meltwater and pelagic habitats in the Antarctic. Fragilariopsis cylindrus displayed physiological traits typical of adaptation to the sea ice environment. Equally, this species showed photosynthetic plasticity, acclimating to the range of environmental conditions, explaining the prevalence of this species in all Antarctic habitats. Pseudo-nitzschia subcurvata displayed a preference for the meltwater environment, but unlike F. cylindrus, photoprotective capacity was low and regulated via changes in PSII antenna size. Chaetoceros sp. had high plasticity in non-photochemical quenching, suggesting adaptation to variable light conditions experienced in the wind-mixed pelagic environment. While only capturing short-term responses, this study highlights the diversity in photoprotective capacity that exists amongst three dominant Antarctic diatom species and provides insight into links between ecological niche adaptation and species++ distribution
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.
Behrendt, L., Larkum, A., Norman, A., Qvortrup, K., Chen, M., Ralph, P.J., Sorensen, S.J., Trampe, E. & Kuhl, M. 2011, 'Endolithic chlorophyll d-containing phototrophs', ISME Journal, vol. 5, no. 6, pp. 1072-1076.
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Cyanobacteria in the genus Acaryochloris are the only known oxyphototrophs that have exchanged chlorophyll a (Chl a) with Chl d as their primary photopigment, facilitating oxygenic photosynthesis with near infrared (NIR) light. Yet their ecology and natural habitats are largely unknown. We used hyperspectral and variable chlorophyll fluorescence imaging, scanning electron microscopy, photopigment analysis and DNA sequencing to show that Acaryochloris-like cyanobacteria thrive underneath crustose coralline algae in a widespread endolithic habitat on coral reefs. This finding suggests an important role of Chl d-containing cyanobacteria in a range of hitherto unexplored endolithic habitats, where NIR light-driven oxygenic photosynthesis may be significant.
Ulstrup, K., Kuhl, M., van Oppen, M.J., Cooper, T.F. & Ralph, P.J. 2011, 'Variation in photosynthesis and respiration in geographically distinct populations of two reef-building coral species', Aquatic Biology, vol. 12, pp. 241-248.
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Studies of the regulation and importance of physiological processes such as coral photosynthesis and respiration on coral reefs require knowledge of spatio-temporal patterns of variability at different scales. Oxygen microelectrodes were used to measure photosynthesis and dark respiration of 2 corals, Pocillopora damicornis and Turbinaria reniformis, in the northern (Lizard Island) and central (Davies and Broadhurst Reefs) regions of the Great Barrier Reef (GBR) in winter and summer. Genetic characterisation of Symbiodinium revealed that P. damicornis hosted a single symbiont type (Symbiodinium C1) in both regions, whereas T. reniformis harboured 2 types, dependent on location. Colonies at Lizard Island harboured Symbiodinium D, whereas colonies at Davies Reef harboured Symbiodinium C2. Rates of gross photosynthesis were greater in the central than in the northern GBR in summer. A similar pattern was detected for dark respiration rates in T. reniformis. No seasonal change in either photosynthesis or dark respiration was evident in the northern GBR, possibly due to less annual variability in light conditions, and for T. reniformis, additionally the presence of Symbiodinium D. These results highlight that environmental conditions coupled with regional-scale distribution of Symbiodinium are likely to exert important influences on respiration and photosynthetic performance of reef-building corals.
Petrou, K. & Ralph, P.J. 2011, 'Photosynthesis and net primary productivity in three Antarctic diatoms: possible significance for their distribution in the Antarctic marine ecosystem', Marine Ecology Progress Series, vol. 437, pp. 27-40.
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Photosynthesis and net primary productivity were measured in 3 Antarctic diatoms, Fragilariopsis cylindrus, Pseudo-nitzschia subcurvata and Chaetoceros sp., exposed to rapid changes in temperature and salinity representing a range of conditions found during a seasonal cycle. Measured differences in fluorescence-derived photosynthetic activity and oxygen evolution suggested that some alternative electron cycling activity was present under high irradiances. F. cylindrus displayed the highest rates of relative electron transport and net primary productivity under all salinity and temperature combinations and showed adaptive traits towards the sea-ice-like environment. P. subcurvata displayed a preference for low saline conditions where production rates were greatest. However, there was evidence of photosynthetic sensitivity to the lowest temperatures and highest salinities, suggesting a lack of adaptation for dealing with sea-ice-like conditions. Chaetoceros sp. showed high plasticity, acclimating well to all conditions but performing best under pelagic conditions. The study shows species-specific sensitivities to environmental change, highlighting photosynthetic capacity as a potentially important mechanism in ecological niche adaptation. When these data were modelled over different seasons, integrated daily net primary production was greatest under summer pelagic conditions. The findings from this study support the general observations of light control and seasonal development of net primary productivity and species succession in the Antarctic marine ecosystem.
Doblin, M.A., Petrou, K., Shelly, K., Westwood, K., van den Enden, R., Wright, S., Griffiths, B. & Ralph, P.J. 2011, 'Diel variation of chlorophyll-a fluorescence, phytoplankton pigments and productivity in the Sub-Antarctic and Polar Front Zones south of Tasmania, Australia', Deep Sea Research Part II: Topical Studies in Oceanography, vol. 58, no. 21-22, pp. 2189-2199.
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Marine primary production is a fundamental measure of the ocean++s capacity to convert carbon dioxide to particulate organic carbon for the marine foodweb, and as such is an essential variable used in ecosystem and biogeochemical models to assess trophic dynamics and carbon cycling. The Sub-Antarctic Zone (SAZ) is a major sink for atmospheric carbon and exhibits large gradients in ocean conditions on both temporal and spatial scales. In this dynamic system, an understanding of small-scale temporal changes is critical for modelling primary production at larger scales. Thus, we investigated diel effects on maximum quantum yield of PSII (FV/FM), photosynthetic pigment pools and primary productivity in the western (Diel 1) and eastern SAZ region (Diel 3) south of Tasmania, Australia, and compared this to a station at the polar front (Diel 2). Phytoplankton in the eastern SAZ had the greatest diel response, with cells showing decreased FV/FM and increased biosynthesis and transformation of xanthophyll and other photoprotective pigments during the day, but only in the surface waters (0 and 10m). Diel responses diminished by 30 m. Cells in the western SAZ had similar responses across the depths sampled, increasing their FV/FM during the night and increasing their xanthophyll pigment content during the day. Phytoplankton at the polar front (Diel 2) showed intermediate diel-related variations in photophysiology, with xanthophyll conversion and increases in photoprotective pigments during the day but constant FV/FM.
Earp, A.A., Hanson, C.E., Ralph, P.J., Brando, V.E., Allen, S., Baird, M.E., Clementson, L., Daniel, P., Dekker, A.G., Fearns, P.R., Parslow, J.S., Strutton, P.G., Thompson, P.A., Underwood, M., Weeks, S. & Doblin, M.A. 2011, 'Review of fluorescent standards for calibration of in situ fluorometers: Recommendations applied in coastal and ocean observing programs', Optics Express, vol. 19, no. 27, pp. 26768-26782.
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Fluorometers are widely used in ecosystem observing to monitor fluorescence signals from organic compounds, as well as to infer geophysical parameters such as chlorophyll or CDOM concentration, but measurements are susceptible to variation caused by biofouling, instrument design, sensor drift, operating environment, and calibration rigor. To collect high quality data, such sensors need frequent checking and regular calibration. In this study, a wide variety of both liquid and solid fluorescent materials were trialed to assess their suitability as reference standards for performance assessment of in situ fluorometers. Criteria used to evaluate the standards included the spectral excitation/emission responses of the materials relative to fluorescence sensors and to targeted ocean properties, the linearity of the fluorometer++s optical response with increasing concentration, stability and consistency, availability and ease of use, as well as cost. Findings are summarized as a series of recommended reference standards for sensors deployed on stationary and mobile platforms, to suit a variety of in situ coastal to ocean sensor configurations. Repeated determinations of chlorophyll scale factor using the recommended liquid standard, Fluorescein, achieved an accuracy of 2.5%. Repeated measurements with the recommended solid standard, Plexiglas Satinice plum 4H01 DC (polymethylmethacrylate), over an 18 day period varied from the mean value by 1.0% for chlorophyll sensors and 3.3% for CDOM sensors.
Petrou, K., Hassler, C.S., Doblin, M.A., Shelly, K., Schoemann, V., van den Enden, R., Wright, S. & Ralph, P.J. 2011, 'Iron-limitation and high light stress on phytoplankton populations from the Australian Sub-Antarctic Zone (SAZ)', Deep Sea Research Part II: Topical Studies in Oceanography, vol. 58, no. 21-22, pp. 2200-2211.
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The high nutrient low chlorophyll (HNLC) surface waters of the Southern Ocean are characterised by high concentrations of nitrate and phosphate, low concentrations of dissolved iron and deep vertical mixing. Future climate scenarios predict increased sur
Jimenez Denness, I.M., Kuhl, M., Larkum, A. & Ralph, P.J. 2011, 'Effects of flow and colony morphology on the thermal boundary layer of corals', Journal of the Royal Society Interface, vol. 8, no. 65, pp. 1785-1795.
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The thermal microenvironment of corals and the thermal effects of changing flow and radiation are critical to understanding heat-induced coral bleaching, a stress response resulting from the destruction of the symbiosis between corals and their photosynt
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.
Lilley, R., Ralph, P.J. & Larkum, A. 2010, 'The determination of activity of the enzyme Rubisco in cell extracts of the dinoflagellate alga Symbiodinium sp. by manganese chemiluminescence and its response to short-term thermal stress of the alga', Plant Cell and Environment, vol. 33, no. 6, pp. 995-1004.
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The dinoflagellate alga Symbiodinium sp., living in symbiosis with corals, clams and other invertebrates, is a primary producer in coral reefs and other marine ecosystems. The function of the carbon-fixing enzyme ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) in dinoflagellates is difficult to study because its activity is rapidly lost after extraction from the cell. We report procedures for the extraction of Rubisco from Symbiodinium cells and for stable storage. We describe a continuous assay for Rubisco activity in these crude cell extracts using the Mn2+ chemiluminescence of Rubisco oxygenase. Chemiluminescence time courses exhibited initial transients resembling bacterial Form II Rubisco, followed by several minutes of linearly decreasing activity. The initial activity was determined from extrapolation of this linear section of the time course. The activity of fast-frozen cell extracts was stable at -80 C and, after thawing and storage on ice, remained stable for up to 1 h before declining non-linearly. Crude cell extracts bound [14C] 2-carboxy-D-arabitinol 1,5-bisphosphate to a high molecular mass fraction separable by gel filtration chromatography. After pre-treatment of Symbiodinium cell cultures in darkness at temperatures above 30 C, the extracted Rubisco activities decreased, with almost complete loss of activity above 36 C. The implications for the sensitivity to elevated temperature of Symbiodinium photosynthesis are assessed.
Herrera-Silveira, J.A., Cebrian, J., Hauxwell, J., Ramirez-Ramirez, J. & Ralph, P.J. 2010, 'Evidence of negative impacts of ecological tourism on turtlegrass (Thalassia testudinum) beds in a marine protected area of the Mexican Caribbean', Aquatic Ecology, vol. 44, no. 1, pp. 23-31.
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Many marine protected areas (MPAs) have been established in recent years. Some MPAs are open to tourists to foster environmental education and generate revenue for the MPA. This has been coined ++ecological tourism+ . Here, we examine the impact of ecological tourism on turtlegrass (Thalassia testudinum) health in one area of the ++Costa Occidental de Isla Mujeres, Punta Canc+n y Punta Nizuc+ MPA in the Mexican Caribbean. A heavily visited location was compared with an unvisited location. Turtlegrass leaves at the visited location were sparser, shorter, grew more slowly, and had more epiphytes than at the unvisited location. Vertical and horizontal rhizomes of turtlegrass also grew more slowly at the visited than at the unvisited location. There is reasonable evidence to suggest that the observed differences are likely due to the deleterious impacts of novice and careless snorkelers. If continuing, these impacts could cause severe degradation of the visited areas in this MPA and, thus, changes in management policies seem in order.
Csaszar, N., Ralph, P.J., Frankham, R., Berkelmans, R. & van Oppen, M.J. 2010, 'Estimating the Potential for Adaptation of Corals to Climate Warming', PLoS ONE, vol. 5, no. 3, pp. 1-8.
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The persistence of tropical coral reefs is threatened by rapidly increasing climate warming, causing a functional breakdown of the obligate symbiosis between corals and their algal photosymbionts (Symbiodinium) through a process known as coral bleaching. Yet the potential of the coral-algal symbiosis to genetically adapt in an evolutionary sense to warming oceans is unknown. Using a quantitative genetics approach, we estimated the proportion of the variance in thermal tolerance traits that has a genetics basis (i.e. heritability) as a proxy for their adaptive potential in the widespread Indo-Pacific reef-building coral Acropora millepora. We chose two physiologically different populations that associate respectively with one thermotolerant (Symbiodinium clade D) and one less tolerant symbiont type (Symbiodinium C2). In both symbiont types, pulse amplitude modulated (PAM) fluorometry and high performance liquid chromatography (HPLC) analysis revealed significant heritabilities for traits related to both photosynthesis and photoprotective pigment profile. However, quantitative real-time polymerase chain reaction (qRT - PCR) assays showed a lack of heritability in both coral host populations for their own expression of fundamental stress genes. Coral colony growth, contributed to by both symbiotic partners, displayed heritability. High heritabilities for functional key traits of algal symbionts, along with their short clonal generation time and high population sizes allow for their rapid thermal adaptation. However, the low overall heritability of coral host traits, along with the corals' long generation time, raise concern about the timely adaptation of the coral-algal symbiosis in the face of continued rapid climate warming.
McMinn, A., Pankowskii, A., Ashworth, C., Bhagooli, R., Ralph, P.J. & Ryan, K. 2010, 'In situ net primary productivity and photosynthesis of Antarctic sea ice algal, phytoplankton and benthic algal communities', Marine Biology, vol. 157, no. 6, pp. 1345-1356.
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Primary production at Antarctic coastal sites is contributed from sea ice algae, phytoplankton and benthic algae. Oxygen microelectrodes were used to estimate sea ice and benthic primary production at several sites around Casey, a coastal area in eastern Antarctica. Maximum oxygen export from sea ice was 0.95 mmol O2 m-2 h-1 (*11.7 mg C m-2 h-1) while from the sediment it was 6.08 mmol O2 m-2 h-1 (*70.8 mg C m-2 h-1). When the ice was present O2 export from the benthos was either low or negative. Sea ice algae assimilation rates were up to 3.77 mg C (mg Chl-a)-1 h-1 while those from the benthos were up to 1.53 mg C (mg Chl-a)-1 h-1. The contribution of the major components of primary productivity was assessed using fluorometric techniques. When the ice was present approximately 55++65% of total daily primary production occurred in the sea ice with the remainder unequally partitioned between the sediment and the water column. When the ice was absent, the benthos contributed nearly 90% of the primary production.
Wright, J.T., Byers, J.E., Koukoumaftsis, L., Ralph, P.J. & Gribben, P.E. 2010, 'Native species behaviour mitigates the impact of habitat-forming invasive seaweed', Oecologia, vol. 163, no. 2, pp. 527-534.
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Habitat-forming invasive species cause large, novel changes to the abiotic environment. These changes may elicit important behavioural responses in native fauna, yet little is known about mechanisms driving this behaviour and how such trait-mediated responses influence the fitness of native species. Low dissolved oxygen is a key abiotic change created by the habitat-forming invasive seaweed, Caulerpa taxifolia, which influences an important behavioural response (burrowing depth) in the native infaunal bivalve Anadara trapezia. In Caulerpa-colonised areas, Anadara often emerged completely from the sediment, and we experimentally demonstrate that water column hypoxia beneath the Caulerpa canopy is the mechanism instigating this +pop-up+ behaviour. Importantly, pop-up in Caulerpa allowed similar survivorship to that in unvegetated sediment; however, when we prevented Anadara from popping-up, they suffered >50% mortality in just 1 month. Our findings not only highlight the substantial environmental alteration by Caulerpa, but also an important role for the behaviour of native species in mitigating the effects of habitat-forming invasive species.
Seery, C.R. & Ralph, P.J. 2010, 'Ecological relevance of a chlorophyll a fluorescence ecotoxicological endpoint', Toxicological and Environmental Chemistry, vol. 92, no. 8, pp. 1529-1540.
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With the increasing use of new techniques to assess toxic stress and the effects of pollution, it is important to ensure that any ++++new++++ endpoint employed is able to demonstrate a level of eco-relevance. Though recent application of chlorophyll a fluorescence parameters to macroalgal bioassays has been successful, a level of eco-relevance for such use has not been experimentally shown. As such, this article presents a series of experiments designed to establish a link between fluorescence parameters and higher-level effects (supra-individual level). The results show that fluorescence parameters are capable of predicting germination success of macroalgal gametes and can do so much sooner than the actual event of germination. Furthermore, a decline in DF=F0m is shown to be strongly associated with a reduced germination success. Thus, a level of eco-relevance has been established for the fluorescence endpoint that is at least equal to that of the widely accepted germination-based macroalgal bioassays.
Buxton, L.J., Badger, M. & Ralph, P.J. 2009, 'Effects Of Moderate Heat Stress And Dissolved Inorganic Carbon Concentration On Photosynthesis And Respiration Of Symbiodinium Sp (Dinophyceae) In Culture And In Symbiosis', Journal of Phycology, vol. 45, no. 2, pp. 357-365.
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The influence of temperature and inorganic carbon (C-i) concentration on photosynthesis was examined in whole corals and samples of cultured symbiotic dinoflagellates (Symbiodinium sp.) using combined measurements from a membrane inlet mass spectrometer and chl a fluorometer. In whole corals, O-2 production at 26 degrees C was significantly limited at C-i concentrations below ambient seawater (similar to 2.2 mM). Further additions of C-i up to similar to 10 mM caused no further stimulation of oxygenic photosynthesis. Following exposure to 30 degrees C (2 d), net oxygen production decreased significantly in whole corals, as a result of reduced production of photosynthetically derived oxygen rather than increased host consumption. Whole corals maintained a rate of oxygen evolution around eight times lower than cultured Symbiodinium sp. at inorganic carbon concentrations < 2 mM, but cultures displayed greater levels of photoinhibition following heat treatment (30 degrees C, 2 d). Whole corals and cultured zooxanthellae differed considerably in their responses to C-i concentration and moderate heat stress, demonstrating that cultured Symbiodinium make an incongruous model for those in hospite. Reduced net oxygen evolution, in whole corals, under conditions of low C-i (< 2 mM) has been interpreted in terms of possible sink limitation leading to increased nonphotochemical energy dissipation. The advantages of combined measurement of net gas exchange and fluorometry offered by this method are discussed.
Collier, C., Lavery, P., Ralph, P.J. & Masini, R. 2009, 'Shade-induced response and recovery of the seagrass Posidonia sinuosa', Journal Of Experimental Marine Biology And Ecology, vol. 370, no. 1-2, pp. 89-103.
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The effect of shading on the seagrass Posidonia sinuosa Cambridge et Kuo was investigated to identify mechanisms that prolong its survival during periods of low light and permit its subsequent recovery. We also tested whether the responses were consistent in plants growing at different depths. Shade treatments were low (LS; 70 - 100% of ambient Photosynthetic Photon Flux Density), medium (MS; 12 - 39%) and heavy (HS; 5 - 4%) at the shallow (3 - 4 m) site, whilst the deep (7 - 8 m) site had no HS treatment. HS at the shallow and MS at the deep site were below minimum light requirements (MLR) for the long-term survival of P. sinuoso.
Strom, D., Ralph, P.J. & Stauber, J.L. 2009, 'Development of a Toxicity Identification Evaluation Protocol Using Chlorophyll-a Fluorescence in a Marine Microalga', Archives Of Environmental Contamination And Toxic..., vol. 56, no. 1, pp. 30-38.
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Growth inhibition bioassays with the microalga Nitzschia closterium have recently been applied in marine Toxicity Identification Evaluation (TIE) testing. However, the 48-h test duration can result in substantial loss of toxicants over time, which might lead to an underestimation of the sample toxicity. Although shorter-term microalgal bioassays can minimize such losses, there are few bioassays available and none are adapted for marine TIE testing. The acute (5-min) chlorophyll-a fluorescence bioassay is one alternative; however, this bioassay was developed for detecting herbicides in freshwater aquatic systems and its suitability for marine TIE testing was not known. In this study, a chlorophyll-a fluorescence bioassay using the marine microalga Isochrysis galbana was able to detect contaminants other than herbicides at environmentally relevant concentrations and tolerated the physical and chemical manipulations needed for a Phase I TIE. Phase I TIE procedures were successfully developed using this chlorophyll-a fluorescence bioassay and used to identify all classes of contaminants present in a synthetic mixture of known chemical composition. In addition, TIEs with both the acute fluorescence bioassay and the standard growth inhibition bioassay identified the same classes of toxicants in a sample of an unknown complex effluent. Even though the acute chlorophyll-a fluorescence end point was less sensitive than the chronic cell division end point, TIEs with the chlorophyll-a fluorescence bioassay provided a rapid and attractive alternative to longer-duration bioassays.
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.
Baird, A.H., Bhagooli, R., Ralph, P.J. & Takahashi, S. 2009, 'Coral bleaching: the role of the host', Trends In Ecology & Evolution, vol. 24, no. 1, pp. 16-20.
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Coral bleaching caused by global warming is one of the major threats to coral reefs. Very recently, research has focused on the possibility of corals switching symbionts as a means of adjusting to accelerating increases in sea surface temperature. Although symbionts are clearly of fundamental importance, many aspects of coral bleaching cannot be readily explained by differences in symbionts among coral species. Here we outline several potential mechanisms by which the host might influence the bleaching response, and conclude that predicting the fate of corals in response to climate change requires both members of the symbiosis to be considered equally.
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.
Kuhl, M., Holst, G., Larkum, A. & Ralph, P.J. 2008, 'Imaging of oxygen dynamics within the endolithic algal community of the massive coral porites lobata', Journal of Phycology, vol. 44, no. 3, pp. 541-550.
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We used transparent planar oxygen optodes and a luminescence lifetime imaging system to map (at a pixel resolution of <200 ?m) the two-dimensional distribution of O<sub>2</sub> within the skeleton of a Porites lobata colony. The O<sub>2</sub> distribution was closely correlated to the distribution of the predominant endolithic microalga, Ostreobium quekettii Bornet et Flahault that formed a distinct green band inside the skeleton. Oxygen production followed the outline of the Ostreobium band, and photosynthetic O<sub>2</sub> production was detected at only 0.2 ?mol photons m<sup>-2</sup> s<sup>-1</sup>, while saturation occurred at ?37 ?mol photons m<sup>-2</sup> s<sup>-1</sup>. Oxygen levels varied from ?60% to 0% air saturation in the illuminated section of the coral skeleton in comparison to the darkened section. The O<sub>2</sub> production within the Ostreobium band was lower in the region below the upward facing surface of the coral and elevated on the sides. Oxygen consumption in darkness was also greatest within the Ostreobium zone, as well as in the white skeleton zone immediately below the corallites. The rate of O<sub>2</sub> depletion was not constant within zones and between zones, showing pronounced heterogeneity in endolithic respiration. When the coral was placed in darkness after a period of illumination, O<sub>2</sub> levels declined by 50% within 20 min and approached steady-state after 40+50 min in darkness. Our study demonstrates the use of an important new tool in endolith photobiology and presents the first data of spatially resolved O<sub>2</sub> concentration and its correlation to the physical structures and specific zones responsible for O<sub>2</sub> production and consumption within the coral skeleton.
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.
Roff, G., Ulstrup, K.E., Fine, M., Ralph, P.J. & Hoegh-Guldberg, O. 2008, 'Spatial heterogeneity of photosynthetic activity within diseased corals from the great barrier reef', Journal Of Phycology, vol. 44, no. 2, pp. 526-538.
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Morphological diagnosis and descriptions of seven disease-like syndromes affecting scleractinian corals were characterized from the southern Great Barrier Reef (GBR). Chl a fluorescence of PSII was measured using an Imaging-PAM (pulse amplitude modulated
Jimenez Denness, I.M., Kuhl, M., Larkum, A. & Ralph, P.J. 2008, 'Heat budget and thermal microenvironment of shallow-water corals: Do massive corals get warmer than branching corals?', Limnology And Oceanography, vol. 53, no. 4, pp. 1548-1561.
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Coral surface temperature was investigated with multiple temperature sensors mounted on hemispherical and branching corals under (a) artificial lighting and controlled flow; (b) natural sunlight and controlled flow; and (c) in situ conditions in a shallo
Petrou, K., Doblin, M.A., Smith, R.A., Ralph, P.J., Shelly, K. & Beardall, J. 2008, 'State transitions and nonphotochemical quenching during a nutrient-induced fluorescence transient in phosphorus-starved Dunaliella tertiolecta', Journal of Phycology, vol. 44, pp. 1204-1211.
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Assessments of nutrient-limitation in microalgae using chl a fluorescence have revealed that nitrogen and phosphorus depletion can be detected as a change in chl a fluorescence signal when nutrient-starved algae are resupplied with the limiting nutrient.
Collier, C., Lavery, P., Ralph, P.J. & Masini, R. 2008, 'Physiological characteristics of the seagrass Posidonia sinuosa along a depth-related gradient of light availability', Marine Ecology-Progress Series, vol. 353, pp. 65-79.
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Physiological plasticity has the capacity to prolong seagrass survival under reduced light conditions. However, when light is attenuated across a depth gradient, the relative importance of this over other mechanisms for tolerating long-term light reducti
Bishop, M.J., Kelaher, B.P., Alquezar, R., York, P.H., Ralph, P.J. & Skilbeck, C.G. 2007, 'Trophic cul-de-sac, Pyrazus ebeninus, limits trophic transfer through an estuarine detritus-based food web', OIKOS, vol. 116, no. 3, pp. 427-438.
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The importance to food-webs of trophic cul-de-sacs, species that channel energy flow away from higher trophic levels, is seldom considered outside of the pelagic systems in which they were first identified. On intertidal mudflats, inputs of detritus from saltmarshes, macroalgae or microphytobenthos are generally regarded as a major structuring force underpinning food-webs and there has been no consideration of trophic cul-de-sacs to date. A fully orthogonal three-factor experiment manipulating the density of the abundant gastropod, Pyrazus ebeninus, detritus and macrobenthic predators on a Sydney mudflat revealed large deleterious effects of the gastropod, irrespective of detrital loading or the presence of predators. Two months after experimental manipulation, the standing-stock of microphytobenthos in plots with high (44 per m(2)) densities of P. ebeninus was 20% less than in plots with low (4 per m(2)) densities. Increasing densities of P. ebeninus from low to high halved the abundance of macroinvertebrates and the average number of species. In contrast, the addition of detritus had differing effects on microphytobenthos (positively affected) and macroinvertebrates (negatively affected). Over the two-months of our experiment, no predatory mortality of P. ebeninus was observed and high densities of P. ebeninus decreased impacts of predators on macroinvertebrate abundances. Given that the dynamics of southeast Australian mudflats are driven more by disturbance than seasonality in predators and their interactions with prey, it is likely that Pyrazus would be similarly resistant to predation and have negative effects on benthic assemblages at other times of the year, outside of our study period. Thus, in reducing microphytobenthos and the abundance and species richness of macrofauna, high abundances of the detritivore P. ebeninus may severely limit the flow of energy up the food chain to commercially-important species.
Collier, C., Lavery, P., Masini, R. & Ralph, P.J. 2007, 'Morphological, growth and meadow characteristics of the seagrass Posidonia sinuosa along a depth-related gradient of light availability', Marine Ecology: Progress Series, vol. 337, pp. 103-115.
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Morphological and growth characteristics of the meadow-forming seagrass Posidonia sinuosa (Cambridge et Kuo), were measured along a depth-related gradient of light to infer its response to long-term differences in light availability. Morphometric measurements were carried out at 6 depths between 1.6 and 9.0 m in summer and winter at Cockburn Sound and summer only at Warnbro Sound in south-western Australia. The minimum light requirement for P. sinuosa of 8.5% sub-surface light was among the lower range reported for seagrasses. Its slow growth rate (0.5?1.5 mgdry shoot?1 d?1), relative to similarly sized species, may contribute to the low light requirements of this species. Shoot density, leaf area index and biomass showed pronounced and consistent differences among depths (up to 88-fold reduction of above-ground biomass from shallow to deep sites). At the deeper sites, the reduced shoot density probably reduces respiratory demand and alleviates self-shading. Morphological differences (leaf length, width and thickness and number of leaves per shoot) did not follow a clear and consistent trend with depth. Despite a 70% reduction in light availability at the canopy level between the shallowest and deepest sites, leaf growth rate was unaffected by depth during summer, and in winter differed between only a few depths. We propose that the reduction in shoot density partially alleviates the effects of self-shading and permits comparable leaf growth rates across the depth range. These results suggest that for interpreting long-term responses to light availability, shoot density is the most sensitive of the morphological characteristics measured here.
Ryan, K.G., Hegseth, E.N., Martin, A., Davy, S.K., O'Toole, R., Ralph, P.J., McMinn, A. & Thorn, C.J. 2007, 'Comparison of the microalgal community within fast ice at two sites along the Ross Sea coast, Antarctica', Antarctic Science, vol. 18, no. 4, pp. 583-594.
Ralph, P.J., Durako, M.J., Enriquez, S., Collier, C. & Doblin, M.A. 2007, 'Impact of light limitation on seagrasses', Journal of Experimental Marine Biology and Ecology, vol. 350, no. 1-2, pp. 176-193.
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Seagrass distribution is controlled by light availability, especially at the deepest edge of the meadow. Light attenuation due to both natural and anthropogenically-driven processes leads to reduced photosynthesis. Adaptation allows seagrasses to exist under these sub-optimal conditions. Understanding the minimum quantum requirements for growth (MQR) is revealed when light conditions are insufficient to maintain a positive carbon balance, leading to a decline in seagrass growth and distribution. Respiratory demands of photosynthetic and non-photosynthetic tissues strongly influence the carbon balance, as do resource allocations between above- and below-ground biomass. Seagrass light acclimation occurs on varying temporal scales, as well as across spatial scales, from the position along a single leaf blade to within the canopy and finally across the meadow. Leaf absorptance is regulated by factors such as pigment content, morphology and physical properties. Chlorophyll content and morphological characteristics of leaves such as leaf thickness change at the deepest edge. We present a series of conceptual models describing the factors driving the light climate and seagrass responses under current and future conditions, with special attention on the deepest edge of the meadow.
McMinn, A., Ryan, K.G., Ralph, P.J. & pankowski, a. 2007, 'Spring sea ice photosynthesis, primary productivity and biomass distribution in eastern Antarctica, 2002-2004', Marine Biology, vol. 151, no. 3, pp. 985-995.
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While it is known that Antarctic sea ice biomass and productivity are highly variable over small spatial and temporal scales, there have been very few measurements from eastern Antarctic. Here we attempt to quantify the biomass and productivity and relat
Ralph, P.J., Smith, R.A., Macinnis-Ng, C.M. & Seery, C.R. 2007, 'Use of fluorescence-based ecotoxicological bioassays in monitoring toxicants and pollution in aquatic systems: Review', Toxicological and Environmental Chemistry, vol. 89, no. 4, pp. 631-649.
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Chlorophyll a fluorescence has the potential to become a valuable ecotoxicological endpoint, which could be used with a range of aquatic phototrophs. Chlorophyll a fluorescence bioassays have been applied in the assessment of heavy metals, herbicides, petrochemicals and nutrients. The strengths of this endpoint are that it is rapid, non-invasive and non-destructive, while the major weakness is the lack of clear ecological relevance. We provide an overview of chlorophyll a fluorescence applications in ecotoxicology. We reviewed test conditions, parameters and protocols used to date and found standardised protocols to be lacking. The most favoured fluorescence parameters were maximum quantum yield (Fv/Fm) and effective quantum yield (?PSII); microalgae were the most widely used tested organism, herbicides the most commonly tested toxicant, while most studies lacked a summary statistic (such as EC50). We recommend that future research in aquatic chlorophyll a fluorescence ecotoxicology focus on standardisation of test protocols and statistical techniques.
Ralph, P.J., Ryan, K.G., Martin, A.J. & Fenton, G. 2007, 'Melting out of sea ice causes greater photosynthetic stress in algae than freezing in', Journal Of Phycology, vol. 43, no. 5, pp. 948-956.
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Sea ice is the dominant feature of polar oceans and contains significant quantities of microalgae. When sea ice forms and melts, the microalgal cells within the ice matrix are exposed to altered salinity and irradiance conditions, and subsequently, their
Ralph, P.J., Larkum, A. & Kuhl, M. 2007, 'Photobiology of endolithic microorganisms in living coral skeletons: 1. Pigmentation, spectral reflectance and variable chlorophyll fluorescence analysis of endoliths in the massive corals Cyphastrea serailia, Porites lutea and Goniastrea australensi', Marine Biology, vol. 152, no. 2, pp. 395-404.
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We used microscopy, reflectance spectroscopy, pigment analysis, and photosynthesis-irradiance curves measured with variable fluorescence techniques to characterise the endolithic communities of phototrophic microorganisms in the skeleton of three massive
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.
Ulstrup, K.E., Ralph, P.J., van Oppen, M.J. & Kuhl, M. 2007, 'Inter-polyp genetic and physiological characterisation of Symbiodinium in an Acropora valida colony', Marine Biology: international journal on life in oceans and coastal waters, vol. 153, no. 2, pp. 225-234.
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Corals harbouring genetically mixed communities of endosymbiotic algae (Symbiodinium) often show distribution patterns in accordance with differences in light climate across an individual colony. However, the physiology of these genetically characterised communities is not well understood. Single stranded conformation polymorphism (SSCP) and real time quantitative polymerase chain reaction (qPCR) analyses were used to examine the genetic diversity of the Symbiodinium community in hospite across an individual colony of Acropora valida at the spatial scale of single polyps. The physiological characteristics of the polyps were examined prior to sampling with a combined O2 microelectrode with a fibre-optic microprobe (combined sensor diameter 50-100 ++m) enabling simultaneous measurements of O2 concentration, gross photosynthesis rate and photosystem II (PSII) quantum yield at the coral surface as a function of increasing irradiances. Both sun- and shade-adapted polyps were found to harbour either Symbiodinium clade C types alone or clades A and C simultaneously. Polyps were grouped in two categories according to (1) their orientation towardps light, or (2) their symbiont community composition. Physiological differences were not detected between sun- and shade-adapted polyps, but O2 concentration at 1,100 ++mol photons m-2 s-1 was higher in polyps that harboured both clades A and C symbionts than in polyps that harboured clade C only. These results suggest that the acclimatisation of zooxanthellae of individual polyps of an A. valida colony to ambient light levels may not be the only determinant of the photosynthetic capacity of zooxanthellae. Here, we found that photosynthetic capacity is also likely to have a strong genetic basis and differs between genetically distinct Symbiodinium types.
Seery, C.R., Gunthorpe, L. & Ralph, P.J. 2006, 'Herbicide impact on Hormosira banksii gametes measured by fluorescence and germination bioassays', Environmental Pollution, vol. 140, no. 1, pp. 43-51.
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The innovative bioassay described here involves chlorophyll a fluorescence measurements of gametes from the macroalgae, Hormosira banksii, where gametes (eggs) were exposed to Diuron, Irgarol and Bromacil. Response was assessed as percent inhibition from
Charles, A.L., Markich, S.J. & Ralph, P.J. 2006, 'Toxicity of uranium and copper individually, and in combination, to a tropical freshwater macrophyte (Lemna aequinoctialis)', Chemosphere, vol. 62, no. 8, pp. 1224-1233.
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Copper (Cu) and uranium (U) are of potential ecotoxicological concern to tropical freshwater biota in northern Australia, as a result of mining activities. Few data are available on the toxicity of U, and no data are available on the toxic interaction of
Ulstrup, K.E., Ralph, P.J., Larkum, A. & Kuehl, M. 2006, 'Intra-colonial variability in light acclimation of zooxanthellae in coral tissues of Pocillopora damicornis', Marine Biology, vol. 149, no. 6, pp. 1325-1335.
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We investigated heterogeneity of light acclimation of photosynthesis in sun- and shade-adapted coenosarc and polyp tissues of Pocillopora damicornis. The zooxanthellar community within P. damicornis colonies at Heron Island is genetically uniform, yet th
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.
Ulstrup, K.E., Berkelmans, R., Ralph, P.J. & van Oppen, M.J. 2006, 'Variation in bleaching sensitivity of two coral species across a latitudinal gradient on the Great Barrier Reef: the role of zooxanthellae', Marine Ecology Progress Series, vol. 314, pp. 135-148.
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The ability of corals to cope with environmental change, such as increased temperature, relies on the physiological mechanisms of acclimatisation and long-term genetic adaptation. We experimentally examined the bleaching sensitivity exhibited by 2 species of coral, Pocillopora damicornis and Turbinaria reniformis, at 3 locations across a latitudinal gradient of almost 6 degrees on the Great Barrier Reef (GBR), Target bleaching temperature was reached by using a ramping rate of 0.2 degrees C/h. We found that the bleaching sensitivity and recovery of both species differed between corals with clade D symbionts and those with clade C. However, in F damicornis bleaching susceptibility corresponded more strongly with latitude than with zooxanthella type and hence, temperature history, suggesting that local adaptation has occurred. The observed bleaching sensitivity was shown by a decrease in photochemical efficiency (F-v/F-m) in both species of coral. The rate of recovery in T reniformis was highest in explants containing clade D symbionts. The occurrence of clade D in the northern section of the GBR may reflect a long-term response to high sea water temperatures, while the presence of clade D in low abundance in T reniformis at Heralds Prong Reef and Percy Island may be a result of recent bleaching events.
Ryan, K.G., Hegseth, E.N., Martin, A., Davy, S.K., O'Toole, R., Ralph, P.J., McMinn, A. & Thorn, C.J. 2006, 'Comparison of the microalgal community within fast ice two sites along the Ross Sea coast, Antarctia', Antarctic Science, vol. 18, no. 4, pp. 583-594.
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Ulstrup, K.E., Ralph, P.J., Larkum, A. & Kuhl, M. 2006, 'Intra-colonial variability in light acclimation of zooxanthellae in coral tissues of Pocillopora damicornis Received:', Marine Biology, vol. 149, pp. 1325-1335.
Ralph, P.J., McMinn, A., Ryan, K.G. & Ashworth, C. 2005, 'Short-term effect of temperature on the photokinetics of microalgae from the surface layers of Antarctic pack ice', Journal Of Phycology, vol. 41, no. 4, pp. 763-769.
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Microalgae growing within brine channels (85 psu salinity) of the surface ice layers of Antarctic pack ice showed considerable photosynthetic tolerance to the extreme environmental condition. Brine microalgae exposed to temperatures above -5 degrees C an
Macinnis-Ng, C.M., Morrison, D.J. & Ralph, P.J. 2005, 'Temporal and spatial variation in the morphology of the brown macroalga Hormosira banksii (Fucales, Phaeophyta)', Botanica Marina, vol. 48, no. 3, pp. 198-207.
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Hormosira banksii is a morphologically variable macroalgal species from southeastern and southern Australia, which has been previously categorised into ecoforms according to habitat. This study is by far the largest quantitative evaluation of morphologic
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
Ralph, P.J., Larkum, A. & Kuehl, M. 2005, 'Temporal patterns in effective quantum yield of individual zooxanthellae expelled during bleaching', Journal Of Experimental Marine Biology And Ecology, vol. 316, no. 1, pp. 17-28.
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Bleaching is a worldwide phenomenon affecting coral reefs. During elevated temperature and light conditions (bleaching), expelled zooxanthellae show distinct patterns in photosynthetic health. An innovative new device was used to collect individual expel
Ralph, P.J., Schreiber, U., Gademann, R., Kuehl, M. & Larkum, A. 2005, 'Coral photobiology studied with a new imaging pulse amplitude modulated fluorometer', Journal Of Phycology, vol. 41, no. 2, pp. 335-342.
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A new high-resolution imaging fluorometer (Imaging-PAM) was used to identify heterogeneity of photosynthetic activity across the surface of corals. Three species were examined: Acropora nobilis Dana (branching), Goniastrea australiensis Edwards A Haime (
Ralph, P.J., Macinnis-Ng, C.M. & Frankart, C. 2005, 'Fluorescence imaging application: effect of leaf age on seagrass photokinetics', Aquatic Botany, vol. 81, no. 1, pp. 69-84.
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We used the Imaging-PAM fluorometer to map spatial variability of photosynthesis in three seagrass species, Halophila ovalis, Zostera capricorni and Posidonia australis. Photosynthesis was described by relative photosynthetic rate (PS/50), effective quan
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
Ralph, P.J. & Gademann, R. 2005, 'Rapid light curves: A powerful tool to assess photosynthetic activity', Aquatic Botany, vol. 82, no. 3, pp. 222-237.
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Rapid light curves provide detailed information on the saturation characteristics of electron transport, as well as the overall photosynthetic performance of a plant. Rapid light curves were collected from samples of Zostera marina grown under low and hi
Bengtson Nash, S.M., Schreiber, U., Ralph, P.J. & Muller, J.F. 2005, 'The combined SPE: Tox Y-PAM phytotoxicity assay; application and appraisal of a novel Biomonitoring tool for the aquatic environment', Biosensors and Bioelectronics, vol. 20, no. 7, pp. 1443-1451.
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Mounting concerns regarding the environment impact of herbicides has meant a growing requirement for accurate, timely information regarding herbicide residue contamination of, in particular, aquatic systems. Conventional methods of detection remain limited in temrns of practicality due to high costs of oeration and the specialised information that analysis provides. A new phytotoxicity bioassay wa trialled for the detection of herbicide residues in filter-purified (Milli-Q) as sell as antural waters. The performance of the system, which combines solid-phase extraction (SPE) wtih the ToxY-PAM dual-channel yield annalyser (Heinz Walz GmbH), was tested alongside the traditional method of liquid chromatography-mass spectometry (LC-MS). The assay methodology was found to be highly sensitive (LOD 0.1 ngL-1 diuron) with good reproducibility. The study showed that the assay protocol is time effective and can be employed for the aquatic screening of herbicide residues in purified as well as natural waters.
Kuehl, M., Chen, M., Ralph, P.J., Schreiber, U. & Larkum, A. 2005, 'A niche for cyanobacteria containing chlorophyll d', Nature, vol. 433, no. 1, pp. 820-820.
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The cyanobacterium known as Acaryochloris marina is a unique phototroph that uses chlorophyll d as its principal light-harvesting pigment instead of chlorophyll a, the form commonly found in plants, algae and other cyanobacteria; this means that it depends on far-red light for photosynthesis. Here we demonstrate photosynthetic activity in Acaryochloris-like phototrophs that live underneath minute coral-reef invertebrates (didemnid ascidians) in a shaded niche enriched in near-infrared light. This discovery clarifies how these cyanobacteria are able to thrive as free-living organisms in their natural habitat.
Ralph, P.J., Schreiber, U., Gademann, R., Kuhl, M. & Larkum, A. 2005, 'Coral photobiology studied with a new imaging pulse amplitude modulated fluorometer', Journal of Phycology, vol. 41, pp. 335-342.
Macinnis-Ng, C.M. & Ralph, P.J. 2004, 'In situ impact of multiple pulses of metal and herbicide on the seagrass Zostera capricorni', Aquatic Toxicology, vol. 67, pp. 227-237.
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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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Ryan, K.G., Ralph, P.J. & McMinn, A. 2004, 'Acclimation of Antarctic bottom-ice algal communities to lowered salinities during melting', Polar Biology, vol. 27, pp. 679-686.
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Macinnis-Ng, C.M. & Ralph, P.J. 2004, 'Variations in sensitivity to copper and zinc among three isolated populations of the seagrass, Zostera capricorni', Journal of Experimental Marine Biology and Ecology, vol. 302, pp. 63-83.
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Choinski, J.S., Ralph, P.J. & Eamus, D. 2003, 'Changes in photosynthesis during leaf expansion in Corymbia gummifera', Australian Journal Of Botany, vol. 51, no. 1, pp. 111-118.
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Macinnis-Ng, C.M. & Ralph, P.J. 2003, 'In situ impact of petrochemicals on the photosynthesis of the seagrass Zostera capricorni', Marine Pollution Bulletin, vol. 46, no. 11, pp. 1395-1407.
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Macinnis-Ng, C.M. & Ralph, P.J. 2003, 'Short-term response and recovery of Zostera capricorni photosynthesis after herbicide exposure', Aquatic Botany, vol. 76, no. 1, pp. 1-15.
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Hohnberg, D., Ralph, P.J. & Jones, H. 2003, 'Toxicity of the herbicide atrazine at environmental concentrations to Vallisneria Gigantea, assessed using chlorophyll fluorescence', Australasian Journal of Ecotoxicology, vol. 9, pp. 93-100.
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Macinnis-Ng, C.M. & Ralph, P.J. 2002, 'Towards a more ecologically relevant assessment of the impact of heavy metals on the photosynthesis of seagrass, Zostera capricorni', Marine Pollution Bulletin, vol. 45, no. N/A, pp. 100-106.
This in situ study used photosynthetic activity (measured as chlorophyll a fluorescence) and photosynthetic pigment concentrations to assess the effect of copper, cadmium, lead and zinc on the seagrass Zostera capricorni. Custom-made portable in situ exposure (PIE) chambers were developed so seagrasses could be dosed within the meadow. Z. capricorni was exposed to 0.1 and 1 mg l-1 of metal solutions for 10 h. During this time and for the subsequent four-day recovery period, the effective quantum yield of photosystem II (PS II) (?F/Fm?) was measured. While the results were variable, copper and zinc exposed samples had a depressed ?F/Fm? during the exposure period. Samples exposed to zinc recovered to pre-exposure levels but those exposed to copper did not. Cadmium and lead did not impact on the chlorophyll a fluorescence and the chlorophyll pigment data supported these findings. This study presents an innovative new application of chlorophyll a fluorescence stress assessment.
Ralph, P.J., Gademann, R., Larkum, A. & Kuehl, M. 2002, 'Spatial heterogeneity in active chlorophyll fluorescence and PSII activity of coral tissues', Marine Biology, vol. 141, no. N/A, pp. 639-646.
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Ralph, P.J., Polk, S.M., Moore, K.A., Orth, R.J. & Smith, W.O. 2002, 'Operation of the xanthophyll cycle in the seagrass Zostera marina in response to variable irradiance', Journal of Experimental Marine Biology and Ecology, vol. 271, no. 2, pp. 189-207.
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Changes in the photobiology and photosynthetic pigments of the seagrass Zostera marina from Chesapeake Bay (USA) were examined under a range of natural and manipulated irradiance regimes. Photosynthetic activity was assessed using chlorophyll-a fluorescence, and photosynthetic pigments were measured by HPLC. Large changes in the violaxanthin, zeaxanthin, and antheraxanthin content were concomitant with the modulation of non-photochemical quenching (NPQ). Photokinetics (Fv/Fm, rapid light curves (RLC), and non-photochemical quenching) varied as a result of oscillating irradiance and were highly correlated to xanthophyll pigment content. Zeaxanthin and antheraxanthin concentrations increased under elevated light conditions, while violaxanthin increased in darkened conditions. Unusually high concentrations of antheraxanthin were found in Z. marina under a wide range of light conditions, and this was associated with the partial conversion of violaxanthin to zeaxanthin. These results support the idea that xanthophyll intermediate pigments induce a photoprotective response during exposure to high irradiances in this seagrass.
Ralph, P.J. & Short, F.T. 2002, 'Impact of the wasting disease pathogen Labyrinthula zosterae on the photobiology of eelgrass Zostera marina', Marine Ecology Progress Series, vol. 226, no. N/A, pp. 265-271.
Labyrinthula zosterae is clearly shown to be a primary pathogen of eelgrass Zostera marina L., not merely a secondary infection of senescent leaves or an indication of decomposition, The results of this investigation using a Diving-PAM fluorometer indicate that the regions of tissue photosynthetically compromised by Labyrinthula are substantially larger than previously thought. Labyrinthula moves through Zostera marine tissue at a rate of up to 0.8 h-1 during daylight periods. The photosynthetic efficiency of apparently healthy green leaf tissue can be reduced by almost 50% in areas up to 3 mm from a necrotic region infected with Labyrinthula. Once a necrotic spot expands to bisect the eelgrass leaf, the condition of all acropertal tissue diminished; lead tissue up to 5 cm away has severely reduced photosynthetic activity.
Schreiber, U., Gademann, R., Bird, P., Ralph, P.J., Larkum, A. & Kuehl, M. 2002, 'Apparent light requirement for activation of photosynthesis upon rehydration of desicated beachrock microbial mats', Journal of Phycology, vol. 38, no. N/A, pp. 125-134.
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Ralph, P.J., Gademann, R. & Larkum, A. 2001, 'Zooxanthellae Expelled from Bleached Corals at 33C Are Photosynthetically Competent', Marine Ecology Progress Series, vol. 220, pp. 163-168.
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Haynes, D., Ralph, P.J., Pranges, J. & Dennison, B. 2000, 'The Impact of the Herbicide Diuron on Photosynthesis in Three Species of Tropical Seagrass', Marine Pollution Bulletin, vol. 41, no. 0, pp. 288-293.
The impact and recovery from exposure to the herbicide diuron [DCMU; 3-(30,40-dichlorophenyl)-1,1-dimethyl- urea] was assessed for three tropical seagrasses, maintained in outdoor aquaria over a 10-day period. Photosynthetic stress was detected using chlorophyll a Puorescence, measured with a Diving-PAM (pulse am- plitude modulated Puorometer). Exposure to 10 and 100 lg ly1 diuron resulted in a decline in e ective quantum yield (F=Fm0 ) within 2 h of herbicide exposure in Cy- modocea serrulata, Halophila ovalis and Zostera capri- corni. E ective quantum yield also declined over the Rrst 24 h of exposure in H. ovalis at even lower diuron con- centrations (0.1 and 1.0 lg ly1). E ective quantum yield in H. ovalis and Z. capricorni was signiRcantly depressed at all diuron concentrations (0.1 }100 lg ly1) after 5 days exposure, whereas e ective quantum yield in C. serrulata was only signiRcantly lower in plants exposed to highest diuron concentrations (10 and 100 lg ly1). E ective quantum yield depression was present 5 days after plants exposed to 10 and 100 lg ly1 diuron were returned to fresh seawater. These results indicate that exposure to herbicide concentrations present in nearshore Queensland sediments present a potential risk to seagrass functioning.
Ralph, P.J. 2000, 'Herbicide Toxicity of Halophila ovalis Assessed by Chlorophyll a Fluorescence', Aquatic Botany, vol. 66, pp. 141-152.
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Ralph, P.J. 1999, 'Photosynthetic response of Halophila ovalis (R-Br.) Hook. f. to combined environmental stress', Aquatic Botany, vol. 65, no. 1-Apr, pp. 83-96.
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Combinations of stresses showed an additive effect in comparison to the individual stress responses. It is apparent from these results that thermal, elevated-light or osmotic stress increases the sensitivity of Halophila ovalis to any of the other stress
Ralph, P.J. 1999, 'Light-induced photoinhibitory stress responses of laboratory-cultured Halophila ovalis', Botanica Marina, vol. 42, no. 1, pp. 11-22.
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This paper details experiments performed to investigate the short-term stress effects of both high and low-light regimes on laboratory-cultured Halophila ovalis using chlorophyll fluorescence. Increasing irradiance up to 400 mu mol quanta m(-2) s(-1) on
Ralph, P.J., Gademann, R. & Dennison, W.C. 1998, 'In situ seagrass photosynthesis measured using a submersible, pulse-amplitude modulated fluorometer', Marine Biology, vol. 132, no. 3, pp. 367-373.
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Assessments of photosynthetic activity in marine plants can now be made in situ using a newly developed, submersible, pulse-amplitude modulated (PAM) fluorometer: Diving-PAM. PAM fluorometry provides a measure of chlorophyll a fluorescence using rapid-li
Schreiber, U., Gademann, R., Ralph, P.J. & Larkum, A. 1997, 'Assessment of photosynthetic performance of Prochloron in Lissoclinum patella in hospite by chlorophyll fluorescence measurements', Plant And Cell Physiology, vol. 38, no. 8, pp. 945-951.
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Two new PAM fluorometers (pulse amplitude modulated) were used in an investigation of photosynthetic performance of Prochloron resident as a symbiont in the ascidian Lissoclinum patella, growing in a coral reef of Heron Island on the Great Barrier Reef.

Reports

Ralph, P.J. & Sinutok, S. 2013, 'Vallisneria and submerged macrophyte management in Penrith Lakes', AccessUTS Pty Limited, Sydney.
Ralph, P.J., Skilbeck, C.G. & Sinutok, S. 2013, 'Vallisneria and submerged macrophyte management in the Penrith Lakes Scheme', AccessUTS Pty Limited, Sydney.
Petrou, K., Jimenez Denness, I.M., Chartrand, K.M., Ralph, P.J. & Rasheed, A. 2011, 'Seagrass Health Study - Phase II August Update', DEEDI Publication, Cairns, pp. 1-54.
Chartrand, K.M., McKenna, S.A., Petrou, K., Jimenez Denness, I.M., Franklin, J.B., Sankey, T.L., Hedge, S.A., Rasheed, M. & Ralph, P.J. 2010, 'Port Curtis Benthic Primary Producer Habitat Assessment and Health Studies Update: Interim Report December 2010', DEEDI Publication, Cairns, pp. 1-128.
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This interim report provides an update on the Benthic Primary Producer Habitat Assessment and Seagrass Health Studies programs in Port Curtis and Rodds Bay from November 2009 to December 2010. It integrates the multi-faceted monitoring and research program formed from a collaboration between Fisheries Queensland, Vision Environment and Queensland Gas Corporation (QGC) in preparation for the development of a large scale dredging operation for a liquefied coal seam gas port facility on Curtis Island. Many components of this study are still underway and as such results for these are preliminary and are likely to be further refined at the conclusion of experimental work. Full results will be available as part of the final report at the conclusion of experimental studies
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.