Co Authors: John Beardall², Steve Brett³, Martina Doblin?, Was Hosja?, Miguel de Salas?, Peter Thompson?
Hallegraeff G., Beardall, J., Brett, S., Doblin, M., Hosja, W., de Salas, M. and Thompson, P. (2009) Phytoplankton In A Marine Climate Change Impacts and Adaptation Report Card for Australia 2009 (Eds. E.S. Poloczanska, A.J. Hobday and A.J. Richardson), NCCARF Publication 05/09, ISBN 978-1-921609-03-9.
1 School of Plant Science, University of Tasmania, Private Bag 55, Hobart, TAS, Australia
2 School of Biological Sciences, Monash University, Clayton, VIC 3800, Australia
3 Microalgal Services, 308 Tucker Road, Ormond VIC 3204, Australia
4 Plant Functional Biology and Climate Change Cluster, Faculty of Science, University of Technology, Sydney NSW 2065 Australia
5 Department of Water, 7 Ellam St ,Victoria Park , WA, 6100, Australia
6 Australian Antarctic Division, Channel Highway, Kingston, TAS 7050, Australia
7 CSIRO Division of Marine and Atmospheric Research, PO Box 1538, Hobart, TAS 7001, Australia
Expansion of sub-tropical species, including harmful species, into south-eastern waters is driven by warming and a strengthening of the East Australian Current (MEDIUM confidence)
Increased episodes of harmful algal blooms in south-eastern waters in response to extreme rainfall events and warming temperatures (LOW confidence)
Maintain and increase monitoring efforts to detect change in indicator species, and provide information to ocean users on bloom species; maintain and utilise ocean colour satellite derived chlorophyll products
Increase vigilance of harmful algal blooms to allow businesses (such as fish farms) and local agencies to respond rapidly
Professor Gustaaf Hallegraeff was born in the Netherlands and educated at the University of Amsterdam, before joining the CSIRO Marine Laboratories in 1978 and the School of Plant Science of the University of Tasmania in 1992. He is recognised nationally and internationally for his work on harmful algal blooms impacting on human health, the fish farm and shellfish industries, their stimulation by coastal eutrophication and global spreading via ship’s ballast water. His current research focus is on the impact of climate change on phytoplankton in Australian coastal waters and the Southern Ocean. He was awarded the 2004 Eureka Prize for Environmental Research, elected a Fellow of the Australian Academy for Technological Sciences and Engineering in 2005 and currently serves as the Vice-President of the Internal Society for the Study of Harmful Algae.
Dr Peter Thompson leads a small team investigating phytoplankton and nutrient dynamics. He completed a BSc, Masters and received his PhD in biological oceanography in 1991. He has worked on phytoplankton physiology including nutrient uptake dynamics, responses to light, temperature and pH at the University of British Columbia (Vancouver, Canada) and at the Canadian Department of Fisheries and Oceans. Since 1993 Peter has worked for the CSIRO and the University of Tasmania largely on phytoplankton ecology in water bodies under anthropogenic stress; providing advice to industry and resource managers on remediation and monitoring options. Recent work has focused on the impacts of climate variability on phytoplankton dynamics at the shelf scale and the consequences for Australia’s fisheries.
Miguel de Salas was born in Spain. He obtained a BSc (1st class) Hons from the University of Tasmania in 1999 and a PhD from the same institute in 2004 for work on the taxonomy of fish-killing unarmoured dinoflagellates. Subsequently, he was awarded a postdoc fellowship from the University of Tasmania (2005-2008) for the development of quantitative molecular detection technologies for harmful dinoflagellates, principally the genus Alexandrium (PSP producers) and the family Kareniaceae (fish-killers and NSP producers). He currently is employed by the Australian Antarctic Division to work on the impact of climate change on marine protists and repercussions for vertical carbon export in the Subantarctic Zone.
Was Hosja is a senior environmental officer with the Western Australian Department of Water, with over 30 years of experience in phytoplankton and algal bloom monitoring of WA inland, estuarine and marine coastal waters.
Government of Western Australia, Department of Water. Victoria Park Regional Office. 7 Ellam St, Victoria Park WA 6100, Australia. Was.Hosja @water.wa.gov.au
Dr Steve Brett, Director of Microalgal Services, is involved in numerous projects on phytoplankton from Australian coastal waters and has a special interest in distribution and expansion of potentially harmful species. He completed undergraduate studies in marine botany and zoology, and a Ph.D. in phytoplankton biology at the University of Melbourne. He has worked as Curator of the U.S. National Phytoplankton Collection (CCMP) and has also held various university teaching and research positions. In 1998, he founded Microalgal Services in response to the need for an Australian laboratory specializing in identification and monitoring of marine phytoplankton, and now provides services and advice to private and government organizations in most Australian states.
Professor John Beardall was originally trained as a microbiologist and then completed a PhD, on the physiology and biochemistry of phytoplankton photosynthesis, at the University of London. He moved to Australia in 1982, initially to an appointment at La Trobe University then later to Monash University where he is currently Head of the School of Biological Sciences. He is a nationally and internationally recognised expert in algal physiology, especially photosynthesis and respiration. His main research interests at present relate to understanding the likely impacts of global change on phytoplankton and seaweeds, and on the productivity of the oceans.
Dr Martina Doblin graduated from the University of Tasmania and was a postdoctoral research fellow at Old Dominion University, USA before becoming a self supporting research assistant professor from 2000-2004. On return to Australia she worked as a senior policy officer at the Department of Sustainability, Victoria and in mid 2005 joined the University of Technology, Sydney. Recognised nationally and internationally for her work on biogeochemical cycling in aquatic foodwebs, as well as plankton ecology, she was awarded the U.S. Department of Commerce Gold Medal in 2008 together with colleagues for her work on species introductions to the Great Lakes. Her current research examines aquatic foodweb function in relation to environmental changes driven by global and regional processes such as climate change and eutrophication. She currently serves as the Secretary of the Australasian Society for Phycology and Aquatic Botany.
Prediction of the impact of global climate change on marine phytoplankton is fraught with uncertainties. Increasing temperature, enhanced surface stratification, alteration of ocean currents, intensification or weakening of local nutrient upwelling, stimulation of photosynthesis by elevated CO2, reduced calcification through ocean acidification, heavy precipitation, and storm events causing changes in land runoff and micronutrient availability, may all produce contradictory species- or even strain-specific responses. Complex factor interactions exist and simulated ecophysiological laboratory experiments rarely allow for sufficient acclimation or take into account physiological plasticity and genetic strain diversity. In the absence of Australian datasets spanning 30 consecutive years, we must use appropriate datasets from other locations, look to the geological record for past responses to climate, and examine the response of phytoplankton to climate forcing over shorter time scales (e.g., El Niño-Southern Oscillation). Given documented changes in Australia and other parts of the world, we can expect: (1) range expansion of warm-water species at the expense of cold-water species, which are driven polewards; (2) changes in the abundance and seasonal window of growth of selected phytoplankton species; (3) earlier timing of peak production of phytoplankton, especially in temperate regions; (4) Knock-on effects for marine food webs, notably when individual zooplankton and fish grazers are differentially impacted (“match-mismatch”) by climate change. Some harmful algal bloom phenomena (e.g. toxic dinoflagellates benefitting from land runoff and/or water column stratification, tropical benthic dinoflagellates responding to warmer water temperatures and coral reef disturbance) may become worse, while others may diminish in areas currently impacted. The greatest problems for human society will be caused by being unprepared for significant range expansions or the increase of algal biotoxin problems in currently poorly monitored areas, thus calling for increased vigilance in seafood biotoxin and algal monitoring programmes. A combination of laboratory and field approaches over multiple spatial and temporal scales is necessary to better predict climate impacts on phytoplankton.
Unfortunately very few long-term Australian phytoplankton records exist at any single locality, where ideally we need at least 30 consecutive years to recognise and predict long-term trends. The only available Australian data relate to the New South Wales Port Hacking station sampled intermittently since the 1930s, the Tasmanian Maria Island station (monthly hydrology since 1944), the Western Australian Rottnest Island station (hydrology since 1951) and Australian shellfish quality assurance programs in operation in Tas, Vic, SA, WA, NSW, Qld since the 1990s. However we can learn important lessons from the dinoflagellate cyst fossil record that provides an indication of past responses to climate change (McMinn 1988), from the few long-term phytoplankton data sets available in other locations such as the North Atlantic Continuous Plankton Recorder surveys (Hays et al. 2005) and from short-term phytoplankton community responses to El Niño-Southern Oscillation episodes.
For many phytoplankton species, significant bloom episodes can serve as stepping stones towards range expansions via natural current systems, sometimes facilitated by local climate events. Blooms provide a large inoculum to an area and are usually accompanied by large-scale oceanographic phenomena that modify ocean conditions from weeks to months. Furthermore, cyst production may be important because it creates a mechanism for future bloom occurrences, survival through environmental stresses, as well as introduces genetic diversity (recombination) into the population. The cyst-producing dinoflagellate Pyrodinium bahamense is presently confined to tropical, mangrove-fringed coastal waters of the Atlantic and Indo-West Pacific. Starting in 1972 in Papua New Guinea red-brown water discolorations coincided with the fatal food poisoning of three children in a seaside village, diagnosed as paralytic shellfish poison (PSP). Since then, the incidence of toxic blooms have spread to Brunei and Sabah (1976), the central (1983) and northern Philippines (1987) and Indonesia (North Mollucas). Pyrodinium is a serious public health and economic problem for tropical countries, all of which depend heavily on seafood for protein. In the Philippines alone, Pyrodinium has now been responsible for more than 2000 human illnesses and 100 deaths resulting from the consumption of contaminated shellfish as well as sardines and anchovies (Maclean 1989; Hallegraeff and Maclean 1989; Azanza and Taylor 2001). There exists strong circumstantial evidence of a coincidence between Pyrodinium blooms and the El Niño Southern Oscillation (ENSO; Maclean 1989). A survey of cyst fossils (named Polysphaeridium zoharyii) going back to the warmer Eocene 50 million years ago indicates a much wider range of distribution in the past. For example, in the Australasian region at present, the alga is not found in the plankton further south than Papua New Guinea but, some 120,000 years ago, the alga ranged as far south as Belahdelah (32oS) just north of Sydney (McMinn 1988). There is concern that, with increased warming of the oceans, this species may return to Australian waters, Ciguatera, caused by the benthic dinoflagellate species complex Gambierdiscus toxicus, is a tropical fishfood poisoning syndrome well-known in coral reef areas in the Caribbean, Australia, and especially French Polynesia. Whereas, in a strict sense, this is a completely natural phenomenon, from being a rare disease two cen¬turies ago, ciguatera has now reached epidemic proportions in French Polynesia. Evidence is accumulating that reef disturbance by hurricanes, military and tourist developments (Bagnis et al. 1985), as well as coral bleaching (linked to global warming), increased water temperatures (>29OC preferred in culture) and perhaps increasing coral damage due to ocean acidification are increasing the risk of ciguatera by freeing up space for macroalgae for Gambierdiscus to colonize upon. During El Niño events ciguatera increased on Pacific islands where sea surface temperatures warmed (Hales et al. 2001). In the Australian region, Gambierdiscus toxicus is well-known from the tropical Great Barrier Reef and southwards to just north of Brisbane (25oS) but in the past 5 years this species has undergone an apparent range extension into South-East Australian sea grass beds as far south as Merimubula (37oS), aided by a strengthening of the East Australian Current (EAC) (Brett, de Salas & Hallegraeff, unpublished). It is not yet known whether this represents a seasonal (April-May) EAC-driven incursion or whether this species is able to overwinter in southern waters. A similar expansion of Gambierdiscus into the Mediterranean and Eastern Atlantic has also been reported (Aligizaki et al. 2008).
The red-tide dinoflagellate Noctiluca scintillans (known from Sydney as early as 1860) has expanded its range from Sydney into Southern Tasmanian waters since 1994 where it has caused problems for the salmonid fish farm industry. Dakin and Colefax (1933) observed this species to be a minor component of the phytoplankton of New South Wales coastal waters and Wood (1954) in his extensive Australia-wide net-phytoplankton surveys reported this taxon to occur only in Australian east coast estuaries. The first visible Noctiluca “red tide” event was not reported until August 1982 in Lake Macquarie, central New South Wales. However, from a rare bloom former in the 1980s, starting in 1993 this organism has developed into one of the most prominent red-tide organisms in Sydney coastal waters soon after the commissioning of three deepwater ocean sewage outfalls off Australia’s largest coastal city. El Niño years such as 1997 have exhibited the densest Noctiluca blooms, which occasionally have forced closures of Sydney public beaches during spring and summer. While Noctiluca was virtually absent during a seasonal study of Sydney coastal waters during 1978-79, in a repeat survey in 1997-98 the species was present in 61% of samples. Irregular influxes of Noctiluca, most likely carried by the East Australian Current, have also been seen in Port Phillip Bay, Melbourne (since 1993) and Tasmania (since March 1994). No Noctiluca bloom reports are known from Tasmania (43oS) prior to this date. A bloom event which apparently started off the East Coast of Tasmania in September 2001 culminated in March 2002 into a significant threat to the salmonid aquaculture industry in Nubeena on the Tasman Peninsula. Noctiluca blooms have persisted in Tasmanian waters ever since, notably in the period 2001-2006. While in New South Wales this dinoflagellate proliferates at water temperatures of 19-24oC, in colder Tasmanian waters it now has established permanent overwintering populations and thrives even in winter months at temperatures of 10-12oC. We interpret that the gradual warming of East Coast Tasmanian waters, associated with a greater influence of the East Australian Current (Ridgway 2007), has paved the way for the apparent range extension of this warm-water organism into Tasmanian waters. More difficult to explain is how in 2008, the first tropical red Noctiluca bloom was reported from Cairns Harbour in Queensland in March, followed by bloom reports from Port Esperance, Western Australia, and Port Lincoln, South Australia, in May-June (Hallegraeff et al. 2008).
In the North Sea an analogous northward shift of warm-water phytoplankton has occurred due to regional climate warming (Edwards and Richardson 2004, Richardson and Schoeman 2004).While warm-water species can be expected to expand their distribution, cold-water species will contract their range (compare Beaugrand et al. 2002 for zooplankton). For example, the coldwater dinoflagellate cyst Bitectatodinium tepikiense currently is confined to Tasmania (43oS), but in the last interglacial period (120,000 yrs ago) it was found as far north as Sydney (34 oS) (McMinn and Sun 1994).
Several well-studied toxic dinoflagellates such as Alexandrium catenella in Puget Sound (Moore et al. 2008 a,b) and Gymnodinium catenatum in Tasmania, Australia (Hallegraeff et al. 1995) bloom in well-defined seasonal temperature windows (>13 and >10oC , respectively). Climate change scenarios are predicted to generate longer-lasting bloom windows, of which some early signs can be seen with Gymnodinium catenatum now persisting in Tasmania through warmer winter months.
In the North Sea the North Atlantic Oscillation has been shown to affect the length of the phytoplankton growing season which has increased in parallel with the warming of sea surface temperatures (Barton et al. 2003). Seasonal timing of phytoplankton blooms is now occurring there up to 4-5 weeks earlier. Coastal stations at Port Hacking, Rottnest Island and Maria Island all show significant lengthening of the growing season (warmer temperatures in spring and autumn) over the last ~ 50 years but there is no evidence to date of earlier phytoplankton spring blooms (Thompson et al. in press).
There is also evidence of changes in dissolved nutrient concentrations in Australian coastal waters, with a marked decline in silicate in SE Australia (Thompson et al, submitted). Declines in silicate have been reported elsewhere in the ocean (Goffart et al. 2002), are widely expected in a warming world where the vertical delivery of nutrients to the surface ocean may be slowed due to stratification, and are anticipated to restrict the abundance of diatoms (Behrenfeld et al. 2006). Where individual zooplankton or fish grazers are differentially impacted by ocean warming, this may have cascading impacts on the structure of marine food webs (“match-mismatch” sensu Cushing 1974).
Extreme events, storms and rainfall
Episodic storm events affect the timing of freshwater flow, residence time, and the export of nutrients to the coastal ocean including the magnitude, composition (inorganic versus organic; Seitzinger et al. 2002) and timing of nutrient pulses. Changes in the amount or timing of rainfall and river runoff affects the salinity of estuaries and coastal waters. There is some evidence for increasing salinities in Port Phillip Bay and other coastal locations as a result of drought (Thompson et al. in press). Freshwater also modifies the stratification of the water column thereby affecting nutrient resupply from below. While diatoms seem to be negatively affected by the decrease in nutrient concentrations associated with river discharge, dinoflagellates often benefit as this usually increases stratification and the competitive advantage of vertically migrating species as well as the availability of humic substances for growth (Doblin et al. 2006). PSP dinoflagellate blooms of Gymnodinium catenatum (in Tasmania; Hallegraeff et al. 1995) tend to be closely associated with land runoff events. Given the diversity of coastal settings in Australia that receive winter or summer-dominated rainfall, the impacts of changes in land runoff are likely to be regionally specific.
Observed and projected changes in phytoplankton characteristics of Australia’s marine realm.
*Cubillos et al. 2007; **Beardall & Raven 2004, Beardall &Stojkovic 2006, † Goffart et al. 2002)
• Prediction of the impact of global climate change on marine phytoplankton is fraught with uncertainties.
• We can expect: (1) Range expansion of warm-water species at the expense of cold-water species which are driven pole wards; (2) Changes in the abundance and seasonal window of growth of selected phytoplankton species; (3) Knock-on effects for phytoplankton marine webs, when individual zooplankton and fish grazers are differentially impacted (“match-mismatch”) by climate change.
• Some harmful algal bloom phenomena (e.g. toxic dinoflagellates benefitting from land runoff and/or water column stratification, tropical benthic dinoflagellates responding to increased water temperatures and coral reef disturbance) may become worse, while others may diminish in areas currently impacted.
• Increased vigilance in seafood biotoxin and algal bloom monitoring programmes is called for.
Confidence Assessments >
There is MEDIUM evidence and a LOW consensus, therefore LOW confidence, of climate-driven changes in phytoplankton Australian waters due to a lack of long-term data series.
Potential Impacts by the 2030s and 2100s:
Potential impacts by the 2030s and 2100s
There is MEDIUM evidence and a MEDIUM-HIGH consensus from studies elsewhere and from retrospective studies (sedimentary records) that climate change will impact Australian phytoplankton this century. Therefore, a MEDIUM confidence level was assigned.
Adaptation Responses >
The Australian Continuous Plankton Recorder surveys (part of the Integrated Marine Observing System) and Southern Ocean CPR surveys (AAD) are now surveying phytoplankton in East Coast Australian and Southern Ocean waters. National Reference Stations (IMOS) are characterising water column properties and phytoplankton composition at key sites.
Future responses could include a more coordinated system of monitoring phytoplankton and toxins in the Australian seafood and mariculture industry and a means of rapid communication if problems emerge
We need a better understanding of the links between phytoplankton and marine foodwebs supporting commercially important shellfish and fish stocks. Harvested populations should be monitored for changes in condition as a result of declining phytoplankton biomass or nutritional quality.
The high probability of range expansions by toxic species outside their normal range requires health care workers and environmental agencies be alerted to the symptoms and adjust their monitoring appropriately.
Knowledge Gaps >
• The response to elevated CO2 has been determined in < 5% of phytoplankton species, so we have a very incomplete knowledge of the ecophysiological responses of phytoplankton to climate change.
• Very few long-term Australian phytoplankton records exist at any single locality, where ideally we need at least 30 consecutive years to recognise and predict trends in phytoplankton species distributions.
• Complex factor interactions exist and simulated ecophysiological laboratory experiments rarely allow for sufficient acclimation or take into account physiological plasticity and genetic strain diversity. Only a limited number of mixed phytoplankton populations have been investigated in laboratory settings, and these have not been able to replicate physical changes in ocean conditions such as enhanced surface stratification and alteration of ocean currents, intensification or weakening of local nutrient upwelling, stimulation of photosynthesis by elevated CO2, reduced calcification through ocean acidification, heavy precipitation and storm events causing changes in land runoff and micronutrient availability, may all produce contradictory species- or even strain-specific responses.
• At the regional scale, there is little understanding how offshore oceanographic processes affect nearshore coastal waters and how inter-annual and decadal variability in climate (let alone long-term changes) affects phytoplankton populations.
Increasing temperature, enhanced surface stratification and alteration of ocean currents, intensification or weakening of local nutrient upwelling, stimulation of photosynthesis by elevated CO2, reduced calcification through ocean acidification, heavy precipitation and storm events causing changes in land runoff and micronutrient availability, may all produce contradictory species- or even strain-specific responses. A combination of laboratory and field approaches over multiple spatial and temporal scales are necessary to predict climate impacts on phytoplankton.
To address present uncertainties, we recommend:
• Keystone phytoplankton species from around Australia be brought into culture and studied for their responses to variables such as elevated temperature and CO2 and changing pH (see CSIRO Collection of Living Microalgae http://www.marine.csiro.au/microalgae/).
• Maintaining existing long-term monitoring programs in coastal waters that document phytoplankton species composition. (see Integrated Marine Observing System, National Reference Stations and Australian Continuous Plankton Recorder at http://imos.org.au/).
• Increasing the spatial and temporal sampling of phytoplankton in the ocean using optical sensors that record phytoplankton abundance, information about species composition, physiological health and productivity. (See information on instrumentation including multiwavelength and variable fluorometers on moorings, ocean gliders, ships at http://imos.org.au/.; and CSIRO Remote Sensing Facility http://www.marine.csiro.au/~lband/)
• Integrate far field oceanographic processes with those in near shore coastal waters using ship-based observations, satellite remote sensing and regional ocean models to examine the impacts of oceanographic currents, eddies and other large-scale processes on phytoplankton (see National Marine Facility http://www.marine.csiro.au/nationalfacility/)
• Integrate observations of freshwater flow-estuarine dynamics with regional ocean models to examine the impacts of changing rainfall patterns on nutrient, sediment and other pollutant fluxes and the response of phytoplankton to short-term weather events and long-term climate influences (e.g. El Niño-Southern Oscillation).(see Bluelink ocean forecasting http://www.marine.csiro.au/bluelink/)
Further Information >
If appropriate, please supply recommendations for further information bearing in mind this should appeal to a wide section of society. These can be websites, articles not included in the assessment, books, clubs and societies.
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