SHORT COMMUNICATION. Climate-driven range expansion of the red-tide dinoflagellate Noctiluca scintillans into the Southern Ocean

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1 JOURNAL OF PLANKTON RESEARCH j VOLUME 34 j NUMBER 4 j PAGES j 2012 SHORT COMMUNICATION Climate-driven range expansion of the red-tide dinoflagellate Noctiluca scintillans into the Southern Ocean DAVID J. MCLEOD 1,3 *, GUSTAAF M. HALLEGRAEFF 2, GRAHAM W. HOSIE 3 AND ANTHONY J. RICHARDSON 1,4,5 1 CSIRO MARINE AND ATMOSPHERIC RESEARCH, ECOSCIENCES PRECINCT, GPO BOX 2583, BRISBANE, QUEENSLAND 4102, AUSTRALIA, 2 INSTITUTE FOR MARINE AND ANTARCTIC STUDIES, UNIVERSITY OF TASMANIA, PRIVATE BAG 129, HOBART, TAS 7001, AUSTRALIA, 3 AUSTRALIAN ANTARCTIC DIVISION, DEPARTMENT OF SUSTAINABILITY, ENVIRONMENT, WATER, POPULATION AND COMMUNITIES, KINGSTON, TAS 7050, AUSTRALIA, 4 CENTRE FOR APPLICATIONS IN NATURAL RESOURCE MATHEMATICS, SCHOOL OF MATHEMATICS AND PHYSICS, THE UNIVERSITY OF QUEENSLAND, ST LUCIA, QUEENSLAND 4072, AUSTRALIA AND 5 ENVIRONMENTAL DECISIONS GROUP, SCHOOL OF BIOLOGICAL SCIENCES, THE UNIVERSITY OF QUEENSLAND, BRISBANE 4072, AUSTRALIA *CORRESPONDING AUTHOR: david.mcleod@csiro.au Received October 13, 2011; resubmitted on December 23, 2011; accepted in principle December 28, 2011 Corresponding editor: John Dolan We describe a climate-driven range expansion of the red-tide dinoflagellate Noctiluca scintillans into the Southern Ocean ( S 1478E). Sea surface height data showed that a warm-core eddy moving southwards from Tasmania was the potential vector for the transport of Noctiluca. We provide evidence for active feeding of Noctiluca on Southern Ocean phytoplankton. Possible competition with other grazers may have implications for food web dynamics were Noctiluca to become established in the Southern Ocean. KEYWORDS: Noctiluca; climate change; continuous plankton recorder; East Australian current; range expansion; Tasmania Southeast Australia has been identified as a climate change hotspot (Johnson et al., 2011) due to increased southward penetration of the East Australian Current (EAC) (Ridgway, 2007), a situation that appears to be caused by altered circulation patterns in response to global warming (Cai et al., 2005). Over the past 60 years, this increased intensity of the EAC has resulted in more frequent incursions of warm water into Tasmania and an average increase in sea surface temperature approximately four times that of the global ocean (Ridgway, 2007). This extension of the EAC has facilitated the transportation of a range of marine taxa southward into Tasmanian waters, including phytoplankton (Hallegraeff, 2010), zooplankton (Johnson et al., 2011), invertebrates (Ling et al., 2009) and coastal fish (Last et al., 2011). A holoplanktonic example of a recent range expansion into Tasmanian waters is that of the heterotrophic dinoflagellate Noctiluca scintillans (hereafter Noctiluca). This large ( mm diameter) predatory species is one of the most studied red-tide forming organisms (Elbrachter and Qi, 1998; Harrison et al., 2011). Since it doi: /plankt/fbr112, available online at Advance Access publication February 1, 2012 # The Author Published by Oxford University Press. All rights reserved. For permissions, please journals.permissions@oup.com

2 D. J. MCLEOD ET AL. j NOCTILUCA IN THE SOUTHERN OCEAN was first documented in Sydney Harbour in 1860, Noctiluca has extended its range and has now been recorded around most of the Australian coast (Hallegraeff et al., 2008). It was first observed in Tasmania in 1994, apparently carried by the EAC, and has since become established with overwintering populations now present (Hallegraeff et al., 2008). In 2008, it was found in Queensland, Western Australia and South Australia for the first time; regions that have been monitored since the early 1990s (Hallegraeff et al., 2008). Noctiluca exhibits a phagotrophic feeding habit and consumes a variety of prey (Elbrachter and Qi, 1998; Quevedo et al., 1999). This feeding can lead to competition with other grazers, such as copepods that are reliant on the same food source (Elbrachter and Qi, 1998). Noctiluca has also been implicated in the decline of fisheries in the northern Indian Ocean (Thangaraja et al., 2007) and caged fish production in a variety of locations (Huang and Qi, 1997; Smayda, 1997). The continued range expansion of Noctiluca and increased abundance in southeast Australia could have deleterious impacts on important aquaculture, fisheries and tourism in the region. Here, we document the continued range expansion of Noctiluca and include, for the first time, data from the Southern Ocean. Using samples from the Continuous Plankton Recorder (CPR), we describe the most southerly oceanic record of the red-tide forming Noctiluca, a species generally considered neritic in its distribution (Harrison et al., 2011), and provide evidence that climate-driven ocean warming is likely to be the major driver behind the continued range expansion. Potential impacts of feeding by the species on Southern Ocean productivity are discussed. As part of the Southern Ocean CPR (SO-CPR) and Australian CPR (AusCPR) Surveys, a CPR transect was conducted south of Tasmania, Australia between 10 and 12 December 2010 (see Hosie et al. (2003) for detailed CPR methodology used in the Southern Ocean). Sea surface temperature and in vivo fluorescence (indicating chlorophyll concentration) were continuously recorded at 1 min intervals along the transect. Based on the fluorescence/chlorophyll a relationship from a recent study in the same region (458S 1448E), fluorescence readings were converted to chlorophyll a biomass according to Westwood et al. (2011): chl a ¼ 0:14 fluorescence þ 0:991 In the laboratory, the silk was unrolled and cut into segments representing five nautical mile samples. Then, the presence or absence of each phytoplankton taxon was assessed in 20 microscope fields, 300 mm in diameter along two diagonals across the filtering silk, representing 0.02% of the silk (see Richardson et al. (2006) for details on phytoplankton methodology). All zooplankton were rinsed off the silk and counted. Each organism was identified to the lowest taxonomic level possible, usually species. Because of the large size of Noctiluca cells, they were counted during the zooplankton count. Random subsamples of up to a maximum of 10 Noctiluca cells from each sample were examined for evidence of feeding and measured for cell size using digital photography. Cells were scanned under high power (630) and any prey viewed inside the cell were identified to the lowest possible taxa and recorded. To investigate the physical oceanographic conditions at the time of the study, sea surface height anomaly (SSHA) was used to track the movement of a warm-core eddy as it moved southwards from Tasmania. SSHA data were obtained from the updated AVISO data series of altimeter products ( en/data/products/sea-surface-height-products/global/ index.html). Data plotted are a 7-day composite at resolution. A total of 2866 Noctiluca cells were counted in 23 out of the 26 most northern samples along the CPR transect, indicating a bloom that extended a minimum of 130 nautical miles (241 km, Fig. 1). Noctiluca cells were large and had an average diameter of mm. Cells were found in the first sample along the transect ( S E), suggesting that the bloom also occurred north of where we sampled. The maximum number of cells recorded in one 5 nautical mile sample was 364, indicating an abundance of 0.24 cells per litre based on one sample filtering 1.5 m 3 of seawater. It is likely that the true abundance was higher than recorded, due to clogging of the CPR mesh by Noctiluca and therefore reduced filtration efficiency as seen in other studies (Walne et al., 1998). The occurrence of Noctiluca observed here ( S 1478E) is the most southerly record globally. Previously, the most southerly location of Noctiluca comes from Thompson et al. (Thompson et al., 2008), who documented high abundances in the Huon Estuary and D Entrecasteaux Channel, Tasmania (43.48S E) between 2003 and The current observation of Noctiluca is some 240 km further south, equivalent to an average poleward migration rate of 40 km per year. Red-tide forming Noctiluca is a neritic species (Harrison et al., 2011) and oceanic occurrences are uncommon. Due to the large-scale, remote and offshore nature of the bloom, this occurrence is unlikely to be associated with eutrophication or ballast water. In over 20 years of ballast water sampling in the Australian 333

3 JOURNAL OF PLANKTON RESEARCH j VOLUME 34 j NUMBER 4 j PAGES j 2012 Fig. 1. Apparent range extension of Noctiluca scintillans in the Australian region, comparing distribution records in , (expansion of blooms in Sydney region), (range extension into Tasmania), 2008 (first reports in Queensland, Western Australia and South Australia) and 2010 (first report in the Southern Ocean south of Tasmania). The legend shows number of cells per 5 nautical mile segment. Grey circles represent records of Noctiluca from AusCPR samples collected between Melbourne and Adelaide in 2010 (data from www. imos.org.au/emii). Maps are reproduced from Hallegraeff et al. (Hallegraeff et al., 2008). region, Noctiluca has never been seen and, due to its fragility, is unlikely to survive this method of translocation (Hallegraeff, unpublished data). It is much more likely that Noctiluca was transported via oceanographic processes. SSHA data show that a warm-core eddy of the EAC was moving south of eastern Tasmania at the time (Fig. 2). Sea surface temperature was warm inside the bloom ( 13.58C) and cooled outside the bloom 334

4 D. J. MCLEOD ET AL. j NOCTILUCA IN THE SOUTHERN OCEAN Fig. 2. Weekly composites of SSHA in the region south of Tasmania showing movement of the warm-core eddy sampled by the CPR in December (a) Black circle highlights eddy formation off eastern Tasmania. (f) Black line indicates the extent of Noctiluca scintillans from the CPR transect. 335

5 JOURNAL OF PLANKTON RESEARCH j VOLUME 34 j NUMBER 4 j PAGES j 2012 Fig. 3. Chl a, sea surface temperature (8C), Noctiluca scintillans abundance and total copepod abundance along a CPR transect conducted south of Tasmania in December White bars show the extent of the Noctiluca bloom with the highest peak corresponding with 364 cells/5 nautical mile CPR sample. Copepod abundance is represented by grey bars. ( 118C, Fig. 3). The eddy that potentially translocated Noctiluca also extended well south of the CPR transect, and it is plausible that this study only sampled the western edge of a bloom that covered a large geographic area (Fig. 2). The occurrence of Noctiluca in this study continues its expansion southward from Sydney Harbour in 1860 (Hallegraeff et al., 2008) to the Southern Ocean in Isotherms of the EAC have moved.350 km southward over this time (Ridgway, 2007), an observation that has been linked to changes in the South Pacific gyre in response to climate change (Cai et al., 2005). Thus, the range expansion of Noctiluca into the Southern Ocean is likely to be a direct consequence of the increased poleward penetration of the EAC and the subsequent increase in frequency of warm core eddies travelling to Tasmania and beyond. As the EAC is likely to continue to strengthen and transport more warm water and eddies further south (Cai et al., 2005; Ridgway, 2007), there may be more frequent seeding of Noctiluca into the Southern Ocean in the future. Since the first occurrence of Noctiluca in Tasmania in 1994, it has established over-wintering populations that thrive in C waters (Hallegraeff et al., 2008). The sea surface temperature inside the bloom documented in this study was 13.58C. Elsewhere, Noctiluca has been reported throughout winter off the coast of Sylt, Germany, surviving temperatures below 08C (Elbrachter and Qi, 1998). There thus appears to be no thermal barrier to the establishment of Noctiluca in the Southern Ocean. Harrison et al. (Harrison et al., 2011) suggest that multiple temperature strains of the species may exist. It appears likely that the current Southern Ocean occurrence is an extension of the Tasmanian population and is perhaps a cool-water strain capable of establishing populations in the Southern Ocean. Noctiluca generally over-winters in estuarine environments and proliferates in spring and summer when food becomes more abundant (Dela-Cruz et al., 2002). It is unknown whether Noctiluca has an over-wintering mechanism that would be viable in oceanic environments, such as the Southern Ocean. Evidence of active feeding indicates that Noctiluca may impact the Southern Ocean ecosystem were it to become established. Of the 197 cells examined for evidence of feeding, 109 (55%) contained prey visible under a light microscope. In all, eight taxa were identified, with diatoms Thalassiosira spp. (in 40% of cells) and Guinardia striata (20%) the most frequent. No evidence for changes in prey consumption with latitude along the transect were found. A total of 33 phytoplankton taxa were identified from routine phytoplankton analysis, with Thalassiosira spp. the most common species cooccurring with Noctiluca. These small round cells were found in 92% of samples where Noctiluca was recorded and were also the most common prey item. Despite heavy grazing by Noctiluca on Thalassiosira spp., it remained the most prevalent species inside the Noctiluca bloom. It is possible that Noctiluca had recently begun grazing on Thalassiosira spp.; long enough to ingest numerous cells and to reduce total Chl a but not long enough to prevent Thalassiosira spp. remaining common. Dela-Cruz et al. (Dela-Cruz et al., 2002) also found Thalassiosira spp. to be the most frequently consumed prey of Noctiluca off south eastern Australia. 336

6 D. J. MCLEOD ET AL. j NOCTILUCA IN THE SOUTHERN OCEAN Other studies have shown that Noctiluca competes indirectly with other grazers by competition for food (Umani et al., 2004) and directly by predation of invertebrate eggs (Quevedo et al., 1999). Here, copepod abundance was low inside the bloom (mean of 12 individuals per sample) and increased outside the bloom (58 individuals per sample), indicating potential competition for food with Noctiluca. If viable populations of Noctiluca became established in the Southern Ocean in the future, there is likely to be additional competition for phytoplankton with copepod grazers, with unknown effects for the food web. The continued southward expansion of Noctiluca in Australia is consistent with increased warming off southeast Australia and is facilitated by the intensification of the EAC that has been linked to anthropogenic greenhouse gas emissions. On present evidence, the expansion of Noctiluca into the Southern Ocean is eddy-driven from coastal populations off Tasmania. As Southern Ocean temperatures continue to warm and the EAC continues to intensify, Noctiluca could well become resident in the Southern Ocean. ACKNOWLEDGEMENTS We would like to thank the captain and crew of the RSV Aurora Australis who helped deploy the CPR. We acknowledge Ben Raymond from the Australian Antarctic Data Centre (AADC) for his assistance with satellite data. Altimeter products were produced by SSALTO/DUACS and distributed by AVISO with support from CNES. FUNDING SO-CPR is supported by the Australian Antarctic Division through AAS Project 472. AusCPR is funded by the Integrated Marine Observing System (IMOS), which is funded by the Australian Government through the National Collaborative Research Infrastructure Strategy and the Super Science Initiative. REFERENCES Cai, W., Shi, G., Cowan, T. et al. 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