Marine Pollution Bulletin 51 (2005) 428–437 www.elsevier.com/locate/marpolbul
Blooms of the cyanobacterium Lyngbya majuscula in coastal Queensland, Australia: disparate sites, common factors Simon Albert
b
a,*
, Judith M. OÕNeil a,b, James W. Udy a, Kathleen S. Ahern a, Cherie M. OÕSullivan a, William C. Dennison b
a University of Queensland, Centre for Marine Studies, Brisbane, Qld. 4072, Australia University of Maryland, Center for Environmental Science, Cambridge, MD 21613, USA
Abstract During the last decade there has been a significant rise in observations of blooms of the toxic cyanobacterium Lyngbya majuscula along the east coast of Queensland, Australia. Whether the increase in cyanobacterial abundance is a biological indicator of widespread water quality degradation or also a function of other environmental change is unknown. A bioassay approach was used to assesses the potential for runoff from various land uses to stimulate productivity of L. majuscula. In Moreton Bay, L. majuscula productivity was significantly (p < 0.05) stimulated by soil extracts, which were high in phosphorus, iron and organic carbon. Productivity of L. majuscula from the Great Barrier Reef was also significantly (p < 0.05) elevated by iron and phosphorus rich extracts, in this case seabird guano adjacent to the bloom site. Hence, it is possible that other L. majuscula blooms are a result of similar stimulating factors (iron, phosphorus and organic carbon), delivered through different mechanisms. 2004 Elsevier Ltd. All rights reserved. Keywords: Lyngbya majuscula; Bioassay; Nutrients; Land use; Organic carbon; Iron
1. Introduction Lyngbya majuscula (Gomont) is a toxic, filamentous marine cyanobacterium (family Oscillatoriacea), previously cited in the literature as Microcoleus lyngbyaceus (Ku¨tzing) (Diaz et al., 1990; Speziale and Dyck, 1992). L. majuscula grows on solid or sandy substrates or epiphytically on seagrass, macroalgae and corals in the coastal zones of many sub-tropical and tropical oceans. Since the early 1990Õs, nuisance blooms of this toxic cyanobacterium have been observed seasonally in Moreton Bay, Queensland, Australia (Dennison et al., 1999).
*
Corresponding author. Fax: +61 7 33657321. E-mail address:
[email protected] (S. Albert).
0025-326X/$ - see front matter 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2004.10.016
In Moreton Bay, L. majuscula blooms typically begin in the summer (December/January) and expand rapidly over the following two–three months to an area on a kilometre square scale (10–30 km2) (Dennison et al., 1999; OÕNeil and Dennison, 2004). This is often followed by a rapid population collapse, possibly aided by viruses specific to L. majuscula (Hewson et al., 2001). During this cycle L. majuscula has been observed to begin growing from the sediment below the seagrass canopy. As the ÔbloomÕ develops this benthic mat is able to grow sufficiently to overtop the seagrass species creating a blanketing effect that can turn the sediment and bottom water anoxic (pers. obs.). Often after periods of high light, warm temperatures and calm weather, bubbles from rapid photosynthesis by the L. majuscula are trapped within the filament matrix and cause the
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L. majuscula to eventually float to the waters surface to form large surface aggregations. This stage may provide a dispersal mechanism for L. majuscula, enabling it to spread to other regions. The environmental consequences of L. majuscula blooms are still being investigated. Seagrass loss and altered marine plant community structure have been the most significant documented impacts of L. majuscula bloom events to date (Watkinson et al., in press). Economically, L. majuscula blooms within Moreton Bay have had significant impacts on both commercial fish catches (Dennison et al., 1999) and local communities through lost tourism and beach clean up of L. majuscula bloom material washed up on beaches. L. majuscula can also produce a suite of toxins which cause severe skin and eye irritation as well as asthma like symptoms in humans (Osborne et al., 2001). In general, marine plants within Moreton Bay are nitrogen limited (OÕDonohue and Dennison, 1997; Udy and Dennison, 1997). Nitrogen limited systems often favour prokaryotic nitrogen fixers such as cyanobacteria. In the absence of nitrogen limitation, phosphorus can be the limiting nutrient for cyanobacteria growth (Martin and Gordon, 1988) with blooms of cyanobacteria often related to phosphorus loadings from the surrounding environment (Riegman and Mur, 1986; Paerl et al., 1987; Seitzinger, 1991). However, where there is sufficient phosphorus available, biologically available iron often becomes a significant limiting factor of biological growth in oceanic systems (Martin and Gordon, 1988; Martin et al., 1990) as well as coastal and estuarine ecosystems (Hutchins and Bruland, 1998; Hutchins et al., 1998). Cyanobacteria have a high demand for iron (Paerl et al., 1994; Trick et al., 1995) and phosphorus (Paerl et al., 1987; Sanudo-Wilhelmy et al., 2001) for both photosynthesis and nitrogen fixation. Elevated iron concentrations in laboratory studies have: increased productivity and phycocyanin production in Oscillatoria tenius (Trick et al., 1995), increased nitrogen fixation in Trichodesmium sp. (Rueter et al., 1990) and increased toxin production by Microcystis aeruginosa (Utkilen and Gjolme, 1995). Iron is often limiting to marine organisms (Anderson and Morel, 1982), as insoluble ferric iron (Fe(III)) oxides and hydroxy oxides are the thermodynamically preferred forms of iron at seawater pH, with soluble free Fe(II) undergoing rapid oxidation and subsequent precipitation of the ferric form (Byrne and Kester, 1976). Cyanobacteria are unable to take up and utilize these oxides of iron directly. However, in the presence of organic ligands that complex with the soluble iron, oxidation and precipitation is generally decreased making iron more persistent in the dissolved phase in seawater, and hence more bio-available (Emmenegger et al., 1998; Santana-Casiano et al., 2000). Following reductive processes (e.g. photo-reduction) to break these organic
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ligand–iron complexes (Waite and Morel, 1984; Wells and Mayer, 1991; Voelker et al., 1997), phytoplankton and cyanobacteria are able to take up the soluble iron directly from the water column (Anderson and Morel, 1982). Therefore, the level of bio-available iron in seawater can fluctuate greatly depending on the presence of natural complexing agents such as organic carbon. Parallel studies investigating the role these organic rich compounds have as a transport mechanism for bioavailable iron to reach the bloom sites from terrestrial sources, are currently under way (Rose and Waite, 2003). The aim of the current study was to assess potential stimulating factors associated with L. majuscula blooms. Two case studies are presented, Deception Bay (NW Moreton Bay) and Hardy Reef (central Great Barrier Reef). Although there are many interactive factors in bloom development, this project sought to identify key processes that may help explain recent increases of this noxious cyanobacterium.
2. Methods 2.1. Study sites The two sites chosen for this study are geographically disparate (Figs. 1 and 2) with very different hydrology
Fig. 1. Location of ÔsignificantÕ observations of Lyngbya majuscula in coastal waters of Queensland, Australia over the last ten years.
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Despite the significant differences between the sites, both have experienced extensive blooms of L. majuscula over the past 5–10 years. 2.2. Deception bay case study
Fig. 2. Location of Lyngbya majuscula blooms in Moreton Bay over the last ten years.
and water quality, both have experienced blooms of L. majuscula. The first site is Deception Bay (2705 0 S, 15309 0 E), a relatively shallow region (
