Note to Limnology and Oceanography Cryptic blooms: Are thin layers the missing connection? Margaret A. McManus1,*, Mary W. Silver2, Raphael M Kudela2, Percy L. Donaghay3 1University of Hawaii at Manoa Department of Oceanography Honolulu, Hawaii 96822 (808) 956-8623 phone, (808) 956-9225 fax [email protected] (*formerly Dekshenieks) 2University of California at Santa Cruz Ocean Sciences Department Santa Cruz, California 95064 3University of Rhode Island Graduate School of Oceanography Narragansett, RI 02882 17 September 2004 Running Head: Cryptic Blooms and Thin Layers Acknowledgments We thank Mark Carr, Olivia Cheriton, Jim Eckman, Patrick McEnaney, Jennifer Miksis, Pete Raimondi, Jan Rines, Curt Storlazzi, Grieg Steward, Jim Sullivan and Andrea VanderWoude. Special thanks to Jamie Grover (Captain of the RV Paragon), Jared Figurski and Jan Friewald (Diving support). This work is supported by: The Office of Naval Research Physical Oceanography award N00014-01-1-0206 (MM); The Partnership for Interdisciplinary Studies of Coastal Oceans-A long term ecological consortium funded by the David and Lucile Packard Foundation (MM); the National Science Foundation and the ECOHAB program award OCE- 0138544 (RMK); and the Office of Naval Research Biological & Chemical Oceanography award N00014-95-0225 (PLD). We are grateful for this support. 2 Introduction Monterey Bay, located on the central coast of California, is classified as one of the largest National Marine Sanctuaries in the United States. The bay is highly productive and economically important in terms of both fishing and tourism and it has been identified as a key Harmful Algal Bloom (HAB) monitoring site and “hot spot” for the West Coast (Scholin et al. 2000; Trainer et al. 2000). Monterey Bay exhibits a wide dynamic range of oceanographic conditions, from vigorous diatom-dominated upwelling to warm, nutrient-depleted oceanic conditions dominated by picoplankton (e.g. Pennington and Chavez 2000). This is one of the most extensively characterized regions in the United States in terms of basic biological and physical oceanographic processes. Despite this wealth of information, HAB events in Monterey Bay are not easily predicted (Kudela et al. in press). Unfortunately, the majority of HAB events are first detected by the presence of sick or dying animals. This has led to the phrase “cryptic blooms” to denote the sudden onset of toxic events with no immediately apparent large phytoplankton bloom (Scholin pers. comm.). We suggest that the onset of HAB events goes undetected because many HAB species are distributed in discrete ‘thin layers’ in the water column. These ‘thin layers’ range in vertical thickness from 10 centimeters to 3 meters, may extend horizontally for kilometers and may persist for days. They have been shown to be temporally and spatially persistent, and undetectable from remote sensing or by traditional coarse resolution vertical sampling (Dekshenieks et al. 2001; Alldredge et al. 2002; Rines et al. 2002). They are characterized by in-layer concentrations of planktonic organisms that can be orders of magnitude greater than the densities just above or below the structure (McManus et al. 2003). Observations of Thin Layers in Monterey Bay We deployed an autonomous profiler at a 22 m site in northern Monterey Bay in August 2002 and collected a time series of 178 hourly, finescale profiles of temperature, salinity, density, spectral absorption and attenuation (at 9 wavelengths), 150o backscatter at 532 nm, chlorophyll fluorescence, bioluminescence, and oxygen concentration. The data from the autonomous profiler were telemetered to shore, processed in near real-time, and visualized so we could follow the development of thin layers in the system. This finescale sampling revealed the existence of 3 intense thin phytoplankton layers in Monterey Bay. These sub-surface layers measured from 10 cm to 3 m in thickness and persisted on timescales of days. These layers are too thin to be adequately resolved by conventional sampling techniques and thus have often gone undetected despite extensive work in this system. For example, an intense thin layer formed at a density interface in the water column and persisted for 6 days (from 7 August to 13 August 2002). This thin layer increased in intensity by orders of magnitude from an initial absorption value of 0.7 m-1 -1 (ap440) on 7 August to extremely high values of 7 m on 10 August (Figure 1). On 13 August 2002, divers took water samples from above, within and below the persistent thin layer. Counts of phytoplankton, bacteria and cyanobacteria revealed that concentrations of organisms in the layer were 3 to 5 times higher than those above or below the layer (Table 1). In addition, the phytoplankton assemblage was primarily composed of a multi-species assemblage of Pseudo-nitzschia (mostly non-toxic members of the genus), with smaller numbers of the toxic P. australis. In a separate study, during summer 2000 as part of the MBARI MUSE program, observations were made of high concentrations of competent Pseudo-nitzschia in layers at depths below the euphotic zone (Ryan et al. in press). Although noted, no attempt was made to characterize these populations other than identifying their existence; however, Ryan et al. (in press) speculated that the identified layer of Pseudo-nitzschia may have been associated in this layer as either a refugia or as an optimal location for acquiring resuspended iron, a potential trigger for toxin production (Rue and Bruland 2001). Evolutionarily, a possible benefit for concentration of HAB species into thin layers may be relief from grazing pressure. Turner and Tester (1997) noted that some zooplankton grazers may cease feeding and starve rather than consume toxic algae, or they may show sub-lethal effects, changing their behavior or reducing grazing. Zooplankton have also been observed to avoid layers with high concentrations of toxic phytoplankton (Holliday pers. comm.). In addition, we have found that high concentrations of dissolved domoic acid (dDA), the water-soluble phycotoxin produced and released by some species of the diatom Pseudo-nitzschia (see review by Bates 1998), causes krill to cease feeding (Bargu pers. comm.). 4 Monterey Bay Toxic Algae Monterey Bay is well known as a site where both blooms of toxic phytoplankton occur and where shellfish closures and animal deaths are results of the presence of their toxins. A well- publicized outbreak of shellfish poisoning in 1927, which occurred along the roughly 100 miles of coastline between Monterey and San Francisco, led to the discovery that phytoplankton can produce toxins and that shellfish can vector the toxins to humans (Sommer et al. 1937). The responsible species, a dinoflagellate now renamed Alexandrium catenella, was the source of the neurotoxin, saxitoxin, which caused the 1927 paralytic shellfish poisoning (PSP) event. Saxitoxin, however, is not the only phycotoxin present on the California coast. In 1991 the deaths of numerous seabirds in Monterey Bay led to the recognition of the presence of domoic acid (DA). Domoic acid, a neurotoxin that causes amnesic shellfish poisoning (ASP) in humans, is produced by species of the diatom Pseudo-nitzschia (Work et al. 1993). Since DA targets receptors in the nervous system common to many vertebrates, this event signaled a new coastal threat to human health. DA-related deaths and exposures of a wide range of marine organisms have been well documented in Monterey Bay and at other coastal sites in California. These DA- events include kills of the California sea lion Zalophus californianus (e.g. Scholin et al. 2000), and exposure of large baleen whales including humpback and blue whales (Lefebvre et al. 2002a). The vectors of DA to the vertebrate predators appear to be zooplankton such as krill, and schooling fish, especially the northern anchovy Engraulis mordax (Bargu and Silver 2003, Lefebvre et al. 2002b). Okadaic acid (OA) is a third toxin that was recently discovered in Monterey Bay water samples. These water samples were dominated by Dinophysis acuminata (Weber 2000). D. acuminata is a species known to produce OA in other coastal regions. This toxin is less likely to be noticed than saxitoxin or domoic acid, because it produces diarrhetic shellfish poisoning, a non-lethal syndrome that produces gastrointestinal symptoms common to numerous other food-borne illnesses. The densities of D. acuminata and other known OA producers are sufficiently high to 5 suggest that toxin may be a threat, if cell densities are sufficiently high in areas where shellfish are taken by humans (Weber 2000). Observations of Thin Layers in other Coastal Regions Thin layers have been identified as a recurrent feature in a variety of coastal systems including Monterey Bay (Bjornsen and Nielsen 1991; Donaghay et al. 1992; Johnson et al. 1995; Cowles et al. 1998; Montagnes et al. 1999; Rines et al. 2002; McManus et al. 2003; Koukaras and Nikolaidis 2004). Recently, there have been observations of toxic and potentially toxic algae in these thin layer structures (Donaghay et al. 2000, Rines et al. 2002, Koukaras and Nikolaidis 2004). Observations were made of the distribution of Pseudo-nitzschia taxa in a fjord in the San Juan Islands between May 21 and 31, 1996. Rines et al. (2002) observed persistent, subsurface, thin layers located at the pycnocline. Three species of Pseudo-nitzscha were identified from this study. The dominant species observed was P. fraudulenta, there were lower numbers of P. pungens, and P. pseudodelicatissima was observed living in close association with Chaetoceros socialis colonies. Although there have been no recorded outbreaks of domoic acid in the fjord, P. fradulenta has the potential to produce domoic acid. Thin layers of Pseudo-nitzschia spp. could easily escape detection by routine monitoring procedures, and could be a potential source of unexplained toxicity events in other areas of the San Juan Islands (Rines et al. 2002). The first documented Dinophysis bloom from Greek coastal waters associated with a diarrhetic shellfish toxin outbreak was recorded in January of 2000 (Koukaras and Nikolaidis 2004).