JoAnn M. Burkholder, Director

Center for Applied Aquatic Ecology

North Carolina State University, Raleigh, NC 27606

Dinocysts: Lingulodinium machaerophorum, Spiniferites

(Rochon et al. 1999)

Ø Rise in atmospheric CO₂ levels – from ~280 ppm (pre-industrial) to ca. 360 ppm; levels in the troposphere are the highest in 130,000 years (IPCC). The airborne fraction is increasing and is expected to continue to increase at an accelerated rate.

Ø CFCs down but ozone depletion will continue for some time, along with increased UV – Chlorofluorocarbon use is decreasing, but ozone depletion over the Arctic is predicted (NASA) to be maximal from 2010-2019. Spring/summer ozone losses of 11-38% (60% in 1997, 1999) over the Arctic are resulting in flow of large masses of ozone-depleted air southward over Canada and much of the U.S. (up to –5% average change in the Gulf of Maine area), associated with significantly increased UV radiation.

Ø Sea level rise – Major ice pack melting from increased warming trend is causing a rise in sea level (> 0.5 m / 100 years may occur). Significant changes in shorelines and in stratification of coastal water masses are expected.

Ø Disproportionate warming expected in higher latitudes of the Northern Hemisphere would dampen seasonality, leading to more uniform temperature gradients between polar and tropical geographic regions. The resulting reduced atmospheric circulation would depress oceanic mixing and strengthen water-column stratification above the pyncocline.

Ø Significant increases in certain harmful dinoflagellates;

Ø Estuarine and coastal habitats, and present ‘cyst banks’ of harmful algae would lie at greater depths, depressing growth of some species; strengthened stratification generally would stimulate dinoflagellates; and inundation of coastal areas would increase available nutrient supplies, stimulating development of opportunistic algal species.

Based on this approach, some paleospecies such as Bitectatodinium tepikiense increased during cooler climate phases in the eastern North Atlantic, whereas others such as Impagidinium spp. increased during warm phases (Zippi 1992). Previous glacial-interglacial transitions were marked by (i) significant increases in dinoflagellate cyst concentrations, suggesting up to 1000-fold higher productivity; (ii) increased species diversity; (iii) replacement of sparse glacial-stage assemblages (dominated by Brigantedinium simplex) by rich subarctic to cool temperate assem-blages (with abundant Operculodinium centrocarpum, Nematosphaeropsis labyrinthus, and Spiniferites ramosus). Warming periods of the early Holocene were characterized by increased productivity and blooms of toxic algae (e.g., Alexandrium excavatum, Operculodinium centrocarpum, Spiniferites spp.), believed to have been related to a combination of increased nutrients and a greater stability of the water column because of meltwaters, high SST, and increased upwelling or storm activity (Levac 2001). Influxes of these taxa ranged from 50-1800 cysts cm^-2 yr^-1 (Mudie et al. 2001), suggesting that large toxic dinoflagellate blooms occurred at that time (Levac 2001). Late Cenozoic global cooling, in contrast, was associated with declines in species diversity and abundance during the late Pliocine (Géotop and Mudie 1992). Large fluctuations in dinocysts and

microfossils of a second group of algal flagellates, prasinophytes, have been interpreted to indi-cate that Pliocene surface currents were strongly affected by fluvial runoff and shoreward topo-graphic changes (Levac 2001). While there is evidence for declines in some potentially harmful dinoflagellate species during transition periods shifting toward warmer climatic conditions (e.g., Géotop and Mudie 1992), the strongest signals in the available data are for significant increases in dinoflagellates overall during warmer periods, including toxic blooms that apparently elevated oxygen levels in the surrounding environment.

Toxic dinoflagellate blooms have also been correlated with warming trends in climate change in other geographic regions. For example, at present Pyrodinium bahamense is confined to tropi-cal, mangrove-fringed coastal waters of the Atlantic and Indo-West Pacific extending south to Papua New Guinea. A survey of its paleocysts (Polysphaeridium zoharyi, with records dating back 50 million years to the Eocene) indicates that its range was much broader, extending as far south as Sydney Harbour during warmer periods in the Pleistocene (Hallegraeff 1993). There is concern that with increased present-day warming of the oceans, this species may return to Australian waters. This premise is supported by strong correlation between P. bahamense blooms and ENSO events (e.g., Maclean 1989). Other work in coastal waters of Scandinavia has indicated that toxic Dinophysis species develop higher densities in association with positive oscillations of the North Atlantic Oscillation (Belgrano et al. 1999). Also in that region, Dale and Nordberg (1993) documented evidence for blooms of the toxic dinoflagellate, Gymnodinium catenatum beginning about 2000 yr B.P., in relation to a warming trend in climate change.

The rise in sea level would result in deeper deposits of present-day cyst banks of harmful algae, depressing growth of some species. However, development of strengthened stratification in subarctic areas under warming trends in climate change generally would stimulate dinoflagel-lates, many of which migrate during dark periods down to depths where water-column nutrient; supplies are more abundant. Inundation of coastal areas would increase available nutrient supplies, expected to stimulate opportunistic algal species.

Ø Increased productivity and, for some species, increased populations;

Ø UV inhibition of phototactic and photophobic responses, decreased photorepair ability; also in some species, decreased mobility and decreased survival; and inhibition of various grazers.

Both elevated CO₂ and elevated UV significantly affect algal productivity. Laboratory and field research of algal mats and phytoplankton cultures under ambient vs. increased pCO₂ have demonstrated, as expected, that increased inorganic carbon (C_i) promote increased photosynthe-sis and, for some species, increased population density (Rothschild 1997). Concomitant increases in excretion of fixed carbon may enhance bacterial productivity. Such stimulatory effects would be offset by negative impacts of increased UVB radiation. Polar diatom species have shown a wide response to UV exposure but, in general, smaller cells with higher surface area : volume ratios sustained more damage per unit DNA (Antarctic; Karentz et al. 1991). UV radiation also can inhibit nitrogen metabolism (Behrenfeld et al. 1995), ATPases, cytochrome oxidase, and other important enzymes in cell functioning. Interestingly, among the algae, dinoflagellates and cyanobacteria have highly efficient mechanisms to screen out UV (350-450 nm range).

While some interesting trends have been described for Pacific Coast micrograzers, such data are not available for the North Atlantic, so indirect impacts on phytoplankton from changes in higher trophic levels remain poorly understood.

On the basis of compelling historic data for the North Atlantic, supported by limited experimental information, warming trends in climate and accompanying factors (increased UV, dampened temperature differences latitudinally and strengthened stratification, rise in sea level, increased CO₂) likely will stimulate some harmful algal species, especially certain toxic dinoflagellates.

Although warming trends have occurred previously in the geological record, a major difference between past and present conditions is the present-day influence of dense human coastal popula-tion growth. Water quality declines in populated coastal areas have been strongly correlated with poorly treated major quantities of sewage, poorly regulated and abundant hazardous wastes, and high sedimentation from development and up-estuary activities. Given that certain algal species thrive in degraded conditions (e.g., in New England waters, the haptophyte Phaeocystis), the "human factor" would be expected to enhance growth of such species.

Behrenfeld, M.J., D.R.S. Lean and H. Lee (1995) Ultraviolet-B radiation effects on inorganic nitrogen uptake by natural assemblages of oceanic plankton. Journal of Phycology 31:25-36.

Belgrano, A., O. Lindahl and Bodil Hernroth (1999) North Atlantic Oscillation primary produc-tivity and toxic phytoplankton in the Gullmar Fjord, Sweden (198501996). Proceedings of the Royal Society of London (B) 266:425-430.

Dale, B. and K. Nordberg (1993) Possible environmental factors regulating prehistoric and historic "blooms of the toxic dinoflagellate Gymnodinium catenatum in the Kattegat-Skagerrak region of Scandinavia, pp. 53-57. In: Toxic Phytoplankton Blooms in the Sea, by T.J. Smayda and Y. Shimizu (eds.). Elsevier Science Publishers B.V., Amsterdam.

Edwards, L.E. and V.A.S. Andrle (1992) Distribution of selected dinoflagellate cysts in modern marine sediments, pp. 259-288. In: Neogene and Quaternary Dinoflagellate Cysts and Acritarchs, by M.J. Head and J.H. Wrenn (eds.). American Association of Stratigraphic Palynologists Foundation, Dallas.

Hallegraeff, G.M. (1993) A review of harmful algal blooms and their apparent global increase. Phycologia 32:79-99.

Géotop, A. de V. and P.J. Mudie (1992) Pliocene and Quaternary dinoflagellate cyst stratigraphy in the Labrador Sea: Paleoenvironmental implications, pp. 329-346. In: Neogene and Quaternary Dinoflagellate Cysts and Acritarchs, by M.J. Head and J.H. Wrenn (eds.). American Association of Stratigraphic Palynologists Foundation, Dallas.

Karentz, D., J.E. Cleaver and D.L. Mitchell (1991) Cell survival characteristics and molecular responses of Antarctic phytoplankton to ultraviolet-B radiation. Journal of Phycology 27:326-341.

Levac, E. (2001) High resolution Holocene palynological record from the Scotian shelf. Marine Micropaleontology 43:179-197.

Maclean, J.L. (1989) Indo-Pacific red tides, 1985-1988. Marine Pollution Bulletin 20:304-310.

Mudie, P.J., A. Rochon & E. Levac (2001) Palynological records of red tides in Canada: past trends and implications for the future. Palaeogeography, Palaeoclimatology, Palaeo-ecology.

Rachon, A., A. De Vernal, J.L. Turon, J. Matthiessen and M.J. Head (1999) Distribution of Recent Dinoflagellate Cysts in Surface Sediments from the North Atlantic Ocean and Adjacent Seas in Relation to Sea Surface Parameters. American Association of Stratigraphic Palynologists Contribution Series Number 35. AASP, Dallas, 152 pp.

Rothschild, L.J. 1998. Will global change affect planktonic productivity?, pp. 1563-1575. In: California and the World Ocean ’97.

Zippi, P.A. (1992) Dinoflagellate cyst stratigraphy and climate fluctuations in the eastern North Atlantic during the last 150,000 years, pp.55-65. In: Neogene and Quaternary Dinoflagel-late Cysts and Acritarchs, by M.J. Head and J.H. Wrenn (eds.). American Association of Stratigraphic Palynologists Foundation, Dallas.