BIOLOGICAL FINGERPRINTING OF VOLCANIC ERUPTIONS
Knowledge of the source of volcanic aerosols (gases, ash <1 µm diameter) or tephra found in ice or sediment cores may constrain the age of a sequence (e.g., Neall et al., 2008), its volcanic history (e.g., Donoghue et al., 2006), or meteorological (e.g., wind direction) conditions during the eruption (e.g., Narcisi et al., 2005). Geochemical fingerprinting is commonly used to link deposits to volcanoes or volcanic provinces, but Van Eaton et al. (2013, p. 1187 in this issue of Geology) suggest a novel, perhaps intuitively unlikely, tool for fingerprinting tephra: micropalaeontological analysis of ash layers. Frustules of diatoms (single-celled, eukaryotic microalgae with a siliceous skeleton) have been recognized in tephra before (Winsborough, 2000; Pearson et al., 2010), but never shown to have been spread by the eruption. Van Eaton et al. are the first to provide compelling evidence that lake diatoms in the 25,400-yr-old Oruanui tephra (New Zealand) were transported by the volcanic eruption plume. They collected most of their samples from terrestrial settings, so that diatom assemblages are absent or very different above and below the tephra, ruling out contamination. Further, the assemblage contains the diatom species Cyclostephanos novazeelandiae, said to occur only in lakes deeper than 10 m on New Zealand’s North Island, and which should be an unambiguous indicator of the source region for the tephra and environment for the eruption. However, C. novazeelandiae has also been described from streams in the western United States, although only at very low abundance (Blinn and Herbst, 2002), hence the ecology and taxonomy of this species needs further work.
Phreatomagmatic eruptions through lakes such as paleo-Lake Huka (Van Eaton et al.) may entrain diatom-rich sediments as well as living diatoms. Diatoms in the Oruanui tephra on Chatham Island, 850 km from its proposed source, belong to the same species assemblages as found in more proximal tephra, the first direct evidence that diatoms have been transported significant distances in eruption plumes. Diatoms are similar in size and density to volcanic ash, thus can remain air-borne over long distances. Marine diatoms in Greenland and central Antarctic ice cores have been transported by wind over hundreds of kilometers, and fossil lake diatoms from the Bodélé Depression in Africa have been collected on Barbados and in Florida (Harper and McKay, 2010). Micropalaeontological analysis thus could be useful in some specific tephra provenance studies, but is not likely to become routine: a phreatomagmatic eruption must occur through lake or ocean diatomites, and diatom assemblages must contain species endemic to a specific location, rather than the more likely cosmopolitan diatoms. However, a compelling case has now been made to pay attention to microfossils within tephras.
SURVIVING THE ERUPTION
The discovery of diatoms in tephras brought there in a volcanic eruption plume raises the question whether living diatoms could be dispersed through that process to colonise new areas. Aerobiology—the study of biological organisms in the atmosphere—is increasing in prominence with improved sampling and analytical methodologies that employ molecular genetic techniques (Kellogg and Griffin, 2006). Microorganisms brought into the atmosphere by storms, e.g., prokaryotes such as Alphaproteobacteria and Betaproteobacteria, may stay aloft and survive for several days in the troposphere, being transported thousands of kilometers (DeLeon-Rodriguez et al., 2013). Bacteria, Archaea and fungi are the dominant viable cells found in such studies, and viable diatom cells have not been seen, possibly due to the complexity of their cells relative to prokaryotes, and their lower tolerance to stress. Some diatoms in the 25,400-yr-old Oruanui tephra contain golden-brown organic matter, and Van Eaton et al. propose that diatom protoplasm might have survived the eruption (their figure DR3). This is provocative, but not conclusive evidence that the organic matter is derived from diatoms, which potentially could be tested through chlorophyll-derived biomarker analysis (e.g., Hodgson et al., 2003). The Oruanui tephra is 25,400 yr old, and if the organic matter can persist that long, it could have survived for thousands of years in the sediments beneath palaeo-Lake Huka. The presence of organic matter is thus not, per se, evidence that diatoms survived transport.
Could viable, vegetative diatom populations survive instantaneous heating during the eruption, near-instantaneous cooling/freezing in the high atmosphere, days or even months out of water away from their essential nutrients, and rapid increases in ultraviolet radiation? There is evidence on the survival of diatoms from culture experiments. Stauroneis anceps cells, dried slowly with >0.1 mm soil particles, were able to regenerate after 16 mo desiccation (Hostetter and Hoshaw, 1970), but eruption-associated desiccation would likely be rapid. Terrestrial and aquatic benthic diatom species were heated gradually or instantaneously to 40 °C, frozen or desiccated, but none of the 34 species studied survived desiccation, only three terrestrial species survived freezing, and abrupt heating was more lethal than gradual heating, with aquatic diatoms faring worse than terrestrial ones (Souffreau et al., 2010). Diatoms can survive if frozen fairly slowly at 1 °C/min, then kept in the dark for 48 h after re-warming (Buhmann et al., 2013), but instantaneous freezing caused significant cell death, and pigments were damaged without the dark recovery period (Buhmann et al., 2013). The effect of increased ultraviolet radiation (UVR) on diatoms is more complex. No photo-inhibitory effect was seen in benthic diatoms (Wulff et al., 2008), but increased UVR induced photo-inhibition in planktonic diatoms with decreasing temperature (Sobrino and Neale, 2007), photosynthetic benefits with increasing temperature (Halac et al., 2010), and some Southern Ocean marine diatoms have UV light–absorbing compounds (mycosporine-like amino acids, or MAAs) (Ingalls et al., 2010). Thus one could conclude, in general, that diatoms instantaneously heated in an eruption, then left for a significant amount of time up in the atmosphere, are not likely to survive, most probably due to the negative effects of desiccation.
Could diatoms survive transportation in a water-rich eruption plume, encased in protective coatings of water, ice, or fine ash (Van Eaton et al.)? These would shield them somewhat from UVR, and some diatom species can survive dark conditions (>1 yr) (e.g., Veuger and van Oevelen, 2011). Many diatoms, however, form physiologically-distinct resting spores to survive prolonged environmental stress, while their vegetative cells die. Diatoms in culture use intracellular nitrite to enter a resting stage, increasing cell survival for up to 28 weeks (Kamp et al., 2011), and despite cellular reorganization during periods of darkness, diatoms maintain the ability to photosynthesize, and rapidly recover once returned to the light (Nymark et al., 2013). But it takes a diatom hours to days to assimilate the silicic acid for synthesis of the silica wall of the resting spore, and to re-package the cell material, and no spores were indentified in the Oruanui tephra diatom assemblage.
VOLCANIC ERUPTION PLUMES AS VECTORS FOR BIOLOGICAL DISPERSAL
Vectors for passive dispersal of viable diatom cells over great distances include water currents, birds, wind and humans (Vanormelingen et al., 2008). It has been suggested that these vectors are successful because they protect diatoms from desiccation (Proctor, 1959). However, passive vectors might be unnecessary for dispersal, because small organisms including diatoms could be ubiquitous (Finlay et al., 2002). If the ubiquity hypothesis (Fenchel and Finlay, 2004) is correct, geographically restricted species do not exist, reducing the utility of entrained diatom populations for fingerprinting volcanic tephra deposits. Accidental introduction of diatoms via human vectors, however, and their subsequent proliferation (Edwards et al., 2001), is evidence that endemism does exist in diatoms (Vanormelingen et al., 2008). Molecular studies show cryptic species within cosmopolitan, morphologically indistinct diatoms, and related, yet distinct, clades within Pseudo-nitzschia pungens have geographically different distributions (Casteleyn et al., 2008). This raises the intriguing possibility of genetically testing living populations of the most abundant, geographically widespread diatom in the Oruanui tephra (Aulacoseira ambigua) for cryptic species. If they do exist, volcanic eruption plumes are not likely to have played a role in their dispersal, because the Southern Hemisphere westerly winds would have produced a genetically homogenous population. However, if populations of A. ambigua are indistinguishable, volcanic eruption might have acted as the dispersal vector. Van Eaton et al. thus present a provocative hypothesis on diatom dispersal, which can be evaluated by further studies.