By Ron Shimek with illustrations by Jan Kocian

Introduction

Over the past many years when I have spoken to many aquarists, students, and other audiences about modern and ancient biology, one of the implicit themes for my discussions has been the ubiquity of death as a biological factor.  This may seem odd, for after all, the word “Biology” is defined as the study of life.  Nevertheless, it has many times been noted that “death” is the price we pay for being alive.  Death is the reason for evolution, the less-fit die… leaving those animals that are more fit.

The ways in which organisms perish may run the gamut from the singular, everyday, ultra-mundane and almost meaningless death – meaningless except, of course, to the creature involved, which leaves the world much as it was before; to being a minor part of a huge array of dying, referred to as “a mass extinction event” that may radically change the world’s remaining array of living creatures.

In our explorations of the natural world, we often see – and often are the cause – of the timely or untimely end of some creatures.  Sometimes these events are welcome, such as the delightful revenge swat terminating the existence of a female mosquito while she is trying to procure a blood meal for the development of her eggs.  More often, the events are essentially inconsequential; such as the perishing of innumerable members of the aerial insect plankton as they impact with the teeth of innumerable smiling, speeding motorcyclists.   And some deaths are apparently meaningless, and perhaps all the more tragic for that, as the many organisms that perish over a large area for no apparent reason other than bad luck, when nature serves up a plate of natural disaster, such as the unimaginably humongous volcanic eruptions of the Siberian traps of about 251 mllion years ago; eruptions that nearly brought multicellular life to an end, or the somewhat lesser, but much faster, and probably much more visually exciting, cosmic Croquet crash of 65 million years ago that left only the birds as living dinosaurs.

At the other end of the scale are the more local extinctions that impact every ecosystem now and then, or periodically.  Such local extinctions range from the drying up of a mud puddle, which may have thriving populations of many microbes, to the death and destruction wrought upon many suburban monocultural grassy meadows when they are mowed weekly in the summer, to the massive death and destruction in the clear cutting of a forest, finally to those much more serious events in marine ecosystems referred to as “Dead Zones”.

Dead zones are just what the name implies, areas where life is lacking, either permanently or on some sort of transitory scale.   The largest dead zones are in enclosed oceanic basins where the bottom is permanently anoxic and the waters are full of sulfides.  Given the name of “Euxenic zones” because the largest such is found in the bottom of the basin containing the Euxenic ( = Black) Sea, these areas are totally devoid of aerobic life, although they generally have thriving communities of anoxic bacteria and archaea.  Euxenic zones are generally permanent.  However, there are many types of transient dead zones.

Short-Term Marine Dead Zones

Some of the more “classic” of marine dead zones were characteristically of short duration and caused by the superimposition of several physical events coupled with some unfortunate biological events.

Commonly referred to as “red tides”, these events occur regularly along many shorelines, and although the resulting mortality events tend to look the same from above the water’s surface, the causes are often different from place-to-place and are quite often difficult to determine.  In the dim, dark, ancient days of legend and mythos when I was but a mere studentling, I took a class from an esteemed, exalted and venerated professor of classical rank whose words, like those of the acclaimed Aristotle in the not too distant past, were absolutely unquestioned.   Although his reputation has faded somewhat as times have passed, many of his studies remain classics from the founding days of population ecology.  About the time of my birth, he was one of the first researchers to hypothesize a cause for red tides that appeared to be reasonable and met the test of experimental validation.

However, almost 20 years later, while taking a course at the Marine Biological Laboratory in Woods Hole, Massachusetts, I listened to him characterize his search for the cause of red tides in Florida, as a search looking for some event or factor that wasn’t there, which he realized should be easy to find as it wasn’t there in large quantities.  So all one had to do to find the cause of these red tides was to evaluate the ecosystem in question and then find was what was missing in the largest quantities from that ecosystem.  That, in turn, would lead you to the yellow brick road, and eventually to the answer you were seeking (Slobodkin, 1953).  As an aside, this fellow’s lectures were all suffused with similar logic.  It made taking notes and subsequently rereading those notes to try to understand what had been said in the lecture a real joy, and we students were universally glad that this class was graded on a simple credit/no credit system.   Basically, if you showed up for the class, you got credit.  Ah… Sigh….

Red tides may or may not have a primary human cause or may simply, and misleadingly, appear to have such a cause.   When a dead zone appears in close proximity to a metropolitan area, or a source of agricultural runoff, probably the first cause of the event is considered to be some sort of pollution; and this is justifiably so.  However, in all such cases, the actual cause of the event needs to be examined much as a forensic examination needs to be done in the case of a criminal investigation.   And just as the forensic examinations portrayed in television “dramas” are only tangent to reality, the biological forensic examinations of a marine “event” are very different than what is thought to occur by even the well-educated public.  Probably the biggest difference is the speed by which things don’t occur.  Many of the necessary examinations require a great deal of time and painstakingly detailed work to reach a result.  For even a small and simple event, it may take from weeks to months to analyze samples and get definitive results.  Nevertheless, the process is an interesting and quite amazing one.

Right NOW!!!

Presently, several different investigations of biological problems are being investigated in virtually every major estuary in the United States, including the Puget Sound of the Pacific Northwest.   These include, in no particular order, studies of changes occurring due to global climate change; studies investigating the effects of introduced species, particularly with regard to their effects on native species that are important in commercial and sports fisheries; studies examining the natural history of ecologically important species, such as, in Puget Sound, all the species of salmon, as well as other fishes and various crustaceans such as Dungeness crabs, and important mollusks such as geoducs, and of course, marine mammals such as killer whales, and sea lions.  Also, there is an emergency study or series of studies trying to get some sort of handle on the immense mortality that is presently being seen in many sea star species along the entire West coast of the U. S. and Canada.

Jan Kocian, diving photographer extraordinare, and my co-author for this blog, has been actively surveying several marine subtidal areas in northern Puget Sound for some time, with the objective of obtaining photographic evidence of, particularly, the sea-star wasting disease epidemic.  As is often the case in a study such as this, serendipity will rear its head, and wholly unexpected observations will be made.

Figure 1.  The habitat in a typical, “healthy” and normal view is shown at the bottom.  The dying or dead brittle stars are coming out of the habitat, probably to avoid the anoxia that occurred in the sediments.

On 18 September, 2014, Jan had just finished his weekly survey dive at the wharf at Coupeville on Whidbey Island, Washington.  He reported that “The many mottled sea stars (Evasterias trochellii) which until recently escaped the wasting disease now were now gone, having died off, and those few survivors didn’t look all that healthy, either”.  Leaving his normal survey area near the pier, looking for better water clarity, he started seeing things he had never previously observed.  At depths from about 7.5 m  to 9 m ( about 25 feet to about 30 feet), there were many animals lying exposed on the sandy sea floor, looking limp, sick or dead.  Red sea cucumbers (Cucumaria minata) were flaccid and dead, while several Aleutian Moon snails (Cryptonatica aleutica) were in odd postures.  Proceeding a bit further, brittle stars, which had always been buried deep in the sediments showing only their arms waving in the light current, had crawled out of the sediments and were lying wholly exposed all over the surface of the muck, showing their entire bodies.  A few were even uplifted as if they were starting to spawn.  In the midst of the stars were some pink/yellow worms, another rare or unusual sight.  These worms were Polycirrids, a group recently split off from the Terebellids.  Also dozens and dozens of Nuttall’s cockles (Clinocardium nuttallii) were on the sediment surface with their siphons out, instead of being buried as they normally are.  

Figure 2. Stressed or dying cockles. The black layer seen on some of the cockles indicates that their normal habitat is aerobic only near the surface, and anaerobic deeper in the sediment. It is likely that the anaerobic conditions became more pronounced and caused this dying zone.

Figure 3. Death of the sea urchins and brittle stars.

Figure 4. Cucumaria miniata dying and decomposing.

Figure 5. Dead, dead, dead, and dead – or dying

Returning to the site two days later, on the 20^th of September, to survey the site and to do some wide angle photography he found the impacted area was now covered with a layer of cloudy or milky water.  Water clarity was reduced to only a few feet which rendered wide angle photography difficult.  After examining the site, with regard to the extent of the dead zone, it appeared that depth didn’t seem to be a critical factor, at least on the shallow side of the site and topography didn’t seem to have enough differences to cause the changes, either.

On a return to the site on 22^nd September, the area containing dying animals was not only still present it was spreading; whatever seemed to be the cause was still doing its dirty work.  Documenting the milky water was difficult, as the layer was not particularly well defined, nevertheless, there was a lot of flocculent material floating in it.  The sites he had previously photographed were now wholly within “the Milky Way” which made photography difficult.  However, outside the cloudy water, the many tube dwelling worms in the area’s sediments were apparently unaffected.   The milky water appeared to be created from within the sediments.  The water was not cloudy like this when he first found all the infaunal creatures on the surface.

Figure 6. Milky water layer with flocculent material, probably due to decomposition byproducts.

Figure 7. The white and black condition of the sand is due to the decomposition of all the infaunal animals that came up from the sediments and died on the sediment surface. The white is a characteristic bacterial genus named Beggiatoa. It has several species that metabolize hydrogen sulfide and decomposing critters.

Figure 8. The aftermath. Sulfur bacterial mats formed by metabolizing decomposing animals in the sediment.

Three days after this, on 25^th September, upon returning to the site, conditions had changed considerably.  The milky water layer was gone, although there still was flocculent material in the water.  Strong winds in the previous couple of days appear to have blown the milky, possibly stagnant, water mass away or mixed it with cleaner offshore water.  The brittle stars on the surface were gone, possibly blown away in currents,  although there were some arms waving above the sediments, indicative of a few stars still living below the surface.  Whether these were the same stars that had been on the surface or others that had remained below the surface is unknown.  The clams were not visible on the surface, but the horse clam siphons were visible in their normal postures.  Most other animals, such as the worms, were no longer visible on the surface.  The exceptions were the red sea cucumbers, Cucumeria miniata, where many specimens were lying fully exposed, and apparently dead, on the surface.  As their tissues contain a lot of toxic saponins, scavengers tend to leave these dead Cucumaria miniata alone.  It may take several weeks for their bodies to slowly decompose.

Jan continued his regular dives on the 29^th of September.  While visibility in shallow water was still good, upon entering the area of the dead zone, the visibility was much worse than in the surrounding area, but the water was not milky.  A few living Cucumaria were acting oddly, not quite dead, but just slightly responsive to touch.  The horse clams buried in the sediment were extending their siphons and apparently feeding.  These could have been clams that had not extended their siphons through the event and finally tried feeding again, or they could have been clams that had been on the surface and subsequently reburied.  Some more brittle stars were found on the surface, many with autotomized arms.  Numerous green sea urchins were found with their spines in abnormal postures, definitely not looking healthy.

At this time, Jan was not looking too healthy either, having caught a cold.  He was unable to return to diving until the 12^th of October.  When he could return to the site, in shallow water, it appeared that all was back to normal, the Cucumaria miniata was feeding as usual and the brittle stars were extending their arms from the sediments apparently feeding normally.  However, the water clarity was poor; only about 1.1m to 1.5m (four to five feet).

Figure 9. The white bacteria are about the only thing that will decompose the sea cucumbers, because of the toxic chemicals in their body walls.

Dropping down to 40 feet (12 m) the seabed was black instead of its usual grey-brown, and it was covered with a white bacterial mat.  This white mat is often referred to as Beggioatoa, which is a bacterial genus that is found in hydrogen sulfide rich environments.  It is a typical pollution marker for areas that have been rendered anoxic, killing much of the infauna.  Typically in areas such as these, the environment will be aerobic during the day, due to algal photosynthesis, but because of the amount of organic matter in sediments, once the sun goes down, so does the oxygen concentration and the sediments become anaerobic or anoxic.

Over the next week, on dives until the 19^th of October, the dead zone appeared to be evident.  The full extent of the dead area, and the reason for the mortality, remain indeterminate.  Typically in Puget Sound, the benthos is very rich, so that a mortality event such as this may take several months for even partial recovery.  Although the substrate will appear to recover in a few months, quantitative sampling will show the benthos make take two or more years before it has returned to normal.

References:

de Matos Nogueira, J. M., Fitzhugh, K., & Hutchings, P. 2013. The continuing challenge of phylogenetic relationships in Terebelliformia (Annelida: Polychaeta). Invertebrate Systematics, 27(2), 186-238.

Long, E. R., Dutch, M., Aasen, S., Welch, K., & Hameedi, M. J. (2005). Spatial extent of degraded sediment quality in Puget Sound (Washington State, USA) based upon measures of the sediment quality triad. Environmental monitoring and assessment, 111(1-3), 173-222.

Shimek, R. L. 1992. North Beach High Intertidal Biota in the Area of Proposed Beach Modifications: Sediment Infauna and Beach-Wrack or Drift Biota. Pages 1-67. Parametrix, Inc., Seattle. Shimek, R. L., T. Thompson, and D. Weitkamp.  1991. Slag, benthos, and bioassays: poor correlation of bioassay predictions and the benthos. In:  Chapman, P., F. Bishay, E. Power, K. Hall, L. Harding, D. McLeay, M. Nassichuk and W. Knapp (Eds.)  Proceedings of the seventeenth annual aquatic toxicity workshop, November 5-7, 1990, Vancouver, B. C.  Canadian Technical Report of Fisheries and Aquatic Sciences. No. 1774. Vol. 2:1046.

Shimek, R. L., T. A. Thompson, T. H. Schadt, and D. E. Weitkamp.  1992.  Interpreting conflicting biological and chemical results from a Puget Sound sediment data set.  Puget Sound Water Quality Authority. Puget Sound Research ’91, Proceedings. 2:546-552.

Slobodkin, L. B. 1953.  A possible initial condition for red tides on the coast of Florida. Journal of Marine Research, 12(1): 148-155.