by Thomas Höpner and Gerd Meurs

Early summer 1996: So-called black spots are registered in the mudflats off the German coast, which are increasingly spreading into huge areas. While some diagnose a dying mudflat as a result of environmental pollution, others speak of weather-related, temporary phenomena. The Wadden Sea Ecosystem Research Centre has been investigating the black spots in experimental simulations for seven years. Conclusion: Decades of high nutrient supply have led to a localised accumulation of organic material in the mudflats, which can lead to the complete consumption of oxygen during decomposition. A chain of unusual events can lead to the widespread occurrence of black spots or black areas.

The crisis. Wadden Sea guides, environmental associations, the National Park administration, the Lower Saxony State Office for Ecology and Wadden Sea ecosystem research were never more in agreement than in the first half of June 1996. Whatever the state of the East Frisian Wadden Sea (especially south of Baltrum) was called - overturned, black patch, catastrophe: what experts never wanted to completely rule out as an extreme consequence of over-fertilisation and overexploitation had occurred, but at the same time considered it unlikely: The black spots (the abbreviated name of the warning signal processed by the ecosystem research team) had become the black areas (the unfortunately appropriate and quick term coined by the national park administration). Whereas in previous years the former reached 0.1 % of the dry areas at most, on 12 June it was up to 20 %, according to estimates by the Lower Saxony State Office for Ecology following aerial surveys. Tidal creeks carried black water. Hydrogen sulphide reached toxic concentrations in the pore water and surface water. Residual water on the mudflats had an oxygen deficit everywhere. There was a mass mortality of lugworms and mussels, and this after the cockle losses of the ice winter. The peak was reached on 12 June. From the 13th, strong winds and falling temperatures alleviated the visual phenomena without achieving a fundamental improvement.

This is what happened in the seventh and, as planned, final year of ecosystem research (ÖSF) in the Wadden Sea of Lower Saxony, in which seven of 30 working groups worked on the "black spots" complex of questions, sedimentologically, sediment-chemically, microbiologically and zoologically.

Quote: "Some observers have the subjective impression that the anaerobic sediment area is expanding at the expense of the aerobic sediment area, even reaching the surface of the tidal flat sediment in small areas at individual locations (surprising due to the absence of localised pollution). This would be the first predictable consequence of the "eutrophication" that has been convincingly documented for the North Sea.

This was the extremely cautious formulation in 1988 in the ÖSF's "Programme Concept" (ARSU GmbH. UBA-Texte 11/89). It was clairvoyant to a certain extent, and it was fortunate (from the researcher's point of view), because the black spots have since increased on the main ÖSF study areas. Nature showed how they came about. Macroalgae (another eutrophication phenomenon) were clumped together by waves and currents and buried in the sediment. Other triggers were dead sand clams. The biodegradation consumed the oxygen so quickly that it could not be replenished from the surface. It was replaced by the seawater component sulphate, which was reduced to sulphide. This, together with iron ions, produced the black colour. The colour was an indicator of the absence of oxygen. When the colour appeared on the surface, it indicated the absence of oxygen and the presence of sulphide. This made the surface hostile to life.

Observed in this way, the phenomenon became accessible to experimental simulation. It was easy to create black spots by burying algal biomass (and other biogenic degradable material) and it had become easier to study them (Höpner, Th. & Michaelis, H., Sogenannte Schwarze Flecken: ein Eutrophierungssymptom des Wattenmeeres. In: J. L. Lozán et al. (eds.). Warning signals from the Wadden Sea. Blackwell Wissenschaftsverlag Berlin. S. 153-159, 1994).

The condition that the signal warned of was the overloading of the sediment's capacity to break down biomass. The overload was caused by an oversupply of biomass, i.e. a phenomenon of eutrophication. The signal was suitable as such because it was easy to observe. It was equally suitable as a warning signal and as an object of research because it had a lifespan of weeks or months. It was reliable, because it was nothing other than the biological damage itself, but still on the smallest surface and directly surrounded by biologically and chemically healthy sediment. It allowed an investigation before it developed into ecological damage. Since the end of the ice winter, it has indicated a critical approach to large-scale overload. However, this was not enough for a concrete crisis warning. But when the crisis materialised, we knew what it was.

The decomposition of organic material is a natural function of the tidal flat sediments in the material cycles of the coastal sea. Organic material is produced locally ("autochthonous") by the growth of bacteria, algae, plants (seagrass is unfortunately negligible) and bottom animals, or it comes from the offshore sea area ("allochthonous") with tides, currents and wind. It is incorporated into the sediment through physical rearrangement and burrowing by bottom animals (bioturbation). Near the surface, decomposition takes place under oxygen consumption, at depth mainly under consumption of sulphate, one of the main components of seawater. As long as the degradation capacity is not overloaded, a balance is established, recognisable by a "redox horizon" at a depth of a few centimetres or sometimes only a few millimetres in the case of silt sediments. It separates the deeper black oxygen-free (anaerobic) sediment from the overlying light-coloured oxic sediment layer. The position of the redox horizon is significantly influenced by bioturbation, as this is the most important transport route for oxygen to the depths. Sulphide (hydrogen sulphide), which is formed in the anaerobic sediment, is oxidised back to sulphate in the oxic (aerobic) layer, so that the bottom animals dependent on oxygen from the surface are protected from the toxic sulphide (for these processes see Th. Höpner, Das Wattsediment als biochemisches Reaktionsmedium, EINBLICKE 7, 8-12 (1988).

The black spot is "nothing other" than the absence of the oxic sediment layer and the appearance of black anaerobic sediment on the surface. For this to happen, not only must the degradation capacity be overloaded, but bioturbation must also disappear. The two are connected, because no organism can live in the black spot except bacteria, which carry out fermentation and steps of sulphur metabolism and methane formation.

In the following, the algae biomass shall be the model load. It has the approximate (molar) composition 450 C : 45 N : 1 P (I. Kellner). The load (based on dry biomass) derived from natural processes was 3 kg per square metre in a 5 cm layer at a depth of 10 to 15 cm. The material changes in the sediment were mainly observed as changes in the concentration of dissolved substances in the pore water. It was not only a question of the fate of the algae components, but also of those sediment components that were dissolved under the influence of the altered chemistry. Many collaborators were involved, mostly in the form of Diplom and doctoral theses. Their names are mentioned in each case.

Organic carbon. The decomposition of algal biomass begins with the breakdown of its macromolecules into small soluble intermediate products, which are found as DOC (dissolved organic carbon) in the pore water. In the pore water of an uncontaminated sediment there is at most 20 mg/l DOC (E. Koke). In a polluted sediment it can be 800 mg/l DOC (I. Kellner), in laboratory microcosms even 4,000 mg/l DOC (M. Robak). Acetic acid makes up 60 % of the carbon (M. Oetken, C. Riemer), the rest is distributed among many amino acids, sugars, etc. (M. Robak). It is the DOC components that are used by the sulphate-reducing bacteria and are oxidised to carbon dioxide in the process. Acetic acid and others are also precursors of methane.

Nitrogen. The algae nitrogen is released as ammonium and reaches 600 µMol/l in the pore water (I. Langner) and thus toxic concentrations. "Normal" is 50 µMol/l. Ammonium escapes from the sediment into the tidal water by diffusion (efflux) and contributes to its nutrient content. This enables algae growth, and so the material cycle spiral turns.

Phosphate. In addition to the phosphate from the algae biomass, phosphate is released into the pore water as a result of the reduction of the sediment. Up to 120 µMol/l are reached (I. Langner), "normal" is at most 5 µMol/l. Here too, the efflux contributes to the nutrient enrichment of the tidal water.

Sulphate. At 24 µMol/l, sulphate is one of the main components of seawater and therefore also of pore water. In stress experiments, complete depletion of the sulphate was achieved on various occasions (B. Oelschläger), i.e. all sulphate was reduced to sulphide. Nothing comparable could be found in the literature.

Sulphide. Consequently, sulphide concentrations of up to 20 µMol/l were found, "normal" being 0.05 at most (B. Oelschläger). The difference to the original sulphate concentration can be explained not only by a loss through diffusion into the tidal water, but also by the reaction with the sediment's own iron to form black iron sulphide. Laboratory experiments have shown that this iron can reduce the sulphide pore water concentration by about 3 µMol/l (G. Klos). The binding capacity of the iron is then exhausted. A sediment area exposed in this way is therefore more sensitive to new pollution for a longer period of time (one year or more) than an area that has not yet been polluted. Sulphide was released into the atmosphere as hydrogen sulphide. It is one of the climate-relevant gases.

Dimethyl sulphide. The characteristically unpleasant-smelling decomposition product of an osmoregulating algae constituent reached 300 µMol/l in relation to pore water, occasionally much more. It is broken down to methane and sulphide under anaerobic conditions, but is quite stable in oxic sediment and can also enter the atmosphere, where it is categorised as a climate-relevant gas (G. Meyer).

Methane. It is not (as previously assumed) only formed after the sulphate has been exhausted, but already during ongoing sulphate reduction (M. Rackemann). One of the reasons for this is that acetic acid is a very good methanogenic substrate. Methane bubbles in the sediment play a role in the short-term alteration of black spots because they are compressed by the hydrostatic pressure of the tidal water and relax again as it drains away, sucking in or pushing out pore water from the surface (I. Langner). Methane is also a climate-relevant gas.

Nitrous oxide (laughing gas). Normally, ammonium is oxidised to nitrate in the oxic sediment, which is reduced to elemental nitrogen in the anaerobic-oxic transition zone. This escapes into the atmosphere. This is an ecologically important process that eliminates nitrogen compounds from the ecosystem and does not just relocate them elsewhere. In black sediments, this does not work to the end. Instead of nitrogen, nitrous oxide is produced, the fourth climate-relevant gas produced under such conditions (H. Ebrahimi, P. Lindenlaub).

The mudflats coped with the processes described and the substances occurring without any problems as long as the few and small black spots, i.e. the warning signal, were concerned. The impact on the surrounding sediment was minimal. Organisms were able to escape, and where they did not, their loss was manageable. The diffusion of products into the tidal water and the atmosphere was also negligible. The situation is quite different with the black areas. There is no longer a healthy area at the edges into which organisms can escape, and given the size of the areas (25 km² was mentioned), the amount of substances released into the water and the atmosphere is a cause for concern.

So far, so good. The phenomenon has been described and the causes of its formation have been named. Experts in the matter were now waiting for the appearance of dense macroalgae stocks in which large quantities of organic material are locally fixed. When they decomposed, they warned, black spots (= black areas) would appear over large areas. The black spots appeared even without algae. We never stop learning.

Black spots - an unfortunate chain of natural circumstances? Natural phenomena such as the occurrence of "black spots" are the product of the interplay of many individual events and therefore often defy scientific analysis. However, if key events can be recognised and interpreted as such, at least a "plausible" explanation can be derived. Thus, the following explanations of the occurrence of black areas merely present a "plausible" picture (see diagram) of the events. A whole series of questions remain unanswered.

The winter of 1995/96 was very cold and strong easterly (offshore) winds prevailed for several weeks, resulting in very low water levels. As a consequence, the dry areas in the Wadden Sea were covered with ice for a longer period of time, and during the time without water cover the frost penetrated deep into the mudflats. (To avoid any misinterpretation of the significance of the ice winter, it should be noted that with less than 100 days of ice cover, last winter was by no means a "winter of the century"). The frost and the mechanical rearrangement of the mudflats by drifting ice killed a large part of the fauna living on the surface (blue mussel) or immediately below the surface (pepper, tell and cockle). Even the deeply buried sand clam froze to death.

In spring, persistently low temperatures into April prevented a rapid decomposition of the dead animals. Only with the onset of warm and sunny weather in May did a rapid decomposition of the accumulated organic material and thus a consumption of oxygen occur.

At the same time, a first plankton bloom occurred, initially over a large area in the North Sea off the East Frisian coast, which was caused by a Nordic diatom (Coscinodiscus concinnus). A characteristic of diatoms, even these relatively large ones (up to 0.5 mm), is the storage of fat, which is released when the alga dies. If an algal bloom of this type settles on mudflats or if the algae-derived fatty film enters the mudflats from the sea, a fatty film can form on the surface. It can increase oxygen consumption, make the exchange of oxygen between water/air and the bottom more difficult and possibly hinder the gill respiration of bottom-dwelling animals.

In a cycle of decomposition, oxygen consumption, death and decomposition again, more and more species are caught up in the vortex. In large areas of the East Frisian Wadden Sea - there is clear evidence of this in the area of the island mudflats off Baltrum - more mudflat dwellers such as the sea ringworm and the lugworm fell victim to this self-reinforcing effect from the beginning of June.

Summarising the phenomena described, it seems appropriate to distinguish between the cause and the current triggers of black areas. Over decades, the naturally high productivity of the Wadden Sea has been further increased by nutrient inputs. In the ÖSF it has been proven that black spots are the result of localised biomass accumulation. The limit of the decomposition capacity of the Wadden Sea for organic material seems to have been reached, an explanation that is difficult to prove, but which is plausible if the mechanisms that lead to the formation of black spots are known. In such a predetermined situation, the deviation from "normal", let's call it "an event" for the sake of simplicity, can redirect processes in a way that we had to experience last winter until June. There have often been ice winters, even more severe ones. However, it seems that the ability to compensate for such an event is increasingly being lost.

The bottom line is this: Low temperatures and strong storms in late spring and summer initially turned black patches into black areas only briefly. In the presence of oxygen, the recolonisation of even large, previously oxygen-free areas can occur relatively quickly due to larval fall. If we take the black spots seriously as warning signals and regard the occurrence of black spots as a result of a chain of normal events as an even clearer warning signal, we take it as a warning shot across the bow of human excessiveness in dealing with nature.

Prof Dr Thomas Höpner (60), biochemist at the Institute of Chemistry and Biology of the Marine Environment (ICBM), was appointed to the University of Oldenburg in 1976. For many years, he has been conducting research into the turnover of substances in Wadden Sea sediments as part of the Lower Saxony Wadden Sea ecosystem research programme. Höpner is a member of numerous scientific committees. Among other things, he is Chair of the German Society for Marine Research (DGM). - Dr Gerd Meurs (39) studied biology and geography in Berlin and Oldenburg, where he gained his doctorate in 1994. His work focusses on the description of reproductive cycles of selected species and their significance in environmental monitoring. He was a member of the ecosystem research steering group for two years.