General outline of biological response

The first important feature of interaction between gaseous traces and marine organisms is the quick fish response to a toxic gas as compared with fish response to other dissolved or suspended toxicants. Gas rapidly penetrates into the organism (especially through the gills) and disturbs the main functional systems (respiration, nervous system, blood formation, enzyme activity, and others). External evidence of these disturbances includes a number of common symptoms mainly of behavioral nature (e.g., fish excitement, increased activity, scattering in the water). The interval between the moment of fish contact with the gas and the first symptoms of poisoning (latent period) is relatively short.

Further exposure leads to chronic poisoning. At this stage, cumulative effects at the biochemical and physiological levels occur. These effects depend on the nature of the toxicant, exposure time, and environmental conditions. A general effect typical for all fish is gas emboli. These emerge when different gases (including the inert ones) oversaturate water. The symptoms of gas emboli include the rupture of tissues (especially in fins and eyes), enlarging of swim bladder, disturbances of circulatory system, and a number of other pathological changes.

These general features of fish response observed in the presence of any gas in the water environment are likely to be found for saturated gas hydrocarbons as well. Available materials derived from the medical toxicology of methane and its homologues support this suggestion.

Medical toxicology distinguishes between three main types of intoxication by methane:

• light, results in reversible, quickly disappearing effects on the functions of central nervous and cardiovascular systems;
• medium, manifests itself in deeper functional changes in the central nervous and cardiovascular systems and increase in the number of leukocytes in the peripheral blood; and
• heavy, results in irreversible disturbances of the cerebrum, heart tissues, and alimentary canal as well as acute form of leukocytosis.

These types most likely adequately describe the general patterns of methane effects in vertebrates. However, its features in respect to ichthyofauna remain to be studied. Fish resistance to the presence of gas at different life stages is of special interest. With most toxicants, the most vulnerable periods are the early life stages. The question of whether this general pattern is typical for saturated hydrocarbons still remains open. The importance of this issue in assessing biological effects of natural gas in the water environment is quite obvious.

During toxicological studies of different gases, including methane and its derivatives, one must take into consideration the influence of other factors (especially temperature and oxygen regime) that can radically change the direction and symptoms of the effect. In particular, increasing temperature usually intensifies the toxic effect of practically all substances on fish because of the direct correlation between the level of fish metabolism and water temperature. From the physiological perspective, this can be explained not only by the general intensification of fish metabolism but also by the increased permeability of the tissues for the poisons and increased oxygen consumption under high temperatures. Thus, toxicant concentrations that do not cause any effect under low temperatures can become lethal with increasing water temperature. This circumstance should be taken into consideration during ecotoxicological assessment of the potential impact of natural gas and other toxicants, especially when studies are conducted in high latitudes. In such regions, methane hydrates may be accumulated during the winter and dissociate during the increased temperatures in the summer. This may be followed by the releasing of free methane with corresponding environmental consequences.

Another critical environmental factor that directly influences the gas impact on water organisms is the concentration of dissolved oxygen. Numerous studies show that the oxygen deficit directly controls the rate of fish metabolism and decreases their resistance to many organic and inorganic poisons. This decrease sometimes depends more on the species characteristics and the rate of their gas metabolism rather than on the nature of the poison. From the physiological perspective, such a phenomenon is explained by the fact that the level of hemoglobin in fish blood and the rate of blood circulation through the gills increase under oxygen deficit. Clearly, such effects are of special interest when interpreting the data on fish response to natural gas in situations of significant change in the oxygen regime (e.g., during eutrophication of water bodies or seasonal and weather variations of the oxygen content).

Field and experimental studies support the previously described general pattern of fish response to the presence of methane and its homologues in the environment. In the Sea of Asov, researchers conducted detailed observations after accidental gas blowouts on drilling platforms during summer-autumn of 1982 and 1985 [GLABRYBVOD, 1983; AzNIIRKH, 1986]. The results of these observations indicate the existence of a cause-effect relationship between mass fish mortality and large amounts of natural gas input into the water after the accidents.

Fish in the zones of the accidents developed significant pathological changes. In particular, they displayed impaired movement coordination, weakened muscle tone, pathologies of organs and tissues, damaged cell membranes, disturbed blood formation, modifications of protein synthesis, radically increased total peroxidase activity, and some other anomalies typical for acute poisoning of fish. These pathological changes were found even in the fish collected at a considerable distance from the place of accident. Similar anomalies were observed in fish (flounder, sturgeon) kept for 4-5 days in the net cages in the direct vicinity of the mouth of the accidental gas well. Fish caught on the control stations and fish kept in the control cages did not show any deviations from the norm.

Significantly, some fish showed species-specific features of response to natural gas exposure. For example, flounder was more sensitive to the effect of natural gas than sturgeon. In 1982 and 1985 respectively, 69% and 28% of the flounders kept in the experimental net cages died. However, no sturgeon mortality was observed for the time of the experiments.

Besides the ichthyotoxicological data, studies on gas accidents in the Sea of Asov give some idea about the methane pollution of the water environment and its possible impact on the benthic and pelagic communities. Methane represented over 95% of the released gas. It was present in water in concentrations of 4-6 mg/l directly near the accidental well and in concentrations of 0.07-1.4 mg/l at a distance of 200 m from the platform. The increased content of this gas (0.35 mg/l) was also found 500 m from the well in the windward direction. These results suggest that methane and its homologues can stay in the water environment for a rather long period and spread over considerable distances. Similar conclusions were made based on observations in the Gulf of Mexico, where the areas around offshore drilling rigs had extremely high concentrations of methane and ethane in the water [Sackett, Brooks, 1975].

Information about the effects of methane and its homologues on water communities is very limited. Data indicate that benthic ecosystems have been disturbed and their trophic structure has changed in areas of methane seepage on the shelf of the North Sea and near the shore of California. Dense populations of Beggiatoa sp. were found in bottom sediments of these areas. These microorganisms use oil and gas hydrocarbons as a food source. In turn, they can become the base of the food chain for other benthic organisms [Davis, 1988; Howard, Thomsen, 1989].

Such symbiotic communities and ecosystems dependent on methane oxidation by microorganisms (mainly Methylococcaceae) appear to be typical for areas with high levels of methane in the bottom environment. In particular, they were recently found in areas of gas hydrate formation and gas seepage in the Black Sea and the Sea of Okhotsk [Galchenko, 1995]. The enzyme systems of bivalve mussels that were part of these ecosystems acquired some specific features due to the close symbiosis with methane-oxidizing bacteria.

The results of field studies around the accidental gas well in the Sea of Asov [AzNIIRKH, 1986] suggest that gas affects zoobenthic organisms more than the bacterioplankton and phytoplankton. In areas with a high concentration of methane, the biomass of benthos declined, in particular, because of the mollusk mortality. Some declining of the zooplankton biomass also occurred in the vicinity of the accidental well. However, the high variability of the zooplankton parameters and insufficient amount of available data do not allow us to make any reliable conclusion.

Experimental toxicological studies of the effects of methane and its homologues on water organisms are very limited. Some of them describe the responses of fish and zooplankton to bottled gas (mainly propane) exposure [Sokolov, Vinogradov, 1991; Umorin et al., 1991; Patin, 1993]. One of the studies suggests that under experimental conditions, low-molecular-weight hydrocarbons (methane and others) do not cause harmful effects on marine phytoplankton even at high water concentrations [Sackett, Brooks, 1975].

Laboratory experiments conducted at the Russian Federal Research Institute of Fisheries and Oceanography [Patin, 1993] imitated the conditions of gash (accidental) releases of bottled gas into the water environment. They revealed that immediately after beginning the gas input into the water, fish (young specimen of carp) showed obvious signs of excitement and increased motor activity. They scattered along the experimental vessels. The fish also stopped swallowing atmospheric air, probably because the air bladder was filling with the gas released into the water. Under the impact of subsequent gas releases, fish motor activity slowed, most specimens went down to the bottom, their movements became sluggish, and any responses on physical stimulation (knocking, touching) disappeared. By the end of the experiments, which lasted 60-120 minutes, the fish school behavior was totally disturbed. Some specimens sluggishly and chaotically moved toward the surface. Some settled on the bottom. Most fish showed signs of a balance disturbance and turned on their side.

Studies of behavioral responses to the presence of gas showed a rather high olfactory sensitivity of the fry of bream, perch, and other fish [Sokolov, Vinogradov, 1991]. For example, avoidance effects were clearly seen when concentrations of dissolved gas ranged from 0.1-0.5 mg/l. The threshold concentrations were lower (and hence the sensitivity of behavioral response was higher) for the fry of bream than for the fry of perch. After repeated exposure of fish fry to the short-term impacts of the threshold gas levels, the sensitivity of all fish increased. Avoidance effects were observed in the presence of 0.02-0.05 mg/l of gas. When gas levels rapidly increased, avoidance responses were suppressed. This led to the quick death of the fish.

The concentrations of bottled gas that caused the death of 50% of the fish during 48 hours (LC₅₀) equaled 1-3 mg/l [Umorin et al., 1991]. For zooplankton, this concentration during a 96-hour exposition was 5.5 mg/l without air pumping and 1.75 mg/l with it. These results suggest that fish are more vulnerable to the effects of methane homologues than zooplankton. They also indicate that acute toxic gas effects in fish start under minimum concentration of about 1 mg/l, which approximately match the results from field observations as previously described. Some other studies give similar values of LC₅₀ (96 hour) of natural gas for zooplankton, zoobenthos, and fry of marine fish (0.6-1.8 mg/l) [Borisov et al., 1994; Kosheleva et al., 1997].

The picture of fish response to the exposure of methane and its homologues in the water agrees with the general pattern of organismal response to any toxic or stress impact. This pattern involves consequent stages of indifference, stimulation (excitement), depression, and death of the organism [Metelev, 1971; Patin, 1979; Lukyanenko, 1983]. The previously described experiments suggest that along with the general pattern, some specifics of fish response to the acute impact of natural gas can be distinguished.

In particular, the primary fish response to the gas presence develops much faster than fish response to most other toxicants in the water. Clear signs of such response - the radically increased motor activity of the fish - are observed within the first seconds after gas goes into the water. Fast penetration of methane homologues into the living cells results in the instant impact of gas on fish gills, fish skin, and some other chemoreceptors. The high speed of behavioral response is most likely associated with the similarly rapid impact on the central nervous system.

Another feature of fish response to the gas exposure is a relatively short period between the first contact with gas and persistent signs of their poisoning (latent phase). The duration of this phase in acute experiments is 15-20 minutes. After this time, clear symptoms of acute poisoning indicate the beginning of the lethal phase. This includes the loss of movement coordination, disturbances of breathing, and others [Patin, 1993]. In gas concentrations of 1 mg/l and higher, lethal effects are clearly seen after 1-2 days of exposure.

Thus, in spite on the lack of research, especially under chronic exposure, the observations of both fish behavioral responses and fish mortality suggest a relatively low resistance of ichthyofauna to the presence of natural gas in the water environment. The high speed of primary responses, their clear manifestation, and their relatively short latent phase indicate a possibly damaging impact on the central nervous system of fish. Some data show the likelihood of higher resistance of zooplankton and benthos to the impacts of methane and its homologues. However, their responses still must be studied in the future.

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