Adaptive strategy of brackish-water fauna in pure and polluted waters

Volume 13/Number 7/July 1982 Alzieu, C., Michel, P. & Thibaud, Y. (1976). Pr6sence de micropolluant darts les mollusques littoraux. Sci. P~che, 264, 1-18. Anderlini, V. C. & AI-Harmi, L. (1979). A survey of tar pollution on beaches of Kuwait. Kuwait Institute for Scientific Research Marine Pollution Programme Report EES-I 1. Anderlini, V. C., Mohammed, O. S., Zarba, M. A. & Omar, N. (1981a). Assessment of trace metal pollution in Kuwait. Vol. 1 of the final report of the trace element and bacterial pollutants project: EES-31 A, Kuwait Institute for Scientific Research, Kuwait. Anderlini, V. C., AI-Harmi, L., DeLappe, B. W., Risebrough, R. W., Walker, W., Simoneit, B. R. T. & Newton, A. S. (1981b). Distribution of hydrocarbons in the oyster, Pinctada margarit(fera, along the coast of Kuwait. Mar. Pollut. Bull., 12, 57-62. Anderlini, V. C., Mohammed, O. S., Zarba, M. A., Fowler, S. W. & Miramand, P. (1982). Trace metals in marine sediments of Kuwait. Bull. Envir. Contam. Toxic., 28, 75-80. Bernhard, M. (1978). Heavy metals and chlorinated hydrocarbons in the Mediterranean. Ocean Mgmt, 3,253-313. Burns, K. A. & Smith, J. L. (1977). Distribution of petroleum hydrocarbons in Westernport Bay (Australia); Results of chronic low level inputs. In Fate and Effects of Petroleum Hydrocarbons in Marine Organisms and Ecosystems (Wolfe, D. A., ed.), pp. 442-453. Pergamon Press, New York. Burns, K. A. & Smith, J. L. (1981). Biological monitoring of ambient water quality: The case of using bivalves as sentinel organisms for monitoring petroleum pollution in coastal waters. Estuar. cstl Shelf Sci., 13,433-443. Burns, K. A. & Smith, J. L. (1982). Hydrocarbons in Victorian coastal ecosystems: Chronic petroleum inputs to Western Port and Port Phillip Bays. Archs. Envir. Contam. Toxic., (in press). Elder, D. L., Villeneuve, J. P., Parsi, P. & Harvey, G. R. (1976). Polychlorinated biphenyls in sea-water, sediment and over ocean air of the Mediterranean. Activities of the International Laboratory of Marine Radioactivity, 1976 Report, pp. 136-t56. EPA (1979). Methods of chemical analysis of water and wastes. EPA-600/4-79-020, (March 1979). Method 245.1 (Manual cold vapour technique), pp. 245.1.1-245.1.6. Establier, R. (1978). Contenido en mercurio, cobre y zinc en moluscos de diferentes zonas del Golfo de Cadiz y estrecho de Gibraltar durante el periodo 1976-1977. Inf. Tecn. Inst. Inv. Pesq., 54, 1-19. Farrington, J. W., Teal, J. M. & Parker, P. L. (1976). Petroleum hydrocarbons. In Strategies .for Marine Pollution Monitoring (Goldberg, E. D.. ed.), Chap. 1. John Wiley, New York.

Fowler, S. W. & Elder, D. L. (1980). Chlorinated hydrocarbons in pelagic organisms from the open Mediterranean Sea. Mar. Envir. Res., 4, 87-96. Goldberg, E. D., Bowen, V. T., Farrington, J. W., Harvey, G. R., Martin, J. H., Parker, P. L., Risebrough, R. W., Robertson, W., Schneider, E. & Gamble, E. (1978). The Mussel Watch. Envir. Conserv., 5, 101-125. Gupta, R. S. & Kureishy, T. W. (1981). Present state of oil pollution in the Northern Indian Ocean. Mar. Pollut. Bull., 12,295-301. ICES (1974). Report of the working group for the international study of the pollution of the North Sea and its effects on living resources and their exploitation. Co-operative Research Report No. 39, ICES, Denmark. Khalaf, F. I., AI-Saleh, S., AI-Modyain, L. & AI-Omran, L. (1979). Interim Report. Kuwait Institute for Scientific Research. Report No. KISR/PPI 152/EES-RT-R-7911. Marchand, M., Vas, D. & Duursma, E. K. (1976). Levels of PCBs and DDTs in mussels from the N.W. Mediterranean. Mar. Pollut. Bull., 7, 65-69. Officer, C. B. & Ryther, J. H. (1981). Swordfish and mercury; A case history. Oceanus, 24, 34-41. Oostdam, B. L. (1980). Oil pollution in the Persian Gulf and approaches 1978. Mar. Pollut. Bull., 11,138-144. UNEP (1981). Survey of tar, oil, chlorinated hydrocarbon and trace metal pollution in coastal waters of the Sultanate of Oman. UNEP/ Regional Seas Programme, Geneva. UNESCO (1976a). Guide to operational procedures for the IGOSS pilot project on marine pollution (petroleum) monitoring. Intergovernmental Oceanographic Commission, World Meteorological Organisation, manuals and guides No. 7. UNESCO (1976b). Marine sciences in the Gulf area. UNESCO Technical Papers in Marine Science No. 26. Villeneuve, J. P., Elder, D. L. & Fukai, R. (1981). Distribution of polychlorinated biphenyls in seawater and sediments from the open Mediterranean Sea. Ves Journ~es Etud. Pollutions, CaligarL CIESM, Monaco, pp. 251-256. Wakeham, S. G. & Farrington, J. W. (1980). Hydrocarbons in contemporary aquatic sediments. In Petroleum in the Marine Environment (Petrakis, L. & Weiss, F. T., eds).'American Chemical Society, Washington DC.

Marine Pollution Bulletin, Vol. 13, No. 7, pp. 247-250, 1982. Printed in Great Britain.

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Adaptive Strategy of Brackish-water Fauna in Pure and Polluted Waters GIUSEPPE

COGNETTI Institute o f Z o o l o g y , P i s a University, Via A . Volta, 4, 5 6 1 0 0 Pisa, Italy

A comparative analysis of various brackish-water biotopes has intricated certain characteristics of the community structure, and the colonization and adaptation of various species to very different ecological situations. A large diversity of the fauna in the various biotopes has been ascertained, each of them showing peculiar properties. Together with species typical of these environments, there are many others, often until now never collected in brackish waters, which, according to different local situations, characterize and distinguish various situations. A comparison of the fauna between brackish waters and sea waters polluted by organic wastes point out to what degree adaptive strategies are analogous. Genetic variability of the organisms makes standardization of monitoring methods difficult in these unpredictable environments.

Interdisciplinary research carded out for many years along t h e I t a l i a n c o a s t s h a s r e v e a l e d a series o f d a t a o n t h e f a u n a , flora, productivity and physico-chemical characteristics of waters subjected to various types of pollution. Particular attention has been given to brackish waters. Biotopes investigated in detail were the Venetian lagoon, marshes of Comacchio and mouth of the Reno River on the Adriatic Sea; a n d c a n a l s o f C a l a m b r o n e ( L e g h o r n ) , L a g o o n o f Orbetello and Burano (Grosseto) on the Tyrrhenian Sea (Fig. 1). The aim of these investigations was to ascertain the natural and economic importance of some biotopes and to e v a l u a t e t h e i r level o f p o l l u t i o n . I n a d d i t i o n , it is p o s s i b l e to point out certain common characteristics of each community's structure, colonization and the adaptation of 247

Marine PollutionBulletin

clavata only at Orbetello and Syllis cirropunctata in the Venetian lagoon and at Comacchio. Streblospio shrubsoli is very common at the mouth of the Reno river and is missing at the mouth of the Calambrone canals. Diversity of the various communities is obviously due to the particular ecological characteristics of each biotope but also, for species not normally found in brackish water, to the type of adjacent benthic communities. For example, the great richness and variety of marine bottom fauna in front of the mouth of the Orbetello lagoon is the most important reason for its varied fauna. Therefore, we can clearly distinguish this environment from others studied, even if they have similar physico-chemical characteristics. In the Orbetello lagoon, in particular, the patterns of distribution of organisms were followed from the mouth to the innermost zones (Cognetti etaL, 1978). Many species which perceive the substrate as coarse grained and which are able to penetrate in to the lagoon waters maintain these characteristics in areas more directly influenced by the sea. In the inner lagoon areas, instead, where there is greater instability and an increase in eutrophication, only some of these species are able to adapt. This applies, for instance, to Platynereis dumerilii, Eulalia

Fig. 1 Locationof the investigatedbiotopes.

1, Venetian lagoon; 2, Po river delta; 3, Comacchio marshes; 4, Reno rivermouth; 5, Calambronecanals; 6, Orbetellolagoon; 7, Burano lagoon.

various species to a typical brackish environment, even though in very different ecological situations.

Diversity of Brackish-water Fauna Comparative analysis of the various biotope shows the existence of remarkable differences from one zone to another. This is true of both the more similar environments, such as marshes and lagoons, on the one hand, and river mouths and canals on the other. Typical brackish-water species are present everywhere, even if in different localizations within the same biotope. For instance, Nereis diversicolor and Mercierella enigmatica reach areas with the greatest variations in salinity and along with Polydora ciliata, also adapt to the most eutrophicated waters. On the other hand, Abra ovata, Cerastoderma glaucum and Paranemonia cinerea, although typically found in brackish-water, are less tolerant of the highest variations of certain physico-chemical parameters, in particular oxygen deficiency. Other species which tend to be euryhaline may be absent in one biotope and instead be present in another. They may occur in large numbers in the most ecologically unpredictable zones. The sea anemone Cereuspedunculatus, for example, found only in Orbetello lagoon, is located in the inner zones of the lagoon and reaches sewage-polluted waters together with Ariciafoetida and Scolelepisfuliginosa. This last species is also found at Comacchio and in some marshes of the Po river delta. These examples concern not only euryhaline and saprobic species, but also species with other ecological characteristics. Since they are widely represented their presence is not to be considered as casual. Syllis torquata, for example, has only been collected at Comacchio, Brania 248

sanguinea, E. punctifera, Phyllodoce rubiginosa, P. vittata, Eteone picta, and Exogone gemmifera, which in the sea have a well defined localization on the bottom weeds. In the inner lagoon, in contrast, they are indifferently distributed on various substrates, algae and phanerogams, muddy and sandy bottoms and detritus. The substrate is therefore perceived by the animals as fine grained, as are the other physico-chemical parameters. In the Orbetello lagoon, species diversity of the mudbottom polychaete community in the two basins is quite different (Bonvicini Pagliai & Cognetti, 1982). This is due to colonization of the muddy bottom of the eastern basin by polychaetes living in the sea on well defined substrates. This basin, in fact, presents a high level of eutrophication compared to the western basin. The same occurs in sea communities primarily controlled by physical factors. Even here the nature of the substrate, very important in biologically accommodated communities, loses more and more value (Cognetti, 1972, 1979; Cognetti & Taliercio, 1969).

Colonization Strategies Colonization of brackish waters often occurs with modalities similar to those of polluted marine areas, where, along with typically opportunistic species, there may be nonopportunistic species represented by populations which adapt to these particular conditions. These may occur in a given geographic area, but not in another one, even though it may have analogous ecological features (Cognetti, 1978). As we have seen, in fact, in various brackish biotopes, in addition to typically euryhaline species, there may be present others, even stenohaline, with populations perfectly adapted to the instability of the environment. Evidently this is due to the existence within these species of genotypes with different levels of adaptability, which, by selection, gave rise to populations able to colonize brackish waters. The distribution occurs along a gradient of environmental predictability, where each species may

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reach its maximum growth at the optimal point with modalities analogous to those of opportunistic species of polluted waters. This also occurs for the euryhaline species Cereuspedunculatus, which in certain biotopes may occupy more and more unpredictable environments, and even for stenohaline species such as some Phyllodocidea. Nereis diversicolor does not adapt to polluted conditions at Comacchio and Orbetello, while in the Calambrone canals it is present everwhere, even on bottoms heavily polluted with oil. On the other hand it is well known that a population of this species is adapted in a Cornish estuary heavily polluted by copper, with concentrations of this metal ranging from 20 to over 4000 ppm (Bryan & Hummerstone, 1971). The variability within the populations and the tendency to separate into local races in brackish waters has often been pointed out (Bacci, 1954). Cognetti Varriale (1973) showed a high variation in pharynx size in populations of Nereis diversicolor living in the Calambrone canals. Related to the ecological conditions of the waters, she found that the paragnath number tends to change proceeding from the mouth of the canals towards the more interior zones. While phenotypes with lower number of paragnaths are favoured near the sea, these phenotypes are missing and those with a higher number of paragnaths are favoured in the more interior waters. Many species which tend to be opportunistic penetrate certain brackish biotopes up to the most eutrophicated zones. Some of them, however, do not tolerate extreme variations in some physico-chemical parameters and often do not reach the inner areas. This is the case in Staurocephalus rudolphii, a typical opportunistic species, but which cannot tolerate salinity and temperature fluctuations. Even Capitella capitata, also present at Orbetello, Comacchio and Calambrone, does not reach the inner areas. Nereis caudata and Scolelepis fuliginosa, which together with Capitella capitata occupy the most polluted harbour zones, are distributed instead at Orbetello in the most eutrophicated areas where salinity and temperature fluctuate within large limits during the year. The number of individuals may also fluctuate, as occurs for the opportunistic species in the sea (Grassle & Grassle, 1974). New forms have been collected, some being distinguishable morphologically. At Orbetello and Comacchio a new type of Bran& very similar to Brania clavata was collected, easily distinguishable by certain slight morphological diferences (Cognetti et al., 1975). It is to be noted that Brania clavata was not found in the marshes of Comacchio, while it is present at Orbetello, even if only in the more vivified areas. A similar example is that of Podarkepallida: in harbour areas this polychaete gives rise to populations which differ from those living in adjacent pure waters areas (Zunarelli Vandini, 1971). P. pallida in the Orbetello lagoon is represented by a population morphologically distinguishable from both the offshore populations and that in Leghorn harbour (Zunarelli Vandini, 1978). It would therefore be interesting to analyze electrophoretically the intraspecific variation of this species, as has been done for some polychaetes (Grassle & Grassle, 1974; Rice & Simon, 1980); moreover, the possible existence of sibling species, as ascertained in Cap#ella capitata (Grassle, 1976) and Ophryotrocha (~kesson, 1978), must be considered.

Conclusions Data obtained during these studies on brackish waters point out a large diversity of the fauna in the various biotopes, each of them showing peculiar properties. There are, obviously, a series of species typical to these environments but together with these there are many others which, according to different local situations, characterize and distinguish various biotopes. In populations of the latter species, many of which until now have never been collected in brackish waters, one may consider the existence of certain genotypes that control a functional phenotypic flexibility and are, therefore, capable of allowing survival in unstable environments such as those studied. By selection, populations particularly adapted (and sometimes morphologically distinguishable) differentiate, and are therefore able to respond to environmental stress. High mortality rate in distrophic brackish waters, evidenced by large numerical fluctuations in the same zone during the year, is probably the result of an intense selection to adapt to unpredictable situations. This is in agreement with that pointed out by Grassle & Grassle (1974) for opportunistic species. A comparison between brackish waters and polluted sea waters points out to what degree adaptive strategies in these unpredictable environments are analogous. In fact, in polluted sea waters of certain geographical zones, nonopportunistic species may appear, which then give rise to populations able to adapt to the most unpredictable environments (Cognetti, 1978). However, the difference in adaptation in waters affected by peculiar sources of poilutants (e.g. heavy metals, sodium carbonates and hydrates, thermal pollution, etc.), where populations specialized to these highly peculiar environments may differentiate, should be emphasized. These populations are, for this reason, extremely labile. In fact, their existence is dependent on the persistence of those special environmental conditions to which they are adapted. A return to normal conditions may, therefore, cause their complete disappearance, as pointed out for Syllis amica and Ophryotrocha hartmanni in the Piombino harbour (Cognetti, 1979). From the point of view of assessing pollution-induced changes, the survey of damage caused by pollution on this type of benthic community is easily ascertainable. It is more difficult, however, to establish the level of pollution in the ecosystems discussed above, where the communities, even in completely normal conditions, are predominantly controlled by physical factors. As pointed out by Clark (1979), the standardization of monitoring methods to get early warning of pollution damage is particularly difficult due to the genetic variability of the organisms and continuous replication of samples to a large extent is needed, even if this incurs notable difficulties from an operational point of view.

~kesson, B. (1973). Reproduction and larval morphology of five Ophryotrocha species (Polychaeta, Dorvilleidae). Zool. Scripta, 2, 145-155. Bacci, G. 0954). Alcuni rilievi sulle faune di acque salmastre. Pubbl. Staz. zool. Napoli, 25, 380-396. Bonvicini Pagliai, A. M. & Cognetti, G. (1982). Ecology of polychaetes in the coastal brackish lagoon of Orbetello (Tuscany). Boll. Zook 48, (in press).

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Marine Pollution Bulletin Bryan, G. W. & Hummerstone, L. G. (1971). Adaptation of the polychaete Nereis diversicolor to estuarine sediments containing high concentrations of heavy metals - I. General observations and adaption to copper. J. mar. biol. Ass. UK, 40, 845-863. Clark, R. B. (1979). Monitoring change in the marine environment. Atti Soc. Tosc. Sci. Nat. Sez. B, 86, suppl. 229-247. Cognetti, G. (1972). Distribut.ion of the Polychaeta in polluted waters. Rev. Int. Ocean. m~d., 25, 23-34. Cognetti, G. (1978). On some aspects of the ecology of the benthic littoral polychaetes. Boll. Zool., 45, 145-154. Cognetti, G. (1979). Influence of substratum on predominantly physically controlled communities. Rapp. Commn. int. Mer M#dit., 25, 181-182. Cognetti, G., De Angelis, C. M. & Orlando, E. (1975). Attuale situazione ecologica delle Valli di Comacchio e proposte per la loro salvaguardia. Quaderni di Italia Nostra, 12, 69 pp. Cognetti, G., De Angelis, C. M., Orlando, E., Bonvicini Pagliai, A. M., Cognetti Varriale, A. M., Crema, R., Marl, M., Mauri, M., Tongiotgi,

MarinePollutionBulletin,Vol. 13, No. 7, pp. 250-253, 1982. Printedin GreatBritain.

P. & Vandini Zunarelli, R. (1978). Risanamento e protezione dell'ambiente idrobiologico della laguna di Orbetello. 1. Situazione ecologica e ittiocoltura. In£egn. ambientale, 7,316-406. Cognetti, G. & Taliercio, P. (1969). Policheti indicatori dell'inquinamento delle acque. Pubbl. Staz. Zool. Napoli, 37, suppl. 149-154. Grassle, J. (1979). Polychaete sibling species. In Aquatic Oli,eochaete Biolo£y (Brinkhurst & Cook, eds), pp. 25-32. Plenum Press, New York. Grassle, J. F. & Grassle, J. P. (1976). Life histories and genetic systems in marine benthic polychaetes. J. mar. Res., 32,253-284. Rice, S. A. & Simon, J. L. (1980). lntraspecific variation in the pollution indicator polychaete Polydora li£ni (Spionidae). Ophelia, 19, 79-115. Zunarelli Vandini, R. (1971). Observations on a population of Podarke pallida (Polychaeta, Hesionidae) in heavily polluted waters. Boll. Zool., 38, 177-180. Zunarelli Vandini, R. (1978). Variabilita nell'ambito di una specie ad alta valenz~a ecologica, Podarke pallida (Polychaeta, Hesionidae). Boll. Zool., 45,249.

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Enhanced Mercury Tolerance in Marine Mussels and Relationship to Low Molecular Weight, Mercury-Binding Proteins G. ROESIJADI*, A. S. DRUM*, J. M. THOMAS t and G. W. FELLINGHAM ~= *Battelle, Pacific Northwest Laboratories, Marine Research Laboratory, Sequim, WA 98382, USA t Battelle, Pacific Northwest Laboratories, Quantitative Ecology Section, Richland, WA 99352, USA t 344 TaylorCutoffRoad, Sequim, WA 98382, USA Pre-exposure of marine mussels to low levels of mercury (0.5 Mg I-I and less) enhanced their tolerance to more toxic levels. Seawater mercury concentrations similar to our experimental pre-exposure levels have been reported in mercury-contaminated areas where mussels presently exist. A higher pre-exposure concentration (5 ~g i -1) was not effective in inducing enhanced mercury tolerance. The relative effectiveness of pre-exposure concentration in inducing enhanced tolerance was related to induction of mereury-binding proteins, the degree of saturation of mercury on the proteins, and the extent of binding of mercury to other subcellular fractions.

Prior exposure of a variety of organisms to potentially toxic metals such as copper, cadmium or mercury can result in an increased tolerance to toxic levels of the respective metal (Bryan & Hummerstone, 1971; Bryan, 1976; Leber & Miya, 1976; Stokes, 1977; Beattie & Pascoe, 1979; Moriatou-Apostolopoulon, 1978; Bonquegneau, 1979; Rauser & Curvetto, 1980). These organisms possess the capability to adapt, either through genetic or nongenetic mechanisms, to the presence of low (but higher than background) concentrations of these metals and would be better suited for survival either in environments with naturally high levels of metals or those in which human activities have introduced high levels. 250

In certain marine environments, metal-resistant populations (e.g. the polychaete worm Nereis diversicolor and the copepod Acartia clausit) have been identified under conditions of trace metal contamination (Bryan & Hummerstone, 1 9 7 1 ; Bryan, 1 9 7 6 ; MoriatouApostolopoulon, 1978). These animals are clearly adapted for survival in their metal-contaminated environments. Metal-resistant populations of similar or different species may also exist in other contaminated coastal regions such as near urban and industrial centers. We have been interested in determining whether increased resistance to metal toxicity is widespread in marine animals and in investigating mechanisms underlying acquired resistance to metal toxicity. Our primary interest is to examine the relationship between metal toxicity and the role of low molecular weight, metal-binding proteins (similar to metallothioneins) which have been implicated in detoxification of metals such as mercury, cadmium, copper and zinc (Kojima & Kagi, 1978; Roesijadi, 1981). We have previously reported (Roesijadi & Hall, 1981; Roesijadi et al., 1981) the existence of low molecular weight, mercury-binding proteins in the marine mussel, Mytilus edulis. These proteins are induced by mercury exposure and bind significant quantities of cellular mercury. In this study, we explored the relationship between such mercury-binding proteins and induced