Biodiversity conservation problems in the marine environment

Volume 26/Number

4 April

1~93

002> 32fiX 93 $6.00+0.00 g' 1993 Pergamon Press [.tel

~larinc I'ollution lhdletitt, V~lumc 2~. No 4. pp. 179 I,',3 1993.

Prin~cd in (}real Brilain

Biodiversity Conservation Problems in the Marine Environment GIUSEPPE COGNETTI* and MARCO CURINI-GALLETTD *Dipartirnento di Scienze dell'Ambiente e del Territorio, Universita di Pisa, Pisa, Italy ~lstituto di Zoologia, Universitc~di Sassari, Sassari, Italy

Dr. Giuseppe Cognetti, member of the Editorial Board of the Marine Pollution Bulletin, is Professor of Marine Biology in the Faculty of Sciences in the University of Pisa, Italy. His research concerns adaptive strategies of organisms in unpredictable environments, benthic communities and marine environment conservation. Dr. Marco Curini-Galletti is Associate Professor of Zoology in the Faculty of Sciencies of the University of Sassari, Italy. His research interests are systematics and evolutionary biology of marine mesopsammic Platyhelminthes.

Conservation of biodiversity--understood as the expression of complexity of a biological structure both at the community and at the species level--was one of the focal points of the Earth Summit held in Rio de Janeiro. Reported estimates of loss of biodiversity which, with the current trend, will eventually lead to an extinction rate comparable to the massive extinctions at the boundary between Cretaceous and Tertiary, have caused widespread concern. Though it is not possible to quantify the actual level of the phenomenon, it seems undeniable that biodiversity is endangered not only in industrialized countries, but also in areas which, in the recent past, were unaffected. The cause is mainly linked to explosive population growth, leading, among other things, to a systematic destruction of forests and progressive desertification of vast areas. The problems of conservation of biodiversity in the sea are just as serious and complex as on land, although, being less conspicuous and accessible to mass media, they have often received less attention--and, in some cases, information given is unacceptably distorted (see Cognetti, 1992). The causes of reduction of biodiversity in the sea are manifold: for a better understanding of the problem, we enumerate the most conspicuous ones.

Habitat m o d i f i c a t i o n and d e s t r u c t i o n It is well known that the marine environment is more stable than the terrestrial, with stability of parameters

increasing with depth. In general, the more constant the chemico-physical parameters, the more stable the communities, which tend to be characterized by high specific diversity and high levels of genetic variability within populations (Sanders, 1968). Effects of environmental disturbance on biocenoses are all the more conspicuous when the environment affected is more stable. Specific diversity tends to decrease according to the intensity of disturbance, which operates through a gradient of physiological stress leading to a progressive reduction in the number of species and, at the same time, to an increase in the number of individuals of species able to withstand the increasing difficulty of the environment. These species (opportunistic) are characterized by populations with high reproductive rate and low genetic variability, since selection favours few flexible alleles able to withstand a wide range of variation of environmental parameters (Valentine & Ayala, 1978; Grassle & Grassle, 1978). Such a situation is frequently found along coasts neighbouring urban or industrial areas where an adequate deputation of discharges is lacking, in areas polluted by oil or where urban refuse is discharged by ships, in particularly fragile environments or in those with limited water exchange, as in coastal lagoons, an alteration of the input of organic matter or of water circulation may result in catastrophic effects. This has happened in the Orbetello lagoon (Tuscany), which was one of the most interesting brackish water habitats of the Mediterranean, noted for its high biodiversity, and which, in recent years, has been almost totally destroyed. 179

Marine Pollution Bulletin

Another example is the Saudi Arabian Gulf, where due to massive development which took place in the 197(}s and 1980s, the areal extent of mangroves has been reduced to only 4 km 2. Recent war episodes have further jeopardized the mangrove ecosystem in the area, since mangroves are particularly sensitive to oil pollution (Price & Sheppard, 1991). In the case of non-conservative pollution, conditions in affected areas may be restored once the source of disturbance is removed, though sometimes the original composition of the communities remains modified. Local modifications of bottom sediments can also have irreversible negative consequences on populations. It is worth mentioning, in this regard, the case of an interstitial platyhelminth belonging to the complex of sibling species of Pseudomonocelis ophiocephala. This sibling was exclusively known from two bays in the east coast of Corfu (Greece), where it lived intertidally in mixed silty sediments. In 1991 large amounts of fine sand were poured on the beach of one of these bays, with the intent of favouring recreation. This resulted in the total disappearance of the bay's population (Curini-Galletti, unpubl.). Although complete extinction of invertebrate species is still a rare event in the sea, this example concerning a species with limited range raises the suspicion that this might be due to our incapacity to discriminate between morphological and biological species, and that, in the sea as on land, species may disappear before being studied. The maintenance of natural habitats indispensable for the survival of particular species is one of the most difficult problems, especially in the Mediterranean. The case of the monk seal Monachus monachus is typical. This species, albeit protected, faces increasing problems in finding areas suitable for its reproductive requirements and rearing of offspring, particularly along the European coasts. Similar problems are faced by the sea turtles (7;retta caretta and Chelone mydas', which need undisturbed beaches for spawning and egg development. Natural or indirectly man-induced phenomena can also threaten single species or entire biocoenoses. In recent years, extensive bleaching events, particularly severe in the Caribbean, have affected large expanses of coral reefs, which are the most diverse habitats in the sea. This has been related to the present warming trend (Brown, 1987). Particular but exemplary cases are presented by gull species. In the Jutland, the kittiwake Ri,ssa trMactila is reduced to one single population whose nesting habitat (rocky cliffs) is progressively vanishing due to erosion (Prieur~ 1981). The survival of the slender billed gull Larus genei populations in the Northern Adriatic is similarly at stake, This species builds nests on the embankments of saltworks which are progressively being eroded (Fasola, 1986). Intervention aimed at reducing erosion, and habitat reconstruction, are therefore needed in order to avoid the extinction of the populations.

Overexploitation of biological resources The precarious condition of several cetacean and 180

pinniped species, the object of uncontrolled hunting in the past, is well known. Similarly, numerous species of fish, crustaceans and molluscs are at present suffering from severe decline due to overfishing. Control of fishing activity can, and has, improved the situation of several stocks, thanks to the high reproductive potential of these organisms. There is a risk, however, that population depletion and unexpected situations arising might preclude recovery in many of these cases. The case of Sardinopsis coerulea is a good example of this. The overexploitation of this fish in the 1930s and 1940s resulted in a severe depletion of stocks along the US Pacific coast. In 1955 fishing ceased completely since it was no longer economic. It was anticipated that stocks would progressively increase also through recolonization from stocks in Mexican waters, but this did not happen, as a result of a modification of hydrographic conditions intervening in the meantime, and by 1970 the former ecological niche of the sardine had bcen occupied by the anchovy (1)orst, 1978). In recent years a marked dccreasc has been observed in the stocks of the European cel Anguilla atzguilla. The number of young eels going up Italian rivers has decreased alarmingly, notwithstanding the fishing prohibition introduced a few years ago. This is probably linked to river pollution, but also to the heavy captures in past years. Similarly, only few specimens of the large limpet t'atella /'erruginea, which used tO be common akmg the Italian Thyrrenian coast where it has been totally wiped out as a result of its use as food, now survive on some islands of the Tuscan Archipelago. While it is still common in marine parks in Corsica, in the protected areas recently established in Italy the species has yet to recover, apparently because the larvae are short lived in the plankton, resulting in a low dispersal potential. In certain instances, the overexploitation of a commercially valuable species is accompanied by habitat alterations which preclude any possibility of recovery of the populations. Collection of the boring date mussels Lithodornus lithophagus which used to abound in the vertical calcareus cliffs of the Salento Peninsula (Apulia, Italy) and which are eagerly sought after as a delicacy, has been intensified in recent years, to the extent of using underwater pneumatic hammers. This has caused not only the substantial reduction of the stock but also a systematic destruction of the habitat, with consequences to the entire marine community in the area (Boero et aL, 1990}.

Erosion of genetic diversity Much debated is the question of whether the allelic isozyme variation in natural populations is selectively meaningful (Lewontin, 1974; Wills, 1981 ) or whether it should be considered adaptively neutral (Kimura, 1983" Nei, 1975). If largely neutral, allelic diversity should not be of particular importance for adaptive evolution; if largely adaptive, it is meaningful in conservation, as a prerequisite of evolutionary change, and a basis for species' resistance to disturbance. Evidence is increasing to suggest that genetic polymorphism is linked to

Volumc 26/Nunabcr4/April 19t,~3 adaptation to specific environmental parameters (reviews in Milton & Grant, 1984; Kohen & Bayne, 1989). New~ (1990) showed that population survival in conditions of environmental stress (specifically, chemical pollution) is related to selection of particular genotypes. Research involving mostly polychaete species indicates that mechanisms of adaptation to environments polluted by industrial wastes act quickly, with a drastic selection of favourable genes and the building up of vast populations starting from comparatively few specimens with the "right' genotype. When the cause of pollution is removed, the population, due to its reduced genetic heterogeneity, is unable to respond to the new environment and to compete with other rccolonizing species, and is thus eliminated (Cognetti, 1991). Erosion of genetic diversity can be enhanced by environmental chan,,es due--directly or indirectly--to human action. These phenomena can be detected at the initial stage, so that adequate protective intervention could be undertaken. As an example, the brackish water fish Aplumius iherus, endemic to Spain, now has a fragmented range due to drainage of parts of its habitat. The now isolated populations have reached a high level of genetic differentiation (Garcia-Marin et al., 1990). The genetic variability of the species as a whole can be conserved only maintaining the present ecological situation. Reduction of genetic diversity or an increase in the level of homozygosis may lead. in some circumstances, to inbreeding depression as well as to reduction of evolutivc potential in the face of changes of environmental conditions. From this stems a problem which is increasing in the field of conservation, since genetic factors may eventually jeopardize attempts to protect rare or endangered species (McCauley, 1991 ). The problem is also present in farmed species. The loss of genetic variability in many animal and plant species through domestication has stimulated the search of surviving wild stocks in order to recover the original diversity and confer anew the possibility of adaptation. Similar problems arc faced by farmed marine species. For example, in the populations of salmon (Salmo salar) of Norwegian rivers the number of specimens escaped from fish farms exceeds the number of wild ones (Saether & Jonsson, 1991). This could result in an introgression of domestic stock into the wild types, with loss of genetic adaptation to local conditions, as well as a potential for spreading diseases. The establishment of natural 'genetic reserves" is necessary in areas where species reproduce which are subject to fishing or farming, in order to avoid the over exploitation of the wild stock and the loss of the original genetic variability. A further aspect of this problem is the founder effect, which may arise in those species which have experienced a "bottleneck'. A classic example is given by the Cheeta (AciHot(~x ,/ul)attts), whose specimens are at present all genetically identical. This has been linked to past climatic variations which reduced the species to few specimens. The population recovered, but original genetic variability was lost. This phenomenon is also shown by marine mammals: the Northern Elephant Seal

(Mirounga angustirostris), whose populations were reduced to a few specimens at the turn of the last century due to hunting, is electrophoretically homozygote for any locus investigated. On the contrary, the Southern Elephant Seal (Mirounga leonina), whose populations never endured severe bottlenecks, have at present a level of polymorphism which is normal for their systematic group (Argano et al., 1991 ). Drastic protection interventions through international agreements have in many instances avoided extinction of species such as these. However, the chances of survival of species, whose genetic diversity has been severely depleted, in a medium and long term or in conditions of non-protection, is not known.

Anthropic modification of species relationships Human activities in certain instances may fawmr the numerical increase of some species which become invasive and which compete with other organisms present in the same habitat. The herring gull (Larus cachinnans) and the black headed gull (L. ridibundus) largely benefit from food and nesting places which result from human presence. These two species have increased their numbers throughout the Mediterranean and the Atlantic, reducing resources from other gulls. Large colonies of the tern Sterna sandvicensis and S. paradisea on the Meaban island in the Morbihan Gulf in Britanny, numbering about 4000 pairs, are at present smmgly reduced as a direct consequence of the invasion of the herring gull (Prieur, 1981). In the Mediterranean this species competes directly for resources with, or has prey-predator relationships with, species with patchy distributions and unstable demographic parameters, such as the endangered Auidouiffs gull (Larus audouinii) on the Tyrrhenian coasts, or the slender billed gull (Lares genei) in the Upper Adriatic (Fasola, 1986). The expansion of aquaculture resulted in a marked increase of the cormorant (Phalacrocorax carbo), which competes with Ardeids in many respects (Cherubini et al., 1991). In Australia too the increase in number of the silver gull (Larus novaeholhmdiae), caused by availability of food at rubbish dumps, threatens nesting colonies of the banded stilt ((Tadorhynchus [eucocephahts), whose eggs and chicks the gull feeds upon (Bellchambers & Carpenter, 1992). A further interesting aspect of the excessive increase of some species concerns the so-called "reserve effect', which, according to some authors, may arise in marine areas with integral protection. In some Mediterranean marine reserves, in fact, an impoverishment of macrozoobenthos has been documented. ]'his has been related to an excessive concentration in the areas of large fish species of commercial interest (Dentex dentex, Sparus auratus, Dicentrarclms labrax). Furthermore, a reduced algal cover has been observed, related to an increase of phytophagous molluscs (Boudouresquc et aL, 1991 ).

Introduction of alloctonous species The causes of species introductions arc manifold, and 181

Marine PollutionBullclin include the opening of canals through natural barriers (Suez, Panama); transport by ships (as fouling, or in ballast water); creation of artificial enclaves through thermal discharge; importation of species valuable for aquaculture. In the Mediterranean the entry of species from the Red Sea (Lessepsian species) was, until the 1940s, comparatively small due to the presence of the Bitter Lakes whose hypersalinity constituted a barrier to migration. Later readjustments of the Canal connected to war episodes, continued northwards flushing due to a tidal difference, and intensification of ship passage lead to a diminution of salinity in the Bitter Lakes. ('onsequently, the entry of species into the Mediterranean has been dramatically increased and, at present, they constitute a conspicuous fraction of the species living in the south-Eastern Mediterranean (Por, 1978). In some instances an equilibrium of autoctonous and lessepsian species with similar ecological niches has been reached through habitat partitioning. The stomatopod Squilla mantis, for example, is now restricted to deeper water along the Israeli coast, while the lessepsian S. massawensis is found in shallow waters. In other cases no niche separation has been attained, as seen with the autoctonous asteroid Asterina gibbosa, which, along the Israeli coast, has been replaced by the related lessepsian ,4. wega (Por, 1978). The chance or deliberate importation of molluscs and crustaceans creates yet other problems. About 20 years ago the East Asian bivalve Scapharca inaequivah'is reached the Adriatic, possibly via ships. Now, areas in the northern and central Adriatic are covered by enormous masses of this bivalve. The success of this species is due, among other things, to the fact that it is one of the few molluscs with haemoglobin as respiratory pigment instead of haemocyanin. This allows the bivalve to survive in waters with reduced oxygen content, which shields it from the recurrent crises of that sector of the Adriatic (Ghisotti & Rinaldi, 1976). Similarly, tile bivalve Crassostrea gigas and the decapod Penaeus japonicus, originally from Japan and widely cultured in European lagoons, have cohmized vast marine areas. The commercially valuable bivalve 7apes philippinarum, from S.E. Asia, has adapted very well to the Mediterranean environment, where it is gradually replacing the autoctonous 7~ decussala. As well as those animal species which are valuable for aquaculture, some plant species have been accidentally introduced into the Mediterranean. Three Japanese species made their appearance at the end of the 1960s; one of them, Aargasmtm muticum, is also found along English and Dutch coasts. A well known case is ('aulelpa mMfidia, a tropical weed which appeared about 10 years ago off the coast of Provence, replacing other algae and the sea grass Posidonia oceanica. So far. it is still localized and patchy in distribution, but its range is spreading and it has recently reached the Italian coasts. An interesting phenomenon liable to modify the original biocoenoses is thermal discharges from coastal industrial plants utilb'ing seawater for cooling purposes. Ahmg the North American and European coasts, in fact, 182

areas near these discharges, where temperatures are some degrees higher than the surrounding waters, harbour species which normally inhabit lower latitudes. This has been explained as being due to transport of larvae within warm currents or as part of ship fouling; once settled in the area of thermal discharge, the larvae find an environment suitable for their survival, resulting in populations replacing the original communities of the areas. In some cases, these species have gradually adapted to the surrounding colder waters, giving rise to genetically differentiated populations competing with the autoctonous species (Barnett &Hardy, 1984).

Concluding remarks Guidelines may be laid down for planned interventions, based on present knowledge of the progressive reduction of biodiversity in the sea, and on general criteria for conservation proposed by O'Connor (1974): 1. Survey of the most vulnerable species with the institution of protected areas especially designed for the protection of endangered species, in a manner similar to that done for the Monk Seal and the sea-turtles in Greece. 2. Preservation of natural habitats with the establishment of marine parks regulated according to local requirements and in the framework of international cooperation. 3, Active prevention and control of pollution, in order to ameliorate deteriorating ecosystems, even along heavily developed and industrialized coastlines. 4. Restoration of habitats which are deteriorating through natural phenomena or human activities (i.e. silting up of lagoons, erosion, abnormal development of certain species), aiming also at the re-creation of sites of ecological interest whenever possible. These criteria, albeit valid from a theoretical point of view, can in reality be successful only if there is an effective political will to apply them on the basis of extensive scientific knowledge and through international accords. One of the points stressed at Rio de Janeiro is the responsibility shared by all Nations to face the serious ecological problems of the planet in a decisive manner. Yet, in many Third World countries difficulties are overwhelming, since in some instances the mere survival of human populations is at stake. In order to encourage the preservation of biodiversity, economic incentives have been proposed for the countries where species of biotechnological interest live, whose original populations must be preserved in their natural environment. In this regard it is worth mentioning that one of the reasons for the United States refusal to sign the Biodiversity Treaty lies in the concerns of the US biotechnology industry about obligations of transfer of technical knowledge for exploitation, and about payment of royalties to countries where species of biotechnological interest live. Such payments have no! happened so far, as in the case of the rosy periwinkle of Madagascar (the source of two anticancer drugs) lk~r whose exploitation that country did not receive any money (Stone, 1992). This aspect does not concern terrestrial organisms only: morc and more often marine

Volume 26/Number 4/April 1993

plants and animals with pharmacologically active compounds are reported (see Russel, 1984). The preservation of biodiversity, however, does not concern developing countries only; in industrialized countries, as seen above, seriously compromised ecological situations are present, as a result of ignorance and, often, greed. In our opinion, the fundamental aim must focus on altering the reasoning whereby biodiversity is safeguarded for exclusively economic reasons, either through direct exploitation of habitats and species or maintenance of natural environments for human health and recreation. It is important to realize that species or biocoenoses which are at present considered of no apparent economic interest can be of importance for the preservation and functioning of entire ecosystems. A new reasoning should replace the old, a reasoning which embraces the idea that all organisms have intrinsic economical value, including those that current economics consider worthless. Therefore, future plans for development should consider biodiversity as a capital upon which financial resources should be invested, regardless of a more or less immediate and direct utilization. Argano, R., Datlai, R., Lanzavecchia, G., Luporini, P., Melone, G., Ortolani, G., Sbordoni, V. & Scalera Liaci, L. (1991). Zoologiu genemle e sistematiea. Monduzzi Editore. Barnett, P. R. O. & Hardy, B. L. S. (1984). Thermal deformations. In Marine Ecolog3; Vol. 5, (O. Kinne, ed. I. J. Wiley & Sons, Chichester. Bellchambers. K. & Carpenter, G. (1992). Sudden life on Stilt Island. Natural Histon' 4, 42 49. Boero, F., Fanelli, G., Geraci, S., Giangrande, A., Gravili, C., Grilli, G.. Piccinni, R.. lmperatrice, M., Piraino, S., Saracino, O. & Tucci, F. (1990). Impact of Lithophaga lithophaga (L.) (Mollusca) fisheries along the Apulian coast (Ionian and Adriatic Sea). Proceed. 25th Europ. Mar. Biol. ,~vmposium, Lido degli Estensi, Ferrara, Sept. 1015. 1991) Boudouresque, C. F., Caltagirone, A., Lefevre, J., Rico, V. & Semrod, R. (1991). Macrozoobenthos de la reserve naturelle de Scandola (Corse: Mediterranee Nord-Occidentale): Amdyse pluriannuelle de I'effet reserve. Reunion Medpan Ajaceio, 1-7. Brown, B. E. (1987). Worldwide death of corals. Natural cyclical evems or man-made pollution? Mar Pollut. Bull. 18, 9-13. Cognetli, G. 11991). Adaptations in marine unpredictable environments. In Serono Symposia: Biological lndicator; for Environmental Monitoring 27, (S. Bonotto, R. Nobili, & R. P. Revoltella, eds.), 153160.

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