Biodiversity and Adaptive Mechanisms in Brackish Water Fauna

PII: S0025-326X(99)00173-3

Marine Pollution Bulletin Vol. 40, No. 1, pp. 7±14, 2000 Ó 2000 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0025-326X/00 $ - see front matter

Biodiversity and Adaptive Mechanisms in Brackish Water Fauna GIUSEPPE COGNETTI * and FERRUCCIO MALTAGLIATIà  Dipartimento di Scienze dellÕUomo e dellÕAmbiente, Via A. Volta, 6, I-56126, Pisa, Italy àDipartimento di Zoologia ed Antropologia, Corso Margherita di Savoia, 15, I-07100, Sassari, Italy A comparative analysis of estuaries, lagoons and coastal ponds focusing on population di€erentiation, and community structure is necessary to correctly address the issue of brackish water biology. Although the di€erent biotopes all present similar features of environmental unpredictability and the common presence of the hypohalobic contingent (artenminimum), they each have their own characteristics, due to the evolution of peculiar balances in their relation to the sea on the one hand and inland waters on the other. In addition to euryhaline species, locally adapted populations of stenohaline species typical of marine habitats, as well as some recently introduced species, are also found. These species have given rise to euryhaline populations, reaching their maximum development in an optimal site. This situation occurs between basins with essentially similar ecological features and probably depends both on the di€erent degree of adaptability of many species to a speci®c environmental parameter and the type of biocoenoses adjacent to the brackish basin. These populations possess genotypes allowing adaptation to brackish waters, which have resulted in the di€erentiation, through selection, of individuals capable of ®ne-grained perception of environmental unpredictability. Experimental works demonstrated the existence of genetically differentiated populations, or, ultimately, sibling species complexes, in several brackish species with broad geographical distribution and belonging to a wide range of taxonomic groups. The conceptions regarding the uniformity of brackish elements and the doubts concerning the existence of a speci®c brackish fauna come from the fact that attention generally focuses on species in the traditional meaning of the term, that is to say at the macrosystematic level. Comparative analyses of very ®ne morpho-physiological changes and genetic analyses result in a rather di€erent picture, leading to the conclusion that in brackish waters a given species of marine origin often consists of many di€erent forms at various levels of dif-

*Corresponding author.

ferentiation. Ó 2000 Elsevier Science Ltd. All rights reserved. Keywords: adaptive strategies; genetic variation; exotic species; conservation; environmental unpredictability.

Estuaries, lagoons and coastal ponds that communicate with the sea constitute transition environments, namely a morphological and dynamic change between two adjacent ecosystems. Their main characteristic is the instability of the chemical-physical parameters, above all the saline concentration. From a bioecological point of view, a uni®ed view of brackish environments as an ecotone between the sea and inland waters, following the concept proposed by Allee et al. (1949), is a questionable approach, as the heterogeneity of these systems leads to diculty in seeking a generalization. However, if an ecotone is interpreted in a broader meaning of the exchange of resources between adjacent ecosystems and the ecotonal resources produced, this de®nition appears to be fully valid, as such exchanges are implicit in the very principle of an ecotone, which refers to continuous resource ¯ows (Sacchi, 1995). Lagoons and estuaries are typical environments for trophic migrations and act as intermediaries for material discharged from the mainland. Moreover, they carry resources and nutrients to the sea while bene®ting from the action of marine waters, which regulate water temperature, ion balance and oxygenation. In these environments, hydrodynamism is far lower than in the shore area and therefore sedimentation both of terrestrial and marine origin is very accentuated. This favours the settlement of organisms that usually live on this type of substrate in the sea, in sheltered sites (Barnes, 1984). The stable biocoenotic component, whose elements are mainly of marine origin and complete the entire life cycle in this environment, was de®ned as ``halolymnobic'' by Bacci (1954). The component of lymnic origin, with very rare exceptions, has a lower adaptability range and is restricted to areas 7

Marine Pollution Bulletin

closer to freshwater inputs. Studies available in the literature on the distribution, origin and speci®city of these communities re¯ect a variety of con¯icting interpretations. On the one hand Remane (1940) considered brackish waters as a distinct biological dominion (``hyphalmirobious''), characterized by species common to the various biotopes; on the other hand Barnes (1989) denied the existence of an identi®able brackish assemblage and suggested that this environment is simply populated by a small group of thalassogenous species. He also argued that, although these species are certainly euryhaline, they are weak competitors, driven back by more competitive marine species into inland environments characterized by higher environmental unpredictability. These deeply contrasting views may nevertheless each have a degree of validity depending on the type of brackish environment considered. Attempts to provide a unitary and synthetic picture of the biological features of such extremely heterogeneous environments can lead to general conclusions that may be true for one situation, but untrue for another. The chemical±physical parameters of the great basins, remains of the sarmatic sea and naturally of the Baltic sea, follow relatively constant gradients and do not undergo the oscillations observed in most of the more restricted brackish basins, as for example those in the Mediterranean region, which are subjected to continuous changing, partly due to the impact of human activities. In general, it can be stated that brackish environments taken as a whole, at least in the same biogeographic regions, do share a limited number of hypohalobic and cosmopolitan species, which Remane (1934) de®ned as artenminimum. Together with these, other species may be found, with di€erent types of adaptability, as well as some recently introduced species, as we will see later. Even though the di€erent biotopes share analogous characteristics of environmental unpredictability and may have in common the presence of some artenminimum species, each biotope has its own peculiar chemical±physical and biological features due to the evolution of a particular balance in its relation both to the sea and to pluvial and inland waters. Thus, the communities within a biotope may at times have a remarkably high degree of biodiversity (Cognetti, 1994). To address the issue of the biology of brackish environments, it is necessary to undertake a comparative analysis of di€erent biotopes. Investigations should focus not only on the species composition and their distribution in relation to the chemical±physical parameters, but also on population di€erentiation, community structure and strategies of colonization.

Diversity of the Communities The instability of chemical±physical parameters in brackish environments is usually even more pronounced in smaller basins. Each parameter, within some limita8

tions, can represent a limiting factor for a given species. In particular, salinity plays the most important role, which is most clearly seen in the largest lagoons or brackish marine areas, where the distribution of organisms can be established in relation to isohalines. The smallest, and therefore ecologically least predictable, basins can be distinguished from a geomorphological point of view into several categories (lagoons, coastal ponds, estuaries, etc.), re¯ecting their hydrological diversity even in the biocoenotic component. The species living in these environments, both of marine or continental origin, follow a gradient of resistance to the increasing environmental stress. Generally, at a critical salinity level ranging between 5& and 8&, denominated horohalinicum by Kinne (1971), there is a sharp numeric drop. Deaton and Greenberg (1986) pointed out that the ionic relation Ca‡ /Na‡ and K‡ / Na‡ changes dramatically at 2& salinity. Consequently, according to these authors the term horohalinicum, which refers to a speci®c chemical±physical feature, does not correspond to Remane (1934) artenminimum. Thus, the salinity range corresponding to the horohalinicum should be considered as indicative because, in some cases, it can be exceeded depending on the tolerance of the populations of a given species. According to Arndt (1989), the horoalinicum is a physically regulated system in which species interactions do not appear to play a decisive role in Baltic coastal waters. It is an ``unsaturated biotope'' in which some species, such as the polychaete Hediste ( ˆ Nereis) diversicolor and the gastropod Hydrobia ventrosa can be characterized by high rates of population growth, if the salinity is suitable, which do not a€ect the other faunistic components. The distribution pattern is similar to that found in other unpredictable environments, such as polluted waters. Here too, speci®c diversity tends to decrease towards the source of disturbance, according to Sanders's (1968) hypothesis. But the di€erence as compared to lagoon and estuary environments lies in the fact that the maximum critical point in polluted environments corresponds to disappearance of the fauna, while in brackish environments there is a transition to the other community through the restricted contingent of hypohalobic species (artenminimum) (Fig. 1). Such species are considered by Potts and Parry (1964) as a limited portion of inland water communities, namely an ecological subdivision of those assemblages. Deaton and Greenberg (1986), on the contrary, assumed that artenminimum species constitute a typical and highly differentiated brackish community. In brackish waters, in particular those found in the same biogeographical region, it is almost always the same species that compose the artenminimum, but their presence may vary depending on basin area and on the resistance of individual species to variations in other environmental parameters (temperature, oxygen concentration, nature of the substrate) that characterize the basin itself.

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Fig. 1 Indicative scheme of species distribution in the transitional zone between sea and freshwater. (A) Relation between number of species and salinity. (B) Percent proportions of marine, freshwater and hypoalobic contingent species along a salinity gradient.

The succession of communities from the river mouth inwards can be more clearly distinguished in wider basins with greater vivi®cation. Oscillations in saline concentration ranging approximately between 30& and 15& do not substantially in¯uence distribution, which is a€ected primarily by oxygen concentration, temperature and type of substrate. Barnes (1989) argued that the paucity of species characterizing the muddy bottom, which is rich in organic material, is due to the nature of the substrate itself and not to salinity. However, this statement is true within the above-mentioned salinity range. For instance, the saprobic and opportunistic marine species that characterize sea habitats subjected to predominantly organic pollution (e.g. the polychaetes Scolelepis fuliginosa, Nereis caudata and sibling species of Capitella capitata complex) often include populations with varying degrees of euryhalinity in the more internal and degraded areas of ponds and lagoons, although salinity in such areas never falls below the critical threshold of 5±8&. On the other hand, another polychaete, Polydora ciliata, which, as we will see, is a complex of sibling species, is far more euryhaline and occupies these habitats well below the above-mentioned threshold. Areas having a good exchange with the sea are occupied by basically euryhaline marine species, whose populations have developed a broad tolerance to the unpredictability of the lagoon environment and have lost the substrate speci®city that

characterizes these species in the sea (Cognetti, 1978, 1982). As regards sessile animals, their presence is of course a€ected by the availability of hard substrata suitable for larval settlement. Many lagoons and coastal ponds of the Mediterranean sea, regardless of their extension, are characterized by remarkable biodiversity levels due to the input of elements from di€erent biogeographical regions. Above all in the salinity range included between 30& and 10&, many well-structured communities can be found. Although the di€erent biotopes all present similar features of environmental unpredictability and the common presence of the artenminimum, they each have their own characteristics, due to the evolution of peculiar balances in their relation to the sea on the one hand and inland waters on the other. This situation occurs between basins with essentially similar ecological features and probably depends both on the di€erent degree of adaptability of many species to a speci®c environmental parameter and the type of biocoenoses adjacent to the brackish basin. In this context, it is worth pointing out that in addition to typical euryhaline species, stenohaline species from various marine habitats are also found. These species have given rise to euryhaline populations distributed within a lagoon or an estuary, reaching their maximum development in an optimal site. This phenomenon has been observed in numerous brackish biotopes which, in addition to the shared basis of the hypohalobic contingent, also include other more typically marine species. For instance, the echinoderms Ophiura albida, Amphiura chiajei and Asterias rubens are found in the innermost parts of the Scottish ®ords, with populations that are morphologically distinct from those of the adjacent sea. It should also be noted that the Asterias rubens population shares many features with the Baltic sea populations (Pagett, 1981). Cereus pedunculatus, an anthozoan of coastal rock bottoms, is very common in both the lagoons of Orbetello and Sabaudia (Italian Tyrrhenian coast), where it even reaches the innermost areas, but it is not found in other lagoons. The polychaetes Syllis torquata and S. cirropunctata are found only in the Venice and Comacchio lagoons (Cognetti, 1994). The polychaete Gyptis capensis is present only in the Fusaro and Sabaudia lagoons (Giangrande and Gambi, 1985). Some endemisms are also known as regards proseriate ¯atworms: Minona trigonophora is endemic in the Rossillion ponds (Provence, France) (Ax, 1956) and Archiloa cirrifera in the upper Adriatic lagoons (Meixner, 1943), where endemisms of sarmatic origin have also been observed, such as the bryozoan Tendra zostericola and the tanaidacean crustaceans Heterotanais gurneyi of Atlantic origin, and the gastropod Littorina saxatilis. Another hypohalobic element of sarmatic origin is the copepod Calanipeda aquae dulcis, which can be found in some brackish ponds of the Mediterranean. According to Sacchi et al. (1983) they represent the remains of populations that invaded the Mediterranean areas during the ice age. In 9

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the brackish Fusaro lake (Naples, Italy) a polychaete species, Autolytus benazzii, has been described (Cognetti, 1956), which is represented by an extremely high number of individuals showing peculiar characteristics that di€erentiate it from the marine population, including di€erences in stolonization modes. Such di€erences were highlighted by San Martin (1984). The extent of this lagoon population has progressively declined in recent years, due to environmental alterations. The 5& salinity limit is the critical threshold for distribution of lagoon elements. Below this threshold, biodiversity levels drop drastically and, as we have seen, hypohalobic species of marine origin develop, accompanied by those species of lymnic origin which show better adaptation to a slight increase in salinity. The most frequent species found in the composition of the hypohalobic contingent of marine origin belong to a wide variety of zoological groups: the bryozoans Victorella pavida, Bowerbankia gracilis, Conopeum seurati; the polychaetes Ficopomatus ( ˆ Mercierella) enigmatica, Hediste ( ˆ Nereis) diversicolor, Polydora ciliata, Streblospio shrubsolii; the molluscs Hydrobia ventrosa, Abra ovata; the crustaceans Gammarus aequicauda, Corophium volutator, Sphaeroma hookeri, Leptocheirus pilosus, Echinogammarus pungens. These are all species of high ecological adaptability and with wide geographical distribution, and characterize brackish basins as a whole, albeit with notable di€erences. However, many uncertainties still remain as to their systematics, due to the morphological di€erences observed among populations at various localities. Such populations may have a di€erent degree of adaptability to decreasing salinity, as observed in V. pavida (Occhipinti Ambrogi and Scon®etti, 1984). The components of the hypohalobic contingent of lymnic origin likewise present remarkable di€erences among the various biotopes. The mollusc Stagnicola palustris, the crustaceans Gammarus chevreuxi, Palaemonetes antennarius and several tubi®cid oligochaetes can be found up to 6±7& salinity. Tubi®cid tolerance of salinity and oxygen variations has been studied in the estuaries of northern Europe. In the Thames estuary, some tubi®cids, such as Limnodrilus ho€meisteri, Tubifex tubifex, Psammoryctides barbatus do not go beyond the 8& threshold, while others, such as Tubifex costatus, tolerate higher salinity levels. Moreover, they have a marked vertical distribution in the sediment in relation to the oxygen concentration (Hunter, 1981). Young immature individuals occupy the oxygen-rich surface layer, while adults, who can tolerate lower oxygen concentrations, are found in the deeper layers, where reproduction takes place. The extreme boundary between the two biomes should therefore not be considered as a marginal environment marking a transition from marine to freshwater species, but rather as a single and well-de®ned habitat with its own speci®c fauna. It is worth noting that the artenminimum is not only a characteristic of basins with 10

extreme environmental variability, but is also found in the great brackish basins of the Black sea and the Caspian sea, correlating only with a reduction in salinity. Therefore, according to Deaton and Greenberg (1986), the artenminimum cannot be explained purely in terms of the instability of physical factors. Even in the brackish microhabitats of the Mediterranean sea, which may occupy an area smaller than 50 square metres, an artenminimum has been found. It is consistently composed of the poychaetes H. diversicolor and S. shrubsolii, to which other euryhaline species typical of wider basins may be associated, depending on the site (Castelli et al., 1988).

Exotic Species In the past few years, as is well known, an increasing presence of species deriving from di€erent biogeographical regions has been recorded in the various seas. In the Mediterranean, this phenomenon has become particularly evident, mainly as a result of lessepsian migration, maritime trac (shipÕs hulls and bilge waters or shipÕs ballast) and aquaculture. Foreign elements have also been introduced into a number of brackish basins, sometimes giving rise to substantial populations (Cognetti, 1994). Similar cases occurred in the past, although to a more limited extent. In the 1920s, a serpulid polychaete appeared in the Mediterranean and rapidly colonized brackish basins of all kinds, becoming one of the main components of the artenminimum. Fauvel (1923) described this species and considered it as belonging to a new genus (Mercierella); he denominated it as enigmatica, precisely on account of its inexplicable sudden and massive appearance and the total lack of knowledge on its biogeographical region of origin (Fauvel, 1933). Generally the introduction of exotic species has a negative impact on native communities. In many Mediterranean brackish habitats, for example, the presence of the exotic poeciliid Gambusia anis, introduced for malaria mosquito control at the beginning of the century, favoured the reduction and extinction of many populations of the endemic cyprinodontids Aphanius fasciatus and A. iberus (Bianco, 1995; Maltagliati, 1998a). However, the introduction of allochthonous species into brackish waters may contribute to an increase in biological diversity at the local scale. For instance, the amphipod Echinogammarus pungentoides and the hydrozoan Garveia franciscana from the tropical Atlantic and Indian-Paci®c areas have appeared in the northern Adriatic lagoons, probably having arrived together with ®sh and crustaceans imported for aquaculture. The cnidarian Haliplanella lineata from the northwest Paci®c was found by Kiener (1971) in Corsican lagoons. The bryozoan Tricellaria inopinata, belonging to the Indian-Paci®c fauna, has invaded the Venice lagoon (Sacchi et al., 1983). The isopod Paraceneis sculpta, whose genera are well-known along the

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American Atlantic and Paci®c coasts, has been collected in the Venice lagoon (Forniz and Scon®etti, 1985) and in the lake of Tunis (Rezig, 1978). The amphipod Elasmopus pectenicrus of lessepsian origin has invaded some brackish basins of the southeastern Mediterranean, and the sabellid polychaete of Indian-Paci®c origin Desdemona ornata has been found in brackish microhabitats on the Elba Island, in the coastal ponds of Tuscany and Sardinia, in the Venice lagoon and in the Ephesia bay (Greece) (Lardicci and Castelli, 1986; Panagopoulos and Nicolaidou, 1989). The gastropod Littorina littorea of the European Atlantic coasts has appeared in the pond of Faro, in Sicily, imported together with mussels from the Atlantic. Many algae from Japan that were inadvertently transported together with oysters or other animals imported for aquaculture purposes have invaded ponds and lagoons of the Mediterranean sea. Some species can adapt to a broad range of salinity conditions, while others, such as the picnogonid of Indian-Paci®c origin Ammothea hilgendor®, found in the Venice lagoon by Krapp and Scon®etti (1983), are more clearly stenohaline and are localized in the most vivi®ed areas at salinity levels that do not fall below 25&. It should be noted that this phenomenon is by no means restricted to the Mediterranean. Many Mediterranean brackish species have appeared in other biogeographical regions, settling in similar habitats.

Adaptive Strategies in Brackish Waters An overall analysis of the biocoenotic composition of brackish environments suggests that the speci®cally brackish component, shared by most biotopes, is usually restricted to the few species of the hypohalobic contingent. Although Barnes (1989) denial of the existence of a speci®c brackish macrofauna, even with reference to the hypohalobic contingent, may be somewhat too strong, it is undeniable that, at least in the broad 30±10& salinity range, the elements composing the biocoenosis are almost always marine elements with a greater or lesser degree of opportunism, and belong to the various habitats of the coastal areas. In most cases, they are euryhaline species, but it is not uncommon, depending on the various biotopes, to see typically stenohaline species. Barnes (1989) observation holds true in the framework of traditional classi®cation of the species, based on morphological features. But the picture becomes far more complex if di€erent criteria of systematic investigation are adopted. In our opinion, the problem of the speci®city of the brackish bioceonosis and of its di€erence from the two adjacent biomes should be addressed not so much at species but rather at population level, seeking to identify the adaptive mechanisms that have in some cases allowed even kstrategy species to colonize stressful brackish environments. These species clearly include genotypes with varying degrees of adaptability, which have resulted in

the di€erentiation, through selection, of populations capable of ®ne-grained perception of environmental unpredictability, in some cases even the type of substrate. Such populations are distributed along a physiological stress gradient. For instance, a k-strategy anthozoan of coastal rocky bottoms, Cereus pedunculatus, has given rise in some lagoons to r-strategy populations which are not only euryhaline but also capable of occupying areas with a heavy organic pollution load, as observed in the Orbetello lagoon. Similar behaviour has also been observed in several polychaetes and molluscs living not only in the coastal area, but also in subcoastal habitats. Thus, the gastropod Jujubinus striatus, which is typically marine, has an endemic subspecies, J. striatus delpreteanus found in the brackish lake of Faro (Sicily) (Curini Galletti and Palazzi, 1979). Similarly, the typically brackish species of the artenminimum tend to be fragmented into locally adapted populations that are recognizable not only by their physiological behaviour, but sometimes also by their morphological characteristics. Ficopomatus ( ˆ Mercierella) enigmatica populations can be distinguished by the shape of their opercular spines (Cognetti, 1954) and those of Hediste ( ˆ Nereis) diversicolor by the number of chitinous paragnaths on the pharynx (Muus, 1967). According to Muus (1967), the local paragnaths patterns must be taken as evidence of the existence of local isolated populations. In addition, H. diversicolor populations with di€erent degrees of adaptation to the toxic e€ects of heavy metals have been also reported (Bryan, 1984). In a coastal lake of Romania with extremely high salt concentration, which has remained isolated since the last century, a gobid, Potamoschistus microps leopardinus, can be clearly distinguished from the adjacent sea population of the same species, owing to morphological characters, such as colouration size, interorbital distance (Pora, 1972). In several hypersalty lagoons of the Black sea, populations of Hediste diversicolor distinct from those living in oligohaline habitats of the same regions have formed through selection. If individuals living in hypersalty environments are introduced into oligohaline habitats, the survival rate is zero, and the same is true for the reverse phenomenon (Pora and Rosca, 1952). Nereis limicola, distributed in the estuaries located between Vancouver and central California, has settled in freshwater habitats, giving rise to a population sharply di€erentiated from those of other brackish environments (Petit, 1962).

Genetic Diversity in Brackish Waters The question may now be raised of how many species belonging to the multiplicity of groups that have adapted to one or other brackish biotope consist as a matter of fact of highly di€erentiated populations or even sibling species, as suggested by Muus (1967). Their identi®cation by analysis of morphological features is often dicult and at times impossible, but it can be 11

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clearly showed by genetic analysis, as noted by Grassle and Grassle (1974) for the polychaete Capitella capitata. If the problem is addressed from this point of view, statements concerning the non-existence or trivial nature of a speci®c brackish fauna must be revised, both as regards the artenminimum communities and also those with a lower degree of tolerance, ranging between 30& and 10& salinity. The existence of genetically di€erentiated populations has been demonstrated in several brackish species with broad geographical distribution and belonging to a wide range of taxonomic groups. Hediste diversicolor has populations with a high degree of genetic divergence in the Mediterranean (Abbiati and Maltagliati, 1996) and also the North and Baltic seas (R ohner et al., 1997). In both cases, Nei (1978) genetic distances greater than 0.2 have been observed between populations of the various biotopes. In the mollusc Potamocorbula amurensis, introduced from Asia into the San Francisco Bay and capable of adapting to marked salinity variations, a 0.0018±0.0186 genetic distance has been observed in 5 populations of as many sites in the bay (Duda, 1994). Ruditapes decussatus has clearly differentiated into 5 populations distributed over the same number of brackish ponds and estuaries of the Mediterranean and Atlantic seas (Jarne et al., 1988). Analysis of 10 samples of the ostracod Cyprideis torosa collected in the Baltic and the North Sea has revealed two clearly distinct populations with a genetic distance of approximately 0.8 (Sywula et al., 1995). Similar cases are observed for some ®sh species. A high degree of genetic divergence has been detected in Aphanius fasciatus, a teleost typical of brackish environments (Maltagliati, 1999). As shown by Fig. 2, which refers to ®ndings on populations of some Mediterranean sites, allozyme genetic analysis in A. fasciatus demonstrates a set of populations whose genetic di€erentiation appears to be related to the geographical distance. Similarly, as re-

gards the closely related species A. iberus, distinct populations have been observed, with a sharp discontinuity between Atlantic and Mediterranean populations (Doadrio et al., 1996). Some brackish species are e€ectively a complex of sibling species. In a site of the Sea of Japan, Polydora ciliata, a cosmopolitan polychaete of the artenminimum in very many biotopes, has been shown to be composed of two sibling species (Manchenko and Radashevsky, 1998). Similarly, Sato and Masuda (1997) have demonstrated a complex of sibling species, on the basis of genetic diversity and egg size found in Hediste japonica living in estuarine waters. In addition, preliminary allozyme results suggest that Syllis gracilis is a group of sibling species, that are sometimes sympatric both in brackish and marine environments. It should be emphasized that some brackish species, such as the bivalve Cerastoderma edule, have a slight population di€erentiation due to their high potential of larval dispersal in the sea (Beaumont and Pether, 1996). It is therefore essential to address the issue of gene ¯ow among the populations. The teleost Aphanius fasciatus, for instance, has extremely low levels of gene ¯ow, which follow the one-dimensional stepping-stone model (Maltagliati, 1998b). Though very low, gene ¯ow might occur as a consequence of occasional and stochastic events, such as exceptional rainfalls or ¯oods that would force migration of adult individuals along coastal seawaters and/or through transitory inland water pathways. One fundamental issue is the interpretation of the mechanisms allowing many stenohaline species to colonize brackish environments. As we have seen, they are r-strategy populations, which at times can even reach innermost areas of a basin. This problem, which arose in the framework of comparative research on the brackish species of di€erent biotopes (Cognetti, 1994), is being

Fig. 2 Dendrogram of NeiÕs genetic distances among eleven population of the brackish cyprinodontid ®sh Aphanius fasciatus and one of the closely related species A. iberus. Within A. fasciatus populations the genetic distance is related to the geographical distance.

12

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addressed by means of allozyme investigation of some populations of the bivalve Mytilaster minimus and the polychaete Syllis gracilis. Preliminary results showed that the M. minimus population, having become di€erentiated within a lagoon, presents a 0.25 genetic distance from the adjacent marine population. S. gracilis, as noted above, also proved to be a veritable complex of sibling species, likewise di€erentiated from the sea in various di€erent lagoons. Therefore, it would be of great interest to extend such researches to additional unpredictable environments such as those subject to pollution, where similar cases of colonization from the sea could be observed (Cognetti, 1992).

Concluding Remarks The conceptions regarding the uniformity of brackish elements and the doubts concerning the existence of a speci®c brackish fauna come from the fact that attention generally focuses on species in the traditional meaning of the term, that is to say at the macrosystematic level. Comparative analyses of very ®ne morpho-physiological changes and genetic analyses allow to obtain a rather di€erent picture, leading to the conclusion that in brackish waters a given species of marine origin often consists of many di€erent forms at various levels of di€erentiation. This diversity involves not only the artenminimum, but also the typically marine euryhaline populations which have di€erentiated in each individual basin and whose genotypic diversity as compared to the original marine populations forms the object of our current research. Analysis of genetic divergence within typical brackish species shows both a high degree of fragmentation into local populations and, ultimately, the existence of species complexes which may even be sympatric. These distinct populations or sibling species, unidenti®able by means of the classical morphological analysis, show di€ering degrees of adaptability. Geological history substantially a€ects brackish fauna di€erentiation. In the relict basins of the ancient sarmatic region, there are groups that can be considered as exclusively typical of brackish basins, such as the cnidarians Moerisidae and endemic genera of molluscs (Adacna, Monodacna, Didacna), amphipods (Amathillina, Niphargides) and teleosts (Caspialosa, Clupenella, etc.). Elements of sarmatic origin have migrated into several lagoons of the Adriatic sea and a few other basins of the Mediterranean sea. Clearly, the recent origin of the majority of the brackish biotopes lies at the root of the paucity of species and uniformity of their fauna from a macrosystematic point of view, but, at the same time, their elevated selectivity and isolation determine the great diversity observed in the individual elements. As Bacci (1954) pointed out, in these cases the brackish environment is a terminal environment, which is not conservative as it is simultaneously unstable and tran-

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