Mechanisms generating and maintaining the admixture of ...

Marine Biology (1999) 135: 171±179

Ó Springer-Verlag 1999

J. R. Dadon á J. F. Masello

Mechanisms generating and maintaining the admixture of zooplanktonic molluscs (Euthecosomata: Opistobranchiata: Gastropoda) in the Subtropical Front of the South Atlantic

Received: 30 September 1998 / Accepted: 9 May 1999

Abstract The aim of this study was to test the hypotheses of faunistic mixing. Various di€erent mechanisms of the mixture of zooplanktonic organisms may exist in the transition zones. The distribution of planktonic gastropods of the order Thecosomata, which show a high ®delity to the water masses, was analysed. The study area comprises the southern part of the Brazil Current, the Brazil-Malvinas Con¯uence Zone, the Brazil Current Front, the Subtropical Front, the South Atlantic Current and the southern Benguela Current. The Subtropical Front presents sectors with contrasting dynamic characteristics which allow us to test hypotheses about the mechanisms generating faunistic mixture on a mesoscale. The evidence presented in the present study suggests that at least two mechanisms of faunistic mixture exist in the Subtropical Front. One is passive, resulting from environmental mixture in very dynamic front areas, where eddies are formed. The other mechanism occurs when the water column is vertically strati®ed. This mechanism depends on the migratory behaviour of the zooplankters and requires that there is stable strati®cation, that the depth of layers does not exceed the migratory capacity of the larger individuals and that the species can survive the physicochemical gradient.

Introduction From the point of view of physical oceanography, transition zones are areas with mixed water mass propCommunicated by O. Kinne, Oldendorf/Luhe J.R. Dadon (&) á J.F. Masello1 Dpto. Cs. BioloÂgicas, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires y CONICET, 1428 Buenos Aires, Argentina e-mail: [email protected] Present address: 1 Institute of Ecology, Friedrich-Schiller-University Jena, Dornburgerstraûe 159, D-07743 Jena, Germany

erties associated with boundary current extensions, such as the boundary between the subtropical gyres and high latitude circulation systems (Olson 1986). From the point of view of the biogeography of planktonic organisms, transition zones can be delimited by the range of the ecotonal species and by the admixture of organisms from the biogeographic regions bordering the zone. It is a common assumption that, since plankton is passive, the admixture of the species will be passive too. However, not all transition zones possess the same dynamical characteristics. This implies that various di€erent mechanisms of the mixture of zooplanktonic organisms may exist. In the present study the distribution of faunistic groups with a high ®delity to the water masses (hydrological indicators) was analysed. Planktonic gastropods of the order Thecosomata are found in all oceans. As Lalli and Wells (1978) pointed out, they constitute the largest group of holoplanktonic gastropods in terms of species number and total abundance. Several schemes have been proposed for the biogeography of the Thecosomata in the South Atlantic (Meisenheimer 1905; Spoel 1967, 1976; Spoel and Boltovskoy 1981; Dadon and Boltovskoy 1982; Dadon 1998), which all emphasize the existence of a direct relationship between the physical and chemical characteristics of the water masses and the species assemblages which inhabit them. According to these schemes, every water mass contains an association of characteristic species, which di€er from those of adjacent water masses, and which makes them excellent hydrological indicators. In the South Atlantic, the Subtropical Front was described as early as 1905 as a zone where typical species of Euthecosomata of cold and warm waters mix (Meisenheimer 1905). This front (mentioned by many authors as the Subtropical Convergence) is characterised by a relatively sudden change in the temperature of the super®cial waters along the latitudes 37 to 38°S, except for the regions at 30°W and close to South Africa, where the Subtropical Front runs further south (Peterson and Stramma 1991). The structural and dynamical charac-

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teristics of the front vary in di€erent sectors of the South Atlantic. Therefore, it can be expected that the processes which generate faunistic mixtures also vary. In the western sector of the front (Brazil-Malvinas Con¯uence Zone), warm-core eddies form periodically, a phenomenon which does not occur in the central sector. A close association between the processes forming warm-core eddies and the co-occurrence of warm- and cold-water assemblages of Euthecosomata was established for this area (Dadon and Magaldi 1995), which is also observed in Euthecosomata from other parts of the world's oceans (for example, in the North Atlantic; see Wormuth 1985). In contrast, in the Central Atlantic no eddies form and the dynamics of mixture on a mesoscale are much less intense. In order to test biogeographical hypotheses, detailed knowledge of distribution patterns and abundance of the target species are required. Although initial studies on the distribution of the Euthecosomata in the South Atlantic were carried out during the voyage of the H.M.S. ``Challenger'' (1872) and other expeditions (see review in Be and Gilmer 1977), until now the available literature contained numerous imprecisions regarding the limits of the geographical range of species, and thus the understanding of the biogeographical patterns of this group. Most of the previously available abundance data for the area are actually subjective estimations (for example ``abundant'', ``frequent'', ``rare''), which were made by the authors based on non-quantitative samples. More recent studies (Spoel 1967; Haagensen 1976; Be and Gilmer 1977; Spoel and Boltovskoy 1981) report data obtained in various ways (with di€erent sampling methods, di€erent nets, depths, sampling density, etc.), utilising subjective and sometimes varying criteria (see Be and Gilmer 1977). These reviews consequently resulted in generalizations for large areas based on few data obtained only in certain sectors, and therefore errors may have been magni®ed. The only quantitative estimations for Euthecosomata in the South Atlantic at the present are restricted to the southwestern sector, in particular, to the continental shelf of Argentina (Dadon 1984, 1986, 1989, 1990) and Brazil (Montu and Alves Cordeiro 1986; Resgalla 1993; Resgalla and Montu 1994; Dadon and Esnal 1995), which are areas of great dynamic complexity, with little similarity to the rest of the Atlantic. Therefore, it is necessary to obtain original data using quantitative sampling of the complete area. These data will allow the ®rst estimations of the abundance of Euthecosomata across a large area of the Central Atlantic, enabling the determination of species distribution patterns of this important group as well as test hypotheses related to faunistic mixing. The present study includes di€erent areas in the three sectors of the Atlantic (Southeast, Central and Southwest) and with contrasting hydrological characteristics: the Malvinas Current, the Brazil-Malvinas Con¯uence Zone, the Subtropical Front, the South Atlantic Current and the Benguela Current. This makes a comparison between di€erent areas sampled with the same method

possible and, in consequence, facilitates a critical reconsideration of the information available in the literature.

Materials and methods A total of 215 plankton samples were obtained from surface waters during a 19 d cruise aboard the R.V. ``Walther Herwig'' while transiting from Mar del Plata (Argentina) to Cape Town (South Africa) between 5 and 24 March 1971 (Fig. 1). The samples were collected by continuously pumping surface water (0 to 5 m), and were ®ltered through a plankton ®lter with a 100 lm mesh. Every 2 to 3 h the material collected in the plankton ®lter was transferred to individual glass tubes. Zooplanktonic molluscs were extracted manually from the samples. All specimens were extracted, except when samples had an excessive number of individuals (>1500). In these cases, a representative subsample was analysed. A total of 66 637 individuals were extracted and identi®ed to species level according to Spoel (1967) and Be and Gilmer (1977). A high percentage of the captured specimens were juvenile molluscs. For the identi®cation of juveniles, in particular of the genus Limacina, characteristics including the height of the spire, the size and shape of the umbilicus, and the size and orientation of the apex were measured and evaluated. Oceanographic characteristics of the study area The study area comprises the southern part of the Brazil Current, the Brazil-Malvinas Con¯uence Zone, the Brazil Current Front, the Subtropical Front, the South Atlantic Current and the southern Benguela Current (Fig. 1). The following description of the hydrology of the area is based upon Stramma (1989), Stramma and Peterson (1989, 1990) and Peterson and Stramma (1991). The Brazil Current arises when a small part of the South Equatorial Current turns south, approximately at 10°S. At 16°S the Brazil Current is nearly non-existent, and at 24°S only a marginal current remains. To the south of 24°S the Brazil Current regains intensity at about 5% every 100 km. This increase of the ¯ow of the Brazil Current is connected with a recirculation cell along the coasts of Brazil from 30°S, which has been observed with hydrographic measurements and satellite infrared radiation imagery supplemented with drifter trajectories. This recirculation cell has its origins in the con¯uence of the Brazil Current and the Malvinas Current. The Brazil Current separates from the continental shelf between 33 and 38°S, with the average being close to 36°S. This limit was obtained from satellite IR images and is not related to climatic conditions. After its separation from the western limit, the Brazil Current continues to ¯ow south together with the return ¯ow of the Malvinas Current. This is the region known as the Brazil-Malvinas Con¯uence Zone. The southern limit of the Brazil Current ¯uctuates between 38 and 46°S. The Brazil-Malvinas Con¯uence reaches in a southern direction to approximately 46°S. In the extreme south of its extent, warm-core eddies form, which are lost in the subantarctic zone of the Antarctic Circumpolar Current. The circulation of the Subtropical Gyre of the South Atlantic is closed in the south by the South Atlantic Current. It is separated from the Antarctic Circumpolar Current by the Subtropical Front. This front represents the southern limit of the warm waters of the Subtropical Gyre, and is characterised by a sudden change in the temperature of super®cial waters (4°C) and salinity (0.5&) that are found across most of the South Atlantic. It is usually found two to three degrees to the north of 40°S, except at around 30°W and close to South Africa where it runs south of this latitude. In the Southeast Atlantic, the South Atlantic Current penetrates the region of the warm-core eddies of the Agulhas Current Retro¯ection and ®nally ¯ows into the Benguela Current. The latter current is the eastern boundary current of the Subtropical Gyre. It is fed primarily by the South Atlantic Current but it may also receive water from the Agulhas Current as well as subantarctic

173 surface waters coming from perturbations of the Subtropical Front. The atmospheric conditions of the Benguela Current are strongly in¯uenced by the semi-permanent high pressure system over the Subtropical South Atlantic and by a low pressure system which develops over southern Africa in summer. The prevailing winds of the southern and southeastern sector of the Benguela Current create a region of upwelling of cold, nutrient-rich water when they turn. To the south of the Subtropical Front the Antarctic Circumpolar Current is found. This current ¯ows in an easterly direction across the whole South Atlantic. Further south it borders on the Subantarctic Zone, which extends to the Subantarctic Front at its southern limit.

Results and discussion Warm-water species

Fig. 1 Schematic representation of the large-scale, upper-level geostrophic currents and fronts in the South Atlantic Ocean (modi®ed from Peterson and Stramma 1991). Walter Herwig's voyage between Mar del Plata (Argentina) and Cape Town (South Africa) is indicated by a solid line with perpendicular slashes (Malvinas Current alternatively called Falkland Current)

Limacina bulimoides (d'Orbigny, 1836) occurred in the highest densities in the samples (up to a maximum of 352 366 ind/1000 m3). The observed densities are much higher than the maximum values cited for other regions of the world (2856 ind/1000 m3 in the Sargasso Sea: Chen and Be 1964; 1196 ind/1000 m3 in the Indian Ocean: Sakthivel 1977; 486 ind/1000 m3 in the China Sea: Rottman 1976). L. bulimoides was very abundant in the Benguela Current and very sparse in the zones in¯uenced by the Brazil Current, South Atlantic Current and the Subtropical Front (Fig. 2). Limacina in¯ata (d'Orbigny, 1836) was found along the entire cruise transect except in the Malvinas Current. The species was very abundant in the Brazil Current as well as in the Benguela Current, and less abundant in the Central South Atlantic. L. in¯ata reached maximal densities (up to 38 300 ind/1000 m3) in the Brazil Current. These densities are the highest that have been registered in the world's oceans [13 800 ind/1000 m3 in front of Magdalenay (South Baja California): SaÂnchez Hidalgo y Anda 1994; 11 673 ind/1000 m3 in the Sargasso Sea: Chen and Be 1964; 6292 ind/1000 m3 in Barbados: Lalli and Wells 1973; 4010 ind/1000 m3 in the China Sea: Rottman 1976]. Limacina lesueuri (d'Orbigny, 1836) was present in most parts of the Central South Atlantic. The maximum abundance was reached between 10°W and 5°E approximately, decreasing progressively to the west and to the east. The maximum observed densities (24 107 ind/ 1000 m3 in the Central South Atlantic) are much higher than the maximum cited in the literature (998 ind/ 1000 m3 in the Sargasso Sea: Chen and Be 1964; 196 ind/ 1000 m3 in the Gulf Current: Chen and Hillman 1970). It is notable that L. lesueuri and L. in¯ata have a reciprocal relationship where one is more abundant the other is rarer (e.g. Fig. 2). The observed horizontal distribution of the three most abundant species (Limacina bulimoides, L. in¯ata and L. lesueuri) presents a markedly di€erent pattern from that described in previous literature, as is discussed below (see ``Distribution patterns'').

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175 b

Fig. 2 Abundance (ind/1000 m3) versus longitude of the species found (Limacina spp., Styliola subula, Diacria quadridentata, Creseis virgula, Cuvierina columnella)

Limacina trochiformis (d'Orbigny, 1836) was found in the Brazil-Malvinas Con¯uence Zone (between 35 and 50°W), where it occurred with an abundance of up to 1964 ind/1000 m3, and in lower abundance in the region of the Tristan da Cunha group. These maximal densities are close to those registered above the Continental Shelf of Brazil: 1835 ind/1000 m3 (Dadon 1989; Dadon and Esnal 1995), but lower than those registered in other regions of the world's oceans [maximum: 35 200 ind/ 1000 m3 in front of Magdalena Bay (South Baja California): SaÂnchez Hidalgo y Anda 1994]. The observed distribution coincides with former descriptions. Spoel (1967, 1970) mentioned the presence of L. trochiformis in the South Equatorial Area and in the South Transitional Area (between 20°S and 10°N), but its absence at 10°W, which presents a clearly discontinuous distribution in the South Atlantic. Magaldi (1977) consider L. trochiformis one of the most abundant species in the surface waters of Brazil and Uruguay, while, according to Be and Gilmer (1977), it shows peak abundances in tropical regions, although it prefers upwelling zones and the proximity to continents. Styliola subula (Quoy and Gaimard, 1827) was registered in the region of the Tristan da Cunha Islands and in some discontinuous areas (e.g. Fig. 2). This species attained densities up to 714 ind/1000 m3, which are the highest registered in the South Atlantic (e.g. 60 ind/ 1000 m3 for the south of Brazil: Dadon and Esnal 1995). Cuvierina columnella (Rang, 1827) was only found in samples collected close to Tristan da Cunha in abundances of up to 530 ind/1000 m3. These values are much higher than those mentioned in the literature (less than 20 ind/1000 m3 in the China Sea: Rottman 1976; Indian Ocean: Sakthivel 1977; Gulf Current: Chen and Hillman 1970; Stepien 1980; Michel and Michel 1991). Creseis virgula (Rang, 1828) was found in only one patch in the region of the Benguela Current, with a maximum density of 5714 ind/1000 m3. This value is lower than that obtained by Resgalla and Montu (1994) in the south of Brazil (38 000 ind/1000 m3). Diacria quadridentata (de Blainville, 1821) was only present in a single sample from the region of the Benguela Current and in very low density (298 ind/1000 m3; e.g. Fig. 2). Various authors (Spoel 1967; Haagensen 1976; Be and Gilmer 1977; Magaldi 1977) agreed that this species is very sparse in the Atlantic. Cold-water species Limacina helicina (Phipps, 1774) appeared in regular intervals up to approximately 2°E (e.g. Fig. 2). Although it did not reach the abundance of the warmwater species during the transect, nor the maxima observed in other studies (110 000 ind/1000 m3 in the

Argentine Sea: Dadon 1989; 60 000 ind/1000 m3 in the Malvinas Current: Montu and Alves Cordeiro 1986), close to the Tristan da Cunha Islands up to 13 661 ind/ 1000 m3 were recorded. Limacina retroversa (Fleming, 1823) was present in the region of the Brazil-Malvinas Con¯uence Zone, in the South Atlantic Current and the Subtropical Front and close to the Tristan da Cunha Islands. It presented a similar pattern to L. helicina but a much lower abundance (789 ind/1000 m3). These abundances are much lower compared with earlier data for the Atlantic (1 000 000 ind/1000 m3: Boltovskoy 1971; 67 800 ind/ 1000 m3: Dadon 1990). Abundance of the Euthecosomata This study indicates that Euthecosomata are much more abundant than previously realized. In fact, three of the four most important species (Limacina bulimoides, L. in¯ata and L. lesueuri) were recorded in much higher densities than abundances reported in the literature; in the case of L. bulimoides the estimated densities are more than two orders of magnitude higher. The observed di€erences between our study and earlier quantitative studies carried out in other parts of the world's oceans may in part be explained by the mesh size of the net employed. Wells (1973) observed that the relative abundance of the most important Thecosomata increased considerably if nets with mesh size smaller than 100 lm were used, because these nets captured a larger percentage of juveniles. In our samples, more than 90% of the captured specimens were juveniles. Given that in natural populations early juvenile stages may constitute the most numerous age cohorts (Tranter and Fraser 1968) and that they are the base of the population, the estimations of abundance presented here are closer to the true values than previous estimations. The importance of the Thecosomata within the mesoplankton is well established, but the estimations of abundance presented here indicate that they also play a very important part within the oceanic microplankton, in particular in the boundary current areas. Distribution patterns The surface distribution described in this study for the most abundant species di€ers clearly from the distribution described in the literature. The case of Limacina bulimoides is the most remarkable, because the observed horizontal distribution was the exact opposite to what has been repeatedly mentioned in the literature. Spoel (1967) described L. bulimoides incorrectly as absent from the Benguela Current and the Central South Atlantic. Magaldi (1974) described L. bulimoides as one of the three most abundant species of Limacina of the BrazilMalvinas Con¯uence Zone. According to Be and Gilmer (1977), L. bulimoides is present in high concentrations in

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the central region of the South Atlantic and in the Brazil Current. The observed distribution di€ers drastically from these former descriptions, with the only exception being Morton (1954), who described L. bulimoides as abundant in the Benguela Current. L. bulimoides was found to be very abundant in the Benguela Current and was rare in the in¯uence zone of the Brazil Current, the South Atlantic Current and the Subtropical Front. Similar di€erences were observed for Limacina in¯ata. According to Spoel (1967), L. in¯ata rarely occurs in the extreme south of the Benguela Current. Be and Gilmer (1977) considered L. in¯ata very abundant in the Brazil Current and in the Central South Atlantic, and less common in the Southeast Atlantic. Contrary to the previous descriptions the present study shows that L. in¯ata is very abundant in the Brazil Current as well as in the Benguela Current, and less common in the Central South Atlantic. Eydoux and Souleyet (1852), Barth and Pereira de Oleiro (1968) and Haagensen (1976) mentioned Limacina lesueuri as a rare species in the Atlantic, while Be and Gilmer (1977) described it as uncommon. However, this species was common, and in fact was most abundant in the Central Atlantic, in particular between 10°W and 4°E. Regarding its distribution pattern, Be and Gilmer (1977) described correctly that it is preferentially found in central and oligotrophic waters (coinciding in this point with Spoel 1996), but, based on Tesch (1946), described it incorrectly as more common on the west coast of Africa, a region in which the density of L. lesueuri decreases and in which L. in¯ata (between 4 and 9°E) and L. bulimoides (between 9°E and the continent) become dominant. Fig. 3 Logarithm of the abundance of cold-water faunas (Upper panel, solid line) and warm-water faunas (upper panel, dashed line), vertical distribution of temperature and vertical distribution of the salinity versus longitude (vertical distribution of temperature and salinity based on Lenz 1974)

Faunistic assemblages As Brown et al. (1996) pointed out, if there is any basic unit of biogeography, it is the geographic range of a species. In the South Atlantic two faunistic groups or associations were observed, which correlated with the hydrological characteristics observed at megascale in this region: warm-water species and cold-water species. These two groups do not share species in common. The warm-water species are found in the Subtropical Gyre of the South Atlantic, and they are carried by the South Equatorial Current and continue in the Brazil Current, the South Atlantic Current and Benguela Current. The cold-water species occur in the Antarctic Circumpolar Current, which ¯ows eastwards parallel to the South Atlantic Current and the Subtropical Front. In the analysed samples, the simultaneous presence of species from both faunistic groups was observed along large parts of the Subtropical Front (Fig. 3). The latitudinal range of this coexistence in surface waters was established with precision around the Tristan da Cunha Islands and the Gough Islands, where samples were taken between 36°52¢S and 40°34¢S. The extreme north of the distribution of cold-water species extends in this sector to 37°20¢S (Fig. 4). In the Central Atlantic this limit occurs much further south than along the American continental shelf, where it reaches 33°12¢S due to transport by the Malvinas Current (Dadon 1989; Dadon and Esnal 1995). The southern distribution limit of warm-water species could not be determined here, because these species were constantly present across the complete range of latitudes

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studied. In accordance with previous reports (Magaldi 1974), the southern limit for warm-water species would be at 43°S, even though Dadon and Magaldi (1995) have pointed out that some species could reach 49°S if carried by warm-core eddies from the Subtropical Front. Mechanisms that generate the faunistic admixture The faunistic mixture was found to show di€erences between di€erent sectors of the South Atlantic. The faunistic transition zone starts in the western sector of the Brazil-Malvinas Con¯uence Zone. This con¯uence is a very dynamic area and is characterised by a high biological productivity compared with the surrounding area. Lenz (1974) analysed the oceanographic data of the year of sampling and found that the Brazil-Malvinas Current generates a complex pattern of mixture between 55 and 30°W with three semi-permanent meanders between the coast and 40°W (Fig. 3). This pattern seems to be stable across time, and is combined with the formation of warm-core eddies which migrate southwards and cold-core eddies which move northwards (Gordon 1989). This way, the dynamics of the area between 55 and 30°W would generate a patchy environment which could be responsible for the observed mixture of warmand cold-water species. The spatial and temporal periodicity of the pattern may explain the regularity with which samples with a mixed fauna occur in the area of the Brazil-Malvinas Con¯uence (Fig. 3). The strict association between the mixture of Euthecosomata and the dynamic pattern of the formation of warm-core eddies in this area has already been established using satellite information which was obtained simultaneously with plankton samples (Dadon and Magaldi 1995). In this case the hypothesis that the mixture occurs fundamentally passively as a product of the turbulent mixture of the water can not be rejected. To the east, a notable change of the hydrologic dynamics of the Front occurs. In the central zone of the Subtropical Front (30°W to 5°E) the faunistic mixture shows regularities similar to those observed in the Brazil-Malvinas Con¯uence Zone (Fig. 3), but which are

Fig. 4 Logarithm of abundance of cold-water (solid line) and warmwater (dashed line) faunas versus latitude

clearly not related to the formation of meanders and warm-core eddies which do not occur in this region. Consequently the hypothesis of passive mixture has to be rejected here. In this region, the hydrology is more stable, without meanders or eddies. Therefore the analysis of the hydrological dynamics alone does not explain the observed results. The water column shows a soft and permanent thermal strati®cation (Fig. 3), maintained by the sense of rotation of the South Atlantic Current and the Antarctic Circumpolar Current. In this region the cold-water front sinks under the warm water. Therefore, the isotherm of 15 °C is found at a depth of approximately 100 m, while the surface temperature is warmer at around 16 °C (which indicates that the Subtropical Front passes around here). In the described environment the mixture of Euthecosomata can not be driven by purely physical mechanisms. According to the environmental conditions and the hypothesis of passive mixture, the Euthecosomata would have to occur strati®ed, with the warm-water species between 0 and 100 m, and the cold-water species below, without mixed assemblages. In contrast, faunistic admixture was observed in surface waters (0 to 5 m) as would be expected if the 16 °C occurred close to the surface. This mixture does not occur in all samples but shows a marked spatial periodicity (Fig. 3) which does not seem clearly related to any observed physicochemical variable or combination of variables. It is therefore evident that the hypothesis of passive faunistic mixture has to be rejected. A new hypothesis must be employed to explain the observed results. Dadon (1998) suggested an alternative mechanism, which does not depend upon the active turbulent mixture of the water but, in contrast, is only possible if this mixture is restricted. This mechanism may take place in vertically strati®ed environments. According to this model, the strati®cation of the water column initially produces a strati®cation of the plankton, but this situation can be modi®ed by the migratory behaviour of some species. According to this hypothesis the faunistic mixture would require the presence of species which are capable of signi®cant vertical migrations and which possess a wide tolerance of physicochemical variables, allowing them to survive under the conditions of the depth range of the migration. If the migratory species had the same migratory pattern (i.e. nightly ascent and daily descent), we would expect only warm-water species in surface waters during the day and warm- as well as cold-water species at night. The latter originate from deeper layers. Many Euthecosomata perform daily vertical migrations. In the case of Limacina retroversa direct vertical migrations are known. This species forms large patches, lives up to 150 m deep and shows preferentially nocturnal peak abundances (Be and Gilmer 1977; Beckmann et al. 1987). Observations show that it is capable of vertical migrations of about 100 m (Wormuth 1985; Gilmer and Harbison 1986). Similar migrations occur in L. helicina. On the other hand, both species have wide

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tolerances of temperature and salinity. In the South Atlantic, these species are found in a large range of temperatures and salinities (L. helicina: up to 17.8 °C and 34.15&; L. retroversa: up to 19.8 °C and 34.16&). Therefore both species may live in deeper layers during the day and ascend at night, at this time mixing with warm-water species. The faunistic mixture would then not be passive, but would depend upon two factors: (a) the existence of a not too deep warm-water layer above a cold-water layer and (b) the migratory behaviour of at least some species which are tolerant to the conditions of the water column. In order to test this new hypothesis, two predictions were made. The ®rst refers to the time of the day in which the mixture occurs. Given that the cold-water species show a direct migratory pattern, the faunistic mixture should only be observed at night. In fact, in the graphical presentation of the diurnal and nocturnal peak abundances as a function of the longitude, the nocturnal peaks are clearly predominant over the diurnal peaks (Fig. 5). The second prediction is related to the migratory capacity of each individual. The distance which an individual can cover is directly related to its body size, as it depends on its swimming capacity. If the warm-water layer is less deep, a larger variety of individual body sizes are expected among the migratory individuals. However, because the juveniles migrate little or not at all, the deeper the layer, the more dicult it will be for small individuals to reach the surface, and the percentage of large individuals will increase. Therefore, if the faunistic mixture depends on vertical migration from deeper layers, it is to be expected that there will be an area of faunistic mixture generated exclusively by the ascent of individuals capable of migration (the large individuals) to the north of the Subtropical Front. To test this prediction, all individuals of cold-water species (Limacina retroversa and L. helicina) were measured. We found that without exceptions, the captured individuals were of large size (three whorls), and thus capable of migration. The evidence presented seems to imply that at least two mechanisms of faunistic mixture exist in the Subtropical Front. One is passive, resulting from environmental mixing in very dynamic front areas, where eddies are formed. The faunistic admixture is transitory here

and succession will take place (Dadon 1998). The other mechanism occurs when the water column is vertically strati®ed. This mechanism depends on the migratory behaviour of the zooplankters and requires that there is stable strati®cation, that the depth of layers does not exceed the migratory capacity of the larger individuals and that the species can survive the physicochemical gradient. One interesting consequence of the existence of this mechanism is that the mixture of fauna is temporally stable, i.e. the mixture is maintained while the strati®cation of the water column is maintained (Dadon 1998), which is in contrast to what occurs with the passive mechanism. An important biogeographical di€erence between the two mechanisms is related to the spatial extension of faunistic mixture. According to the model of passive mixture, mixing occurs along the complete zone of water mixing, i.e. the transition zone in the biological sense coincides with the transition zone in the physical sense. The faunistic superposition may extend beyond the front itself, but always in direct relation to the dynamics of the physical environment. One example of this is the formation of eddies in the Brazil-Malvinas Con¯uence Zone, which results in the simultaneous presence of cold- and warm-water species in the samples (Dadon and Magaldi 1995). In contrast, according to the model of active mixture, the two transition zones (the physical and the biological) do not have the same extension. The latter is always wider and thus faunistic admixture can be observed at a distance from the front. Depending on the strati®cation of the water column, the extension of this faunistic admixture will be relevant enough to be detected not only at small scales but also at a mesoscale. In any case, the zone of faunistic mixing extends asymmetrically, beyond the front, usually over warm-water masses (in the case of the Subtropical Front of the South Atlantic to the north), given that there is no strati®cation of the water column to the other side of the front. It is probable that the same mechanisms which are here proposed for the Euthecosomata of the Subtropical Front are also found in other groups of zooplankton which show migratory behaviour. Acknowledgements The authors thank Dr. E. Boltovskoy for providing the samples; S. Menu Marque, D. Boltovskoy, G. Rosa, E. Marscho€, B. GonzaÂlez, J. Calcagno and M. C. Rodrõ guez.

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Fig. 5 Logarithm of abundance of cold-water faunas versus longitude (dashed line nocturnal samples; solid line diurnal samples)

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