Marine centres of origin as evolutionary engines
2003; Wiley; Volume: 30; Issue: 1 Linguagem: Inglês
10.1046/j.1365-2699.2003.00810.x
ISSN1365-2699
Autores Tópico(s)Marine Biology and Ecology Research
ResumoThe world ocean supports a dynamic system in which living organisms undergo constant movements. Although some would appear to be sedentary, all are capable of invading new territory at some stage in their life cycle. Underlying these comparatively rapid changes is a much slower evolutionary system whereby new species are formed and spread out. Depending on their place of origin and genetic resources, some of the new species may give rise to continuing phyletic lines. At the same pace, some older species approach extinction by continuing to lose territory. Over time, this evolutionary system appears to be no less dynamic than the contemporary one. In recent years, considerable attention has been paid to the East Indies as a centre of origin for the marine tropics. While other centres of origin in the Antarctic and the North Pacific have been recognized, little attention has been paid to their external influence. Yet in the cooler waters of the oceans, they are as important to those areas as the East Indies is for the tropics. Evidence indicates that evolutionary flows from all three centres contribute to a dynamic system that extends throughout the world ocean. Each of the three centres and its salient features is discussed in turn, the information is summarized, and then stated in the form of a hypothesis. Antarctica has a long history of harbouring a temperate marine fauna. That assemblage first become apparent in the Devonian when the Antarctic continent was still attached to the southern part of Gondwana. At that time, Antarctica belonged to the Malvinokaffric Realm that was distinguished by its lack of many common tropical animal groups (Boucot, 1988; Crame, 1994). This latitudinal position, suggesting the presence of relatively cool conditions, continued throughout the Mesozoic and into the early Tertiary. From the early Cretaceous to the Oligocene, a warm-temperate Weddellian Province extended from the tip of South America to Antarctica and to Australia/New Zealand. That Province disappeared with the development of colder temperature and the Antarctic Circumpolar Current (Crame, 1999). A dramatic change in the temperature zonation of the earth began with the global climatic deterioration of the middle Eocene. A new cold-temperate zone, with winter temperatures from 12 °C down to 2 °C, began to form at the highest latitudes. As a consequence, the warm-temperate waters were forced away from the poles and into lower latitudes. At one time, there was a general belief that Antarctic ice sheets did not form until the early Miocene when there was a circulation of a deep current through Drake Passage between Antarctica and Australia. But there is now evidence that ice sheets probably first formed in the Eocene c. 42 Ma (Keller et al., 1992). At Seymour Island, the La Meseta Formation of the middle-late Eocene has yielded a rich fauna of marine invertebrates as well as fossils of fishes, penguins, whales and marsupials. Some of the bivalves and decapods represent first occurrences of taxa that appeared later on at lower latitudes (Crame, 1994). At first, the Antarctic ice may have waxed and waned with minor climatic cycles, but by late Oligocene time, c. 25 Ma, it appears that a major icepack grounding event took place (Bartek et al., 1992). This is consistent with terrestrial evidence indicating the presence of glaciers and tundra by the early Oligocene (Janis, 1993). The presence of a major icepack in the Antarctic in the late Oligocene suggests that the modern, cold sea surface temperature regime (+2 °C to −2 °C) had become established. By that time, much of the rich Eocene fauna had disappeared, except for animals such as the penguins, whales, fishes, and several of the bivalves and gastropods that remained to become ancestral elements of the modern marine fauna. Late Oligocene–early Miocene fossils from other parts of Antarctica show surprisingly close resemblances to living taxa (Clarke & Crame, 1989). The shelf waters of the Antarctic and Sub-Antarctic are now occupied by a highly distinctive fauna that owes its origin to four historical factors: (1) persistence of a small ancestral group of Mesozoic and early Cenozoic taxa, (2) extinction of many early Tertiary warm-temperate species, (3) geographical isolation produced by the opening of Drake Passage, and (4) invasions by cold-temperate species from the northern hemisphere. The Antarctic Biogeographical Region is divisible into three provinces. The South Polar Province includes the Antarctic continent itself plus the South Shetland, South Orkney and South Sandwich Islands. South Georgia Island and Bouvet Island have many endemic species and each is placed in a province of its own. The Sub-Antarctic is the one biogeographical region on the world that is entirely made up of small, oceanic islands. Within that Region, The Kerguelen Province includes not only Kerguelen Island itself, but also the McDonald, Heard, Prince Edward and Crozet Islands. Macquarie Island has a high degree of endemism indicating that a Macquarie Province should be recognized (Briggs, 1995). The faunal distinctiveness of the Antarctic Region is almost incredible. In the major invertebrate groups, more than half the species are endemics (Knox, 1994). In the fishes, the endemic rate is c. 95% (Gon & Heemstra, 1990; Miller, 1993). Considering the 20+ Myr of isolation, this degree of species endemism might be expected. However, there are also large numbers of endemic genera; for fishes it is c. 70%. For one suborder of fishes, the Notothenioidei, the Antarctic is the site of a major evolutionary radiation. This group, consisting of five families, forty-six genera and 122 species (Nelson, 1994), dominates the ichthyofauna. Notothenioids often comprise 80–90% of the species in Antarctic fish catches. Some of them demonstrate remarkable adaptations to the coldest water (−1.9 °C) by having a glycoprotein in their blood that lowers the freezing point, a lack of red blood cells and aglomerular kidneys. The shelf and upper slope of the Antarctic Region supports 213 fish species. Of these, ninety-six are notothenioids, sixty-seven liparidids (Liparididae) and twenty-three zoarcids (Zoarcidae). Together these three groups comprise 88% of the fish fauna (Eastman, 2000). Unlike the latter two groups, that apparently represent invasions from the North Pacific, the notothenioids probably arose in the Antarctic vicinity. A fossil skull originally identified as a gadiform fish (Eastman & Grande, 1989) has been found to be a notothenioid (Balushkin, 1994). This fossil, from the late Eocene of Seymour Island, Antarctic Peninsula, is the first known fossil of the suborder. In the course of their evolution, the notothenioids adapted to a wide variety of ecological niches (Eastman & Grande, 1989). At the same time, they dispersed in a biogeographical sense. The most primitive (plesiomorphic) of the five families is generally considered to be the Bovichthyidae. Its distribution is almost entirely Sub-Antarctic with some species ranging as far north as New Zealand and Australia. One species inhabits freshwater streams in Australia and Tasmania. The Nototheniidae, the second most primitive family, is widely distributed in both the Antarctic and Sub-Antarctic. The remaining three families, usually considered the most advanced (apomorphic) (Iwami, 1985), are mainly confined to the Antarctic continent. This kind of phylogenetic pattern, in which the more primitive groups occupy the periphery, is a centre of origin characteristic. Notothenioid phylogeny has also been investigated using mitochondrial DNA analysis (Bargelloni et al., 2000). The results confirmed repeated dispersals outward across the Antarctic Convergence, often followed by speciation. Within the notothenioid families Nototheniidae and Channichthyidae, the most primitive genera may be seen to have peripheral distributions (Andriashev, 1986). The Notothenioidei belongs to the order Perciformes and no definite perciform fossils have been found that are older than the Tertiary (Patterson, 1993). Most authors have correlated the radiation of the suborder with the cooling and subsequent isolation of Antarctica (Anderson, 1990). However, the discovery of the late Eocene notothenioid places it in a warm-temperate fauna along with many other warm water species. Considering the impressive amount of evolutionary change that has taken place, the notothenioids may have originated in the earliest Tertiary or even in the late Cretaceous. The Antarctic is an evolutionary centre for penguins (Spheniscidae). Fossils have been found from the Eocene, Oligocene, Miocene, Pliocene and Pleistocene and all finds have been made in the circum-Antarctic area where penguins still occur (Simpson, 1974; Carroll, 1988). At times in the past, there were many more species but most of them have become extinct. The modern fauna consists of six genera and eighteen species. From their diversity centre in the Antarctic, penguins have spread to northern Chile and the Galapagos Islands, southern Africa, Amsterdam Island in the southern Indian Ocean and New Zealand. Antarctica, because of fossil discoveries in its peninsula region, has been steadily assuming greater importance as a centre of origin for Southern Ocean invertebrates. Crame (1996) published a list of living molluscan genera found in present day New Zealand, Australia, or southern South America, that have their earliest fossil records in the La Meseta Formation. The list includes ten genera in six families. In addition, several additional genera from the same formation were noted to have become even more widespread. In the same work, Crame included an extensive list of bipolar mollusca. However, almost all the examples involved relationships between the cold-temperate zones of each hemisphere rather than strictly Antarctic vs. Arctic. Two species of benthic sea-weeds of probable Antarctic origin also exist in the Arctic (van Oppen et al., 1993), but they are also broadly distributed in the cold-temperate waters of both hemispheres. The continual sinking of cold, saline water adjacent to the Antarctic continent and its subsequent movement northward at abyssal depths has had important biogeographical consequences. Historic dispersals from the Antarctic to the major ocean basins and trenches have been proposed for a large number of invertebrate families and genera (references in Vinogradova, 1997). For example, the holothurian family Elpidiidae apparently originated in the Antarctic, then dispersed northward through the Atlantic to the Arctic Ocean and also through the Pacific to the Bering Sea (Gebruk, 1990). The marine isopods in the deep sea may have been introduced to that environment via the Antarctic (Kussakin, 1973). As cold water was conducted into the deep sea from the late Eocene through the Oligocene, it caused significant extinctions. But, at the same time, it created a habitat suitable for the introduction of cold-acclimated organisms from the Antarctic. As a centre of origin, the Antarctic may have had its greatest effect on the abyssal and hadal zones. In addition to its production of species that have invaded other areas, the Antarctic has provided a refuge for phylogenetic relicts. The most generalized gadiform family is probably the Muraenolepididae. Its four species are found on the shelf and slopes of the Antarctic and Sub-Antarctic, thus inhabiting the southern periphery of the order (Andriashev, 1988; Howe, 1990). The lantern fishes of the family Myctophidae originated in the tropical waters of the Tethys Sea but the three most primitive genera are now confined to the Antarctic and Sub-Antarctic (Andriashev, 1988). For the invertebrates, Antarctica has been described as one of the last strongholds of the brachiopods, together with hexactinellid sponges and certain bivalve genera (Crame, 1994). Gastropod relicts include some genera of volutes and marginellids (Powell, 1951). The Antarctic regions have also provided a refuge for groups that have obviously invaded from the far north. Because such immigrants are not usually found in the intervening tropics, their distribution patterns are usually called bipolar. However, in most cases the term bipolar is misnomer, for the majority of the invaders appear to have originated in the northern cold-temperate seas rather than in the Arctic. Among the fishes, the dominant Antarctic groups, aside from the notothenioids, are the families Liparididae, Zoarcidae and Rajidae. The family Liparididae is of north Pacific origin (Andriashev, 1986). Members of the genus Paraliparis, a deep-water group, made their way to the Antarctic via the south American west coast. The family Zoarcidae is also of north Pacific origin and also reached Antarctic waters by moving down the west coast route and across the Scotia Ridge (Anderson, 1988). In his analysis of the history of the Rajidae, Long (1994) determined its origin to have been in the western Tethys and in the boreal seas of western Europe. It apparently dispersed to Antarctica in the early to middle Eocene along the western margin of the Atlantic. There are seven endemic rajid (skate) species in Antarctic waters. Like the notothenioids, they are represented by ancestral fossils from the late Eocene of Seymour Island. Yet the rajids have changed very little in the last 40 Myr. The three fish families and most of the molluscs that have invaded from northern seas probably did so my means of isothermic submergence. But this seems unlikely for shallow water molluscs such as the littorinids and certain buccinids (Crame, 1996). Five species of seals belonging to the family Phocidae are found in Antarctic waters. They are commonly known as the Southern elephant, Crabeater, Ross, Leopard and Weddell seals. The family originated along the shores of the North Atlantic, apparently in the Miocene. They must have reached the Antarctic early in their evolution for each of the species is placed in its own genus (Jefferson et al., 1993). One of the four southern fur seals of the family Otariidae, the Antarctic fur seal, occurs on the Antarctic Peninsula. The others occur in the Sub-Antarctic or farther north. The family originated in the north Pacific (Carroll, 1988) and, as all of the southern species belong to the same genus, their dispersal to the southern hemisphere probably occurred more recently than that of the phocids. The westward convergence of North America on Eurasia, because of the opening of the North Atlantic, apparently resulted in the formation of a terrestrial connection in the late Cretaceous c. 80 Ma (Zonenshain & Napatov, 1989). Once formed, this Bering land bridge, often called 'Beringia', separated the warm-temperate marine biota of the North Pacific from that of the Arctic–North Atlantic. It has been generally thought that Beringia continued to act as a barrier until the opening of a seaway in the Pliocene, c. 3.5 Ma (Herman & Hopkins, 1980). But recent work on bivalves (Kafanov, 1999; Marinkovitch & Gladenkov, 1999) and Cancer crabs (Harrison & Crespi, 1999) indicate that the first Cenozoic opening took place earlier, perhaps as much as 6–12 Ma. After the mid-Eocene, a series of temperature declines in the circumpolar region resulted in the southward movement of the warm-temperate zone and its replacement by a cold-temperate regime. By c. 14 Ma, fossils of numerous boreal (cold-temperate) species and genera could be found in the North Pacific (Golikov & Scarlato, 1989). But, judging from its systematic distinctiveness, that biota probably began its development in the mid-Eocene c. 40 Ma. At the same time, similar temperatures probably existed in the Arctic–North Atlantic. When the Bering Strait first opened, it may have been shallow and provided only limited passage but, by c. 3.5 Ma, it apparently allowed an unrestricted mingling of biotas that had been separated for more than 70 Myr. The event of 3.5+ Ma has been called the Great Trans-Arctic Biotic Interchange (Briggs, 1995). Its biogeographical consequences have been evaluated, with an emphasis on the molluscan faunas, by Vermeij (1991). He identified 295 molluscan species that either took part in the interchange or had descended from taxa that did. Of these, 261 were determined to be of Pacific origin compared with thirty-four of Arctic–Atlantic origin. This gives a ratio of almost 8 : 1 in favour of the Pacific. The modern molluscan species diversity in the North Pacific is approximately twice as great as that of the Arctic–Atlantic. Although many of the molluscan species seemed to have had early Pleistocene origins, Vermeij determined that the vast majority arose by anagenesis (without lineage splitting) so that it was reasonable to suppose that there has been little diversification since the early Pliocene. This means that the asymmetry of the invasions cannot be accounted for by the 2 : 1 ratio in species diversity. There are two viable hypotheses that might account for the predominate success of the invaders from the Pacific: (1) the Pacific species, having come from a more diverse ecosystem, are competitively superior, or (2) an extinction event eliminated much of the Arctic–Atlantic fauna so that it was easy for the Pacific species to occupy the vacated niches. Vermeij (1991) emphasized the importance of the latter cause which he called an 'Hypothesis of Ecological Opportunity'. This is the same idea as 'Incumbent Replacement Model' presented by Rosenzweig & McCord (1991). Both are dependent on extinction to free ecological niches so that they can be occupied by an invader. Neither can explain how replacement occurs without the help of extinctions. At the time of the great interchange c. 3.5+ Ma, the Arctic Ocean was ice-free and boreal (cold-temperate) conditions still prevailed (Golikov & Scarlato, 1989). The final closure of the Panamanian Isthmus c. 3.1 Ma strengthened the Gulf Stream system and favoured the onset of glaciation on the northern continents (Barry, 1989). Raymo (1994) concluded that a major intensification of northern hemisphere glaciation took place between 2.9 and 2.4 Ma. As a result, most of the boreal species were eliminated and the modern Arctic fauna began to develop. Once established, the colder temperature of the Arctic waters prevented further penetration by boreal species, with the exception of some eurythermic arctic–boreal forms. This means that Atlantic boreal species of Pacific origin were already in place at least several hundred thousand years prior to the mid-Pliocene cooling episode. Therefore, it is not possible to ascribe the success of the Pacific invaders to an extinction in the Arctic–North Atlantic. It is more likely that the Pacific species, the products of a more highly diverse ecosystem, were the better competitors. The competition need not have been behavioural, but could have involved such factors as reproductive rate, individual size, or vulnerability to predators or parasites. One must bear in mind that some invading species can successfully establish themselves by insinuation. This strategy is applicable to species that have evolved so that the niche they occupy is unusual to the extent that the invader will not directly compete with a native species. Insinuation may be suspected when an invader succeeds in colonizing an area with a more diverse ecosystem. It might help explain the success of the thirty-four molluscan species that dispersed from the Arctic–Atlantic to the North Pacific. Although the molluscan movements are the best known, as a result of the detailed analysis by Vermeij (1991), almost all groups of North Atlantic macroinvertebrates and fishes possess some species of North Pacific ancestry. Among the fishes, the families Salmonidae, Osmeridae, Zoarcidae, Hexagrammidae, Cottidae, Agonidae, Liparididae, Stichaeidae and Pholididae probably originated in the North Pacific but, during the trans-Arctic interchange, contributed one or more species to the North Atlantic. The cod family Gadidae, on the other hand, developed primarily in the North Atlantic and contributed two species to the North Pacific. Among the marine mammals, fur seals and sealions of the family Otariidae and the walruses of the family Odobenidae originated in the North Pacific, while the seals of the Phocidae are of Atlantic–Mediterranean origin (Carroll, 1988), the eelgrass Zostera (Hartog, 1970) the red alga Phycodrys (van Oppen et al., 1995) and the kelp genus Laminaria (Estes & Steinberg, 1988) originated in the North Pacific, then spread to the North Atlantic. Molluscan research indicates that the trans-Arctic invaders in the Atlantic have generally broader ranges than do native species with pre-Pliocene Atlantic histories (Vermeij, 1991). The apparent evolutionary consequences are of interest. Of the trans-Arctic species that extend into the Atlantic, 48% are derived (speciated) forms. In the Pacific 29% are derived. This indicates a remarkably low level of speciation for the past 3.5 Myr. Vermeij suggested that speciation among marine organisms appears to be much less frequent than assumed by evolutionary biologists. However, there is a difference in species longevity between cold-temperate and tropical habitats. Data from studies of the biota on each side of the Panamanian isthmus, where the separation has been in effect for c. 3.1 Myr, indicate an exceedingly high level of speciation. Molluscan fossils have shown that c. 20–40% of early Pliocene boreal species in the North Pacific have become extinct; but in the boreal North Atlantic more than 50% of the early Pliocene species have been lost (Vermeij, 1989). Cooling episodes associated with northern hemisphere glaciation are generally recognized as the probable cause. Vermeij has maintained that cooling does not fully explain why the North Atlantic extinctions were so much greater, and that reduction in primary productivity must have played a part. But there are reasons why the North Atlantic, during glacial periods, undergoes more severe temperature declines (and extinctions) than does the North Pacific. The North Atlantic is a smaller ocean with a correspondingly smaller heat budget, and it is wide open to the inflow of ice from the Arctic Basin. The North Pacific is protected from ice and cold-water inflow by the Bering land bridge that has always been in place during glacial periods. Another important effect of the cooling of the northern oceans was the separation of the boreal biotas. We have noted that, prior to the first Pliocene cooling episode c. 2.4–2.9 Ma, a boreal biota existed throughout the North Pacific and the Arctic–North Atlantic. Boreal organisms, with the exception of some wide ranging arctic–boreal forms, were extirpated, by the temperature drop, from the Arctic Ocean as well as from the northern parts of the Pacific and the Atlantic. A result was the establishment of a new cold-water Arctic Biogeographical Region. In the Atlantic, an Arctic biota now extends southward to the Strait of Belle Isle in the west and to the Kola Fjord at the base of the Murmansk Peninsula in the east. Included are all of the waters around Greenland and the northern half of Iceland. In the Pacific, an Arctic biota extends southward to Cape Olyutorsky in the west and Nunivak Island in the east. In each ocean, these southern extensions meant that the original Pliocene boreal regions were divided into two, one to the east and the other to the west. Typical boreal species were no longer able to maintain amphipacific and amphiatlantic distributions and evolutionary change began to take place separately in each region. This is why we are now able to define a boreal region on each side of each ocean in terms of its endemic species. Molecular technology has been useful in analysing the genetic divergence displayed by some of the invaders from the North Pacific to the North Atlantic. Four distinct groups have been recognized (Cunningham & Collins, 1998). One group had apparently invaded c. 3.5+ Ma, then subsequently speciated on each side of the boreal Atlantic, but another group of early invaders had not speciated on each side. A third group showed evidence of a very recent migration, while a fourth apparently made two migrations, one early and the other recent. True boreal species should not be able to migrate through the Arctic Region but there is a minor eurythermic group of arctic–boreal species. The third and fourth groups identified probably consist of such species. Although the biota of the Arctic Region owes most of its origin to the boreal North Pacific and North Atlantic, it has developed an appreciable amount of endemism. About 24% of the echinoderm species are endemic (Anisimova, 1989), 14% of the bivalves (Fedyakov & Naumov, 1989), and 19% of the prosobranch gastropods (Golikov, 1989). Among the whales, there are two monotypic genera that belong to the plesiomorphic family Monodontidae. These are the white whale (Delphinapterus) and the narwhale (Monodon). The narwhale is strictly Arctic while the white whale ranges southward into the northern parts of the cold-temperate North Pacific and North Atlantic (Jefferson et al., 1993). In comparison, the Antarctic Region possesses many more endemic species and numerous endemic genera. The differences are attributable to the 25 Myr history of the cold Antarctic biota as opposed to less than 3.0 Myr for the Arctic. In addition to having a great influence on the biota of the Arctic and the North Atlantic, the North Pacific also had far-reaching effects on the southern hemisphere, the Antarctic and the deep sea. The cold-temperate waters of the North Pacific extend from the Arctic boundaries in the Bering Sea to southern California on the east coast and to about Wenchou, China and northern Japan on the west coast. That huge area may be subdivided into two regions and five provinces (Briggs, 1995). The rich marine biota of the North Pacific probably developed over a period of c. 40 Myr. In an evolutionary sense, this biota was an inheritance from warm-temperate and eurythermic tropical species that managed to adapt to the colder temperatures. Its high level of species diversity, compared with that of the North Atlantic, is the result of its larger size and more moderate temperature fluctuations. It has a larger heat budget and during the glacial stages it was protected from the influence of the Arctic Ocean by the Bering land barrier. The North Pacific Centre has contributed a variety of organisms to the cold-temperate southern hemisphere. The migrations took place primarily via isothermic submergence, whereby the species concerned could maintain a suitable temperature by moving beneath the tropics at great depth. Most cases of interhemispheric, isothermic submersion involved populations that have become separated long enough to become distinct at the species or generic level. For example, the fish genus Sebastes (family Scorpaenidae) is extraordinarily diverse in the North Pacific, being represented there by almost 100 species. This genus is represented along the Chilean coast, Tierra del Fuego, the Falkland Islands, Tristan da Cunha and the tip of South Africa (Eschmeyer & Hureau, 1971). A recent molecular study has determined that a total of three species may now be recognized (Rocha-Olivares et al., 2001). All three apparently stem from a single migration that took place through the Eastern Pacific (EP) within the past 200 ka. As noted in the Antarctic account, two other fish families of North Pacific origin are represented by numerous species around the Antarctic continent, the Liparididae and the Zoarcidae. Both are capable of penetrating deep water and probably migrated using isothermic submergence. The Liparididae has an interesting distributional history that has been worked out by Andriashev (1986). The shallow water liparidids of the North Atlantic evidently reached that area during the trans-Arctic biotic interchange. However, members of the genus Paraliparis, a deep water group, made their way to the Antarctic along the west coast of the Americas. From the Antarctic, the genus dispersed northward along the mid-Atlantic ridge and thence to the Arctic Basin. As a result, the liparidid fauna of the Arctic–North Atlantic owes its origin to two migratory groups, the shallow water genera come directly through the Arctic Ocean while the deep water paraliparids migrated all the way to the Antarctic via the EP, then reached the Arctic Basin via the Atlantic. The Zoarcidae probably made its way south in the same manner as Paraliprais. It has speciated extensively in Antarctic and Sub-Antarctic waters (Anderson, 1988). A different tropical submersion route has been suggested for the fish family Cottidae. The southern hemisphere species of this family belong to a distinct genus (Antipodocottus), while the family itself is undoubtedly of North Pacific origin. It has been determined that Antipodocottus is most closely related to Atopocottus tribranchius, a Japanese species (Nelson, 1985). Nelson indicated agreement with Bolin (1952) that the invasion route was probably from Japan southward by way of the Philippines, New Guinea and the New Hebrides. The large brown algae or kelps of the Order Laminariales belong to four families, all of them found in the North Pacific. Three of the families are large and each of these has representatives in the southern oceans. Estes & Steinberg (1988) concluded that the centre of origin for the Order was in the North Pacific and that the southern species must have reached their present ranges via dispersal. Four of the southern species belong to the genus Laminaria. This genus also exists in the North Atlantic and has been taken in deep water off Brazil. So its route south may have been through the Western Atlantic (WA). However, two other southern genera (Macrocystis and Ecklonia) do not exist in the North A
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