Fossil record and biogeographical history
Before the Pleistocene, the shallow-water marine fauna of southern Europe and West Africa, including the Mediterranean Basin, constituted a more or less unified biogeographical entity extending from north-western France to southern Angola (Brébion, 1981; da Silva & Landau, 2007). At times, this fauna exhibited the highest diversity of any fossil fauna known. Lozouet (1998, 1999) recorded some 1600 molluscan species from the Late Oligocene of south-western France alone. Before the Middle Miocene, a marine connection existed between southern Europe and the Indian Ocean (Harzhauser et al., 2002, 2007; Harzhauser, 2009), although some biogeographical divergence between these two regions had already taken place by the Late Oligocene. This faunistic link with the Indo-West Pacific (IWP) realm was first severed during the Early Miocene (Burdigalian), about 19 Ma, and became permanent in the Middle Miocene during the Langhian, about 16 Ma (Harzhauser, 2009). Periodic cooling and perhaps isolation caused numerous tropical taxa to disappear from the eastern Atlantic at various times from the Late Oligocene to the Late Pliocene, leaving the Mediterranean with an increasingly temperate fauna with affinities to the temperate eastern Atlantic (Monegatti & Raffi, 2010). During Pleistocene glacial episodes, the Mediterranean was invaded by cold-adapted North Atlantic taxa, some with ultimate origins in the North Pacific (Malatesta & Zarlenga, 1986; Raffi, 1986).
My compilation of Late Oligocene to Early Pliocene subgenus-level molluscan taxa that disappeared from southern Europe but survived in tropical regions outside the eastern Atlantic contains 94 taxa (Table 1). Of these, 81 (86%) found refuge in the IWP realm, and 36 (38%) did so in tropical America (33 in the western Atlantic, 15 in the eastern Pacific; see Table 2). The IWP served as sole refuge for 57 taxa, whereas tropical America was the only refuge for 12 taxa. Not all the taxa persisted in these refuges until the present day; regional disappearance affected eight western Atlantic refugees, two eastern Pacific ones, and three IWP ones. Of the 94 refugial taxa, two (Projenneria and Pyrazisinus) became globally extinct. The southern European taxa that survived later only in the IWP disappeared from the eastern Atlantic mainly by the end of the Oligocene (10 taxa) or during the first half of the Miocene (37 taxa).
Table 1. Molluscan subgenus-level taxa in the Mediterranean that became restricted to tropical regions outside the eastern Atlantic. Last Mediterranean appearance is categorized as Late Oligocene (O), Early to Middle Miocene (EM), Late Miocene (UM), or Pliocene (Pl); refuges are Indo-West Pacific (I), western Atlantic (A), or eastern Pacific (P); x denotes extinct.
|Acanthotrophon||O||A, P|| |
|Amalda||Pl||I, A||Lozouet, 1992; Landau & da Silva, 2006|
|Astralium||EM||I||Lozouet et al., 2001|
|Babylonia||UM||I||Gittenberger & Goud, 2003; Gittenberger & Uit de Weerd, 2005|
|Bicatillus||EM||I||Lozouet et al., 2001|
|Buccinaria||UM||I||Beets, 1944; Bouchet & Sysoev, 1997|
|Campanile||EM||I||Lozouet et al., 2001|
|Conomitra||UO||A||Bouchet & Kantor, 2004|
|Cymatiella||EM||I||Landau et al., 2009b; Beu, 2010|
|Cypraea||EM||I||Dolin & Lozouet, 2004|
|Discors-Lyrocardium||Pl||I||J. J. ter Poorten, pers. comm. 5/11/2010|
|Dolicholatirus||UM||I, A||Vokes, 1977b; Vermeij & Snyder, 2006|
|Eunaticina||EM||I, P|| |
|Ficus||Pl||I, A, P||Landau et al., 2004b|
|Fissilabia||EM||I||Lozouet & Maestrati, 1994|
|Galeropsis||EM||I, A, P||Lozouet & Le Renard, 1998|
|Gemmuloborsonia||UM||I||Sysoev & Bouchet, 1996|
|Globularia-Cernina||EM||I||Lozouet et al., 2001|
|Gourmya||EM||I, Px||Lozouet et al., 2001|
|Hinea brasiliana group||EM||I||Lozouet & Maestrati, 1994|
|Ilynerita||UM||I||Vermeij et al., 2009|
|Jenneria||EM||Ax, P||Lozouet et al., 2001|
|Lampanella||EM||A||Ozawa et al., 2009|
|Leptoconchus||UM||I, Ax||Lozouet & Le Renard, 1998|
|Lindapterys||UM||I, A||Lozouet et al., 1994; Vokes, 1996|
|Lyncina||EM||I||Dolin & Lozouet, 2004|
|Malea||Pl||I, A, P||Landau et al., 2004b; Beu, 2010|
|Marmarostoma||EM||I||Cluzaud & Cahuzac, 2006a,b; Williams, 2008; Williams et al., 2008|
|Mauritia||EM||I||Dolin & Lozouet, 2004|
|Meiocardia||Pl||I||Matsukuma & Habe, 1995; Monegatti & Raffi, 2001|
|Melongena||UM||I, A, P||Vermeij & Raven, 2009|
|Microgaza||Pl||A||Landau et al., 2004a; Simone & Cunha, 2006|
|Microliotia||UM||I||Le Renard & Bouchet, 2003|
|Naquertia||EM||I, Ax||Lozouet et al., 2001|
|Neritopsis||EM||I, A||Lozouet et al., 2001|
|Nihonia||EM||I||Lozouet & Canevet, 2008;|
|Nucleolaria||UO||I||Dolin & Lozouet, 2004|
|Oniscidea||EM||A||Lozouet et al., 2001|
|Pachyrissoina||EM||I||Lozouet et al., 2001|
|Peasiella||EM||I||Lozouet et al., 2001|
|Perotrochus||Pl||A||Harasewych, 2002; Landau et al., 2003|
|Phenacovolva||UO||I||Dolin & Lozouet, 2004|
|Phyllocoma||EM||I, P||Lozouet et al., 2001|
|Pinctada||Pl||I, A, P||Monegatti & Raffi, 2001; Wada & Tëmkin, 2008|
|Plaziatia||EM||Ax, P||Dolin & Lozouet, 2004|
|Plesiotrochus||EM||I||Lozouet et al., 2001|
|‘Pleuroploca’||Pl||A||M.A. Snyder & Geerat J. Vermeij, in prep.|
|Polinices||EM||I, A, P|| |
|Projenneria||EM||Ix||Harzhauser et al., 2007|
|Pupa||EM||I||Lozouet et al., 2001|
|Pyrazisinus||EM||Ax||Reid et al., 2008|
|Ransoniella||EM||I||Dolin & Lozouet, 2004|
|Scabricola||EM||I||Lozouet et al., 2001|
|Sconsia||EM||Ix, A||Beu, 2005, 2010|
|Septifer||Pl||I||Monegatti & Raffi, 2001|
|Stephopoma||O||I, Ax||Lozouet, 1999; Gibson-Smith & Gibson-Smith, 1982|
|Styliferina||EM||I||Lozouet et al., 2001|
|Tectarius||EM||I||Lozouet et al., 2001|
|Tectus||EM||I||Williams et al., 2008|
|Terebralia||EM||I, Ax||Houbrick, 1991; Lesport & Cahuzac, 2002; Reid et al., 2008|
|Tessellata||EM||I||Dolin & Lozouet, 2004|
|Tibia||EM||I||Kronenberg & Burger, 2002|
|Trapezium||EM||I||Maestrati & Lozouet, 1995|
|Turbinella||O||I, A, Px||Vredenburg, 1924; Vokes, 1984, 1998|
|Typhis||O||I||D’Attilio & Hertz, 1988|
|Vanikoro||EM||A, I, P||Lozouet, 1998|
|Varicospira||EM||I||Lozouet et al., 2001|
|Vasum||EM||I, A, P||Vokes, 1966|
|Vitularia||EM||I, Ax||Lozouet et al., 2001; Vokes, 1977a|
|Volema||EM||I||Lozouet et al., 2001; Vermeij & Raven, 2009|
|Volvatella||EM||I, A||Valdes & Lozouet, 2000|
Table 2. Numbers of regionally extinct Mediterranean molluscan subgenus-level taxa surviving later in tropical refuges outside the eastern Atlantic: Indo-West Pacific (I), western Atlantic (A), and eastern Pacific (P).
|Early to Middle Miocene||54||49||15||9|
The fossil record of West Africa is woefully meager, being represented in the Neogene only by some Early to Middle Miocene deposits in southern Angola (Douvillé, 1933; Brébion, 1983; Lozouet & Gourgues, 1995). In addition to some elements still typical of today’s West African fauna (Anazola, Clavatula, Luizia, Olivancillaria, Perrona, Peyrotia, Purpurellus and Senilia) (see also Vermeij, 1998), at least five taxa in the Angolan Miocene are held in common with southern Europe and became restricted later to tropical areas outside the eastern Atlantic. These are Babylonia and Tibia, both now confined to the IWP; and Malea, Melongena and Vasum, all found today throughout the tropics except in West Africa. As noted by Brébion (1981, 1983), West Africa and southern Europe belonged to the same biogeographical province during the Early Miocene.
The tropical taxa that became regionally extinct in southern Europe and West Africa comprise an ecologically heterogeneous assemblage. Many are hard-bottom, reef-associated taxa, including the trochid Tectus, the turbinids Astralium and Marmarostoma, cypraeoidean cowries (Cypraea, Jenneria, Lyncina, Mauritia, Nucleolaria, Phenacovolva, Plaziatia, Projenneria, Ransoniella and Tessellata), muricids (the coralliophilines Galeropsis and Leptoconchus and the muricopsine Lindapterys), and the turbinellid Dolicholatirus. Several live in cryptic reef environments, including Microliotia, Neritopsis, Pisulinella and Vanikoro; still others are high intertidal specialists, including the littorinids Peasiella and Tectarius and planaxids (Fissilabia and the Hinea brasiliana group). The inshore mangrove and mud-flat environment was also hard hit, with the regional loss of Fissilabia, Ilynerita, Melongena, Placuna, Pyrazisinus, Terebralia and Volema. Regionally extinct sand-dwelling taxa comprise at least 22 taxa including Babylonia, Buccinaria, Campanile, Eunaticina, Ficus, Globularia, Meiocardia, Nihonia, Otopleura, Pupa and Turbinella.
The regional disappearance in the eastern Atlantic of many reef-associated molluscs is understandable in view of the absence of true coral reefs and the rarity and low diversity of reef-forming corals in West Africa (five species; Laborel, 1974). The coast of tropical West Africa today is characterized either by upwelling or, where upwelling is absent (Guinea to western Ivory Coast and the eastern Gulf of Guinea), by extensive freshwater runoff (Le Loeuff & von Cosel, 1998). Both these conditions are inimical to the development of coral reefs.
More puzzling is the regional eastern Atlantic disappearance of taxa that have a strictly continental-coastal distribution and that have a greater tolerance of the conditions now prevailing in West Africa. To this large group of molluscan taxa belong Amalda, Babylonia, Bicatillus, Buccinaria, Campanile, Clinura, Ficus, Globularia, Ilynerita, Meiocardia, Melongena, Pagodatrochus, Pholadomya, Pseudolatirus, Pyrazisinus, Terebralia, Tibia, Trisidos, Tudicla, Turbinella, Varicospira and Volema. The absence of tropical seagrass beds in West Africa south of Mauritania may account for some of these losses (e.g. Turbinella and Volema), but a similar near-absence of seagrasses in the tropical eastern Pacific (den Hartog, 1970; Larkum & den Hartog, 1989) is not associated with the large-scale extinction of molluscs.
Numerous subgenera known from the Late Oligocene to Pliocene of the Mediterranean and elsewhere in southern Europe have since become restricted to West Africa, emphasizing the close biogeographical ties between tropical elements in the fossil record of southern Europe and the modern West African fauna. Well-documented examples include Theliostyla (Vermeij et al., 2009), Peyrotia (Ryall & Vos, 2010), the cypraeids Schilderia and Trona (Dolin & Lozouet, 2004), Persististrombus (Kronenberg & Lee, 2007), Distorsio (Landau et al., 2004b), the muricid Jaton (Vermeij & Houart, 1996), three nassariids (Cyllene, Demoulea and Dorsanum) (Allmon, 1990; Landau et al., 2009a), Polygona (Vermeij & Snyder, 2006), the olivids Oliva and Olivella (Lozouet, 1992; Landau & da Silva, 2006), cancellariids (Admetula, Sveltia, and Tribia) (Verhecken, 2007), the turrid Kyllenia (Garilli & Galletti, 2007), and all Terebridae (Bouchet, 1981). The cancellariid genus Loxotaphrus, whose last appearance in Europe was in the Middle Miocene, also survived in West Africa (Cahuzac et al., 2004; Verhecken, 2007).
Molluscs are not alone in showing these patterns. In his analysis of Mediterranean fish faunas of latest Miocene (Messinian) and Early Pliocene (Zanclian) age, Gaudant (2002) pointed to four taxa (Spratelloides, Eoliscus, Sargocentrum and Alutera) that have subsequently become restricted to the IWP. The coral genera Culicia and Pocillopora occurred in southern Europe and north-west Africa until the Early Miocene but have since disappeared from the eastern Atlantic. Pocillopora today occurs in the IWP and eastern Pacific and is also known from the Pleistocene of the Caribbean region, whereas Culicia is exclusively IWP (Boekschoten & Wijsman Best, 1981; Chaix & Cahuzac, 2005). The brachiopod genus Lingula, confined today to the IWP, occurred in Europe until the Middle Miocene (Serravallian) (Emig et al., 2007).
A few taxa now confined in the eastern Atlantic to West Africa colonized the Mediterranean during Pleistocene interglacial phases. These include the buccinid Gemophos (Vermeij, 2006), Theliostyla (Vermeij et al., 2009) and Persististrombus (Cornu et al., 1993; Detorres et al., 2010). Several tropical eastern Atlantic fish taxa have also been suggested as recently having entered the Mediterranean (Ben Rais Lasram et al., 2008).
Taxa expanding eastwards from tropical America to the Mediterranean and West Africa after the Pliocene can be identified by the absence of pre-Pleistocene fossils in the very rich Miocene and Pliocene faunas of southern Europe. At the subgeneric level these taxa include Bostrycapulus (Collin & Rolán, 2010), Chelyconus (Kraus et al., 2011), Gutturnium (Beu, 2010), Leucozonia (Vermeij & Snyder, 2002), Morula, Nodipecten (Smith, 1991), Thais (Vermeij, 2001), Tonna (Beu, 2010), and several species groups in Echinolittorina (Reid, 2009). Laborel (1974) noted a biogeographical pattern for West African corals that reinforces this post-Pliocene eastward spread of molluscs to West Africa. All West African corals are likely to be immigrants from the Caribbean or Brazil (Laborel, 1974), and none has entered the Mediterranean. The distributional patterns of post-Pliocene migrants to tropical West Africa therefore indicate that the tropical Atlantic source of warm-water species to the Mediterranean was cut off, whereas during and before the Pliocene it provided many species entering the Mediterranean from the south and west during warm periods.
Controls on patterns of invasion
The tropical waters of West Africa are today separated from the Mediterranean to the north and from the Indian Ocean to the south and east by long stretches of coast with intense cold upwelling. A regime of upwelling has existed in the vicinity of the northern Canary Current and the southern Benguela Current since the latest Miocene (Messinian) (Diester-Haass et al., 2002). Through the mid-Pliocene, however, temperatures in these upwelling regions were high, as they are along much of the coast of tropical West Africa, so that a strong thermal barrier among the Mediterranean, tropical West Africa, and the southern African region may not have existed. Low-temperature regimes comparable to today’s began with the onset of glaciation (Marlow et al., 2000). In the south, the advection of warm Indian Ocean waters into the South Atlantic via the so-called Agulhas leakage increased near the ends of glacial episodes and during interglacials (Peeters et al., 2004; Biastoch et al., 2009), with the possible result that species from the Indian Ocean could disperse around South Africa to the eastern and western Atlantic (Vermeij & Rosenberg, 1993; Floeter et al., 2008). Although upwelling in north-western Africa in the Canary Current system increases in intensity with higher sea-surface temperatures because of stronger longshore winds (McGregor et al., 2007), an effect also seen in the Arabian Sea (Goes et al., 2005), the upwelling there remains cold and thus does not support strictly tropical species. During the Early Pliocene, a regime of warm upwelling probably existed in the south-western Mediterranean, as indicated by the presence of the limpet Patella pellucida, which is associated with large seaweeds characteristic of nutrient-rich waters (da Silva et al., 2006). High productivity, probably linked to seasonal upwelling, is also indicated for the south-western Mediterranean during the Early Pliocene by the presence of abundant aggregations of large barnacles (Aguirre et al., 2008).
It was therefore not upwelling itself that created a barrier between tropical West Africa and the present-day Mediterranean or between West Africa and the Indian Ocean. Instead, cooling associated with the latest Pliocene advance of northern glaciers, exacerbated by decreases in planktonic productivity in the Mediterranean since the Pliocene, may be responsible. Because of these changes, some 20% of Early Pliocene Mediterranean bivalves and 71% of gastropods became extinct, mainly at about 3 Ma (Monegatti & Raffi, 2010; B.M. Landau, University of Lisbon, pers. comm.).
The climatic and oceanographic changes that led to the disappearance of many subgenus-level taxa from the eastern Atlantic and to their restriction to other tropical regions also isolated the biota of West Africa’s mainland coast from the rest of the marine tropics. During the warm Early Pliocene, the tropical eastern Atlantic species pool was still a prolific source of immigrants to the Mediterranean, but contraction of the West African tropics during the Late Pliocene largely cut off this source. In today’s warming Mediterranean, the primary source of tropical species is the IWP realm. Unlike the tropical eastern Atlantic biota, which evolved and still flourishes under a regime of high planktonic productivity thanks to seasonal upwelling or extensive input of land-based nutrients by rivers, the IWP biota in the Red Sea comes from a generally oligotrophic regime. The eastern parts of the Mediterranean Sea closest to the Suez Canal, through which Red Sea species are entering the Mediterranean, are becoming both warmer and more oligotrophic (Coma et al., 2009; Por, 2010) owing to the construction of the Aswan Dam on the Nile River in Egypt, which effectively eliminated a major source of terrestrial nutrients.
An additional difference between the two potential source regions for the Mediterranean biota is the degree of defensive specialization of their species, as indicated by the frequency and expression of such shell traits as a narrow aperture, development of tubercles and spines, and reinforced apertural margins. Shallow-water molluscs in the Indo-West Pacific, including the Red Sea, have a much higher incidence of anti-predatory traits than their tropical West African counterparts (Vermeij, 1978). This difference probably reflects a longer history and perhaps greater intensity of anti-predatory selection in the Indo-West Pacific realm than elsewhere in the tropics. The greater defensive prowess of Red Sea immigrants compared with potential immigrants from West Africa may further contribute to the differential success of these Indo-West Pacific migrants.
Although the taxonomic composition of the new tropical component in the Mediterranean does not duplicate the tropical component that disappeared from the eastern Atlantic during the Neogene, the new human-made connection between the IWP realm and the warming Mediterranean will restore the biogeographical link that last existed in this region before the Middle Miocene closure of the Tethys Seaway. As Por (2010) has emphasized, IWP taxa will continue to enter the Mediterranean, strengthening the biotic link and ultimately leading to the establishment of coral reefs, mangroves, and other ecosystems that today characterize the IWP realm but that have been absent from southern Europe since the end of the Miocene.
With the continuing rise in temperature in the Mediterranean, the cold-water barriers that now isolate West Africa from the Mediterranean may disappear, so that tropical Atlantic elements will again be able to enter the Mediterranean as they did during the reflooding of the Mediterranean in the Early Pliocene after the Messinian Crisis. Moreover, taxa entering the Mediterranean through the Suez Canal may spread to West Africa. An increasingly oligotrophic Mediterranean will probably be more receptive to IWP immigrants from the Red Sea than to eastern Atlantic immigrants from the planktonically productive waters of West Africa, but a future Mediterranean biota with both African and IWP elements can be expected.