The tropical history and future of the Mediterranean biota and the West African enigma

Authors


Geerat J. Vermeij, Department of Geology, University of California at Davis, Davis, CA 95616, USA.
E-mail: gjvermeij@ucdavis.edu

Abstract

Aim  Since the opening of the Suez Canal in 1869, many tropical taxa from the Indo-West Pacific (IWP) realm have entered the Mediterranean Sea, which is experiencing rising temperatures. My aims are: (1) to compare biogeographically this tropical transformation of the Mediterranean biota with the tropical faunas of the Mediterranean and adjacent southern European and West African seas during the Late Oligocene to Pliocene interval; (2) to infer the relative contributions of the tropical eastern Atlantic and IWP to the tropical component of the marine biota in southern Europe; and (3) to understand why West Africa is not now a major source of warm-water species.

Location  Southern Europe, including the Mediterranean Sea, and the coast of tropical West Africa.

Methods  I surveyed the literature on fossil and living shell-bearing molluscs to infer the sources and fates of tropical subgenus-level taxa living in southern Europe and West Africa during the Late Oligocene to Pliocene interval.

Results  Ninety-four taxa disappeared from the tropical eastern Atlantic (including the Mediterranean) but persisted elsewhere in the tropics, mainly in the IWP (81 taxa, 86%) and to a lesser extent in tropical America (36 taxa, 38%). Nine taxa inferred to have arrived in the tropical eastern Atlantic from the west after the Pliocene did not enter the Mediterranean. The modern West African fauna is today isolated from that of other parts of the marine tropics.

Main conclusions  Taxa now entering the Mediterranean through the Suez Canal are re-establishing a link with the IWP that last existed 16 million years ago. This IWP element, which evolved under oligotrophic conditions and under a regime of intense anti-predatory selection, will continue to expand in the increasingly warm and increasingly oligotrophic Mediterranean. The IWP source fauna contrasts with the tropical West African biota, which evolved under productive conditions and in a regime of less anti-predatory specialization. Until now, the post-Pliocene West African source area has been isolated from the Mediterranean by cold upwelling. If further warming should reduce this barrier, as occurred during the productive and warm Early Pliocene, the Mediterranean could become a meeting place for two tropical faunas of contrasting source conditions.

Introduction

As global temperatures rise, large-scale biogeographical changes are expected world-wide, some of which are already being observed. Many temperate species are expanding their ranges polewards and contracting their ranges at low latitudes (Barry et al., 1995; Rogers-Bennett, 2007; Jones et al., 2010) in the same way that species did during warm phases of the Pliocene and Pleistocene (Kafanov & Volvenko, 1997; Vermeij, 2005). Biogeographical change will not, however, be limited to latitudinal shifts in distribution. Warming with increased productivity in the Arctic Ocean is predicted to lead to increased penetration of North Pacific species into the North Atlantic (Vermeij & Roopnarine, 2008), as has already been observed for one diatom species (Reid et al., 2007). Transoceanic and intercontinental biotic contacts have generally been strongest during warm periods over the last 25 million years (Vermeij, 2005). Warming therefore affects both the latitudinal and longitudinal ranges of species.

The case with which the present paper is concerned involves the Mediterranean Sea, which is undergoing a rapid and dramatic transformation from a warm-temperate region to a warmer sea in which thousands of tropical species are becoming established owing largely to the human-constructed Suez Canal, which opened for navigation in 1869. Most of the immigrants come from the Red Sea, biogeographically part of the Indo-West Pacific (IWP) realm; a few fish species are coming in from the south and west through the Strait of Gibraltar; and other species are being carried by human-aided transport (Por, 2010). Superficially, this so-called tropicalization (Bianchi, 2007) will restore a biogeographical link between the Mediterranean and IWP that last existed during the Middle Miocene, about 16 million years ago (Ma). This new tropical signature will, however, differ substantially from that prevailing during the warm Early Pliocene (5 to 3 Ma), when most tropical elements in southern Europe had eastern Atlantic (that is, West African) affinities. The regional disappearance or outright extinction of many warm-water taxa living in the Mediterranean about 3 Ma, perhaps in part owing to the advance of northern glaciers southwards in latest Pliocene times, changed the Mediterranean biota into a warm-temperate one (Monegatti & Raffi, 2001, 2010; Monegatti et al., 2002). The tropicalization of southern European faunas has thus taken place from different source pools of species at different times. The modern biogeographical transformation of the Mediterranean biota raises three questions with broader implications. First, what factors prevent tropical West African and western Atlantic taxa from entering the Mediterranean today? Second, will tropical IWP taxa extend into the tropical Atlantic and, if so, how will they interact with the native species they will encounter there? Third, why did so many Late Oligocene to Middle Miocene elements in the Mediterranean and southern European biotas contract their ranges to the IWP and to a lesser extent to tropical America and not West Africa? In short, the biogeographical history of southern Europe (including the Mediterranean) may shed some light on the peculiarities of the West African marine biota and on the history of the marine tropics generally. Moreover, the Mediterranean may serve as a laboratory in which to investigate the kinds of biogeographical alterations that will become much more common as global warming intensifies.

My aims here are to document and discuss patterns of geographical restriction of molluscan subgenus-level taxa that existed in the Mediterranean and nearby areas from the Oligocene to the Pliocene, and to speculate on the factors responsible for these patterns and for the unusual composition of today’s tropical West African fauna. I also discuss patterns of recent invasions of marine taxa to tropical West Africa in relation to the tropicalization of the modern Mediterranean fauna, and make tentative predictions of patterns of biogeographical mixing in the future warm Mediterranean.

Materials and methods

I searched the primary taxonomic and phylogenetic literature in order to identify subgenus-level molluscan taxa that disappeared from tropical southern European seas between the Late Oligocene and Early Pliocene and that subsequently became restricted to tropical regions outside the eastern Atlantic. The compilation is necessarily incomplete, because not all molluscan groups have been subjected to the required comparative analysis in the literature. I have not used the earlier compilation of Robba (1987), because most of the taxa listed by him were either incorrectly identified or have been substantially revised by later authors. I performed my analysis at the level of subgenus, a category assumed here to represent a clade. The regional southern European disappearance of a subgenus almost always implies the extinction of eastern Atlantic species. Persistence of the subgenus elsewhere in the tropics thus means that other species in the subgenus-level clade continued to live in those other regions, and does not mean that southern European species underwent geographical restriction.

Results and discussion

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.
TaxonLast Mediterranean appearanceRefugesReferences
AcanthotrophonOA, P 
AilinzebinaOALozouet, 1999
AmaldaPlI, ALozouet, 1992; Landau & da Silva, 2006
AngariaOI 
AstraliumEMILozouet et al., 2001
BabyloniaUMIGittenberger & Goud, 2003; Gittenberger & Uit de Weerd, 2005
BicatillusEMILozouet et al., 2001
BuccinariaUMIBeets, 1944; Bouchet & Sysoev, 1997
CampanileEMILozouet et al., 2001
CittariumOALozouet, 2002
Clinura-ThatcheriaUMIBeets, 1942
CochlespiraEMIPowell, 1966
ColubrariaEMIHarzhauser, 2009
ConomitraUOABouchet & Kantor, 2004
ConorbisOIPowell, 1966
CymatiellaEMILandau et al., 2009b; Beu, 2010
CypraeaEMIDolin & Lozouet, 2004
Discors-LyrocardiumPlIJ. J. ter Poorten, pers. comm. 5/11/2010
DolicholatirusUMI, AVokes, 1977b; Vermeij & Snyder, 2006
EunaticinaEMI, P 
FicusPlI, A, PLandau et al., 2004b
FissilabiaEMILozouet & Maestrati, 1994
GaleropsisEMI, A, PLozouet & Le Renard, 1998
GemmuloborsoniaUMISysoev & Bouchet, 1996
Globularia-CerninaEMILozouet et al., 2001
GourmyaEMI, PxLozouet et al., 2001
Hinea brasiliana groupEMILozouet & Maestrati, 1994
IlyneritaUMIVermeij et al., 2009
IrravadiaUOILozouet, 2003
JenneriaEMAx, PLozouet et al., 2001
LampanellaEMAOzawa et al., 2009
LeptoconchusUMI, AxLozouet & Le Renard, 1998
LindapterysUMI, ALozouet et al., 1994; Vokes, 1996
LyncinaEMIDolin & Lozouet, 2004
MaleaPlI, A, PLandau et al., 2004b; Beu, 2010
MarmarostomaEMICluzaud & Cahuzac, 2006a,b; Williams, 2008; Williams et al., 2008
MauritiaEMIDolin & Lozouet, 2004
MeiocardiaPlIMatsukuma & Habe, 1995; Monegatti & Raffi, 2001
MelongenaUMI, A, PVermeij & Raven, 2009
MicrogazaPlALandau et al., 2004a; Simone & Cunha, 2006
MicroliotiaUMILe Renard & Bouchet, 2003
MicrostiliferEMILozouet, 1998
NaquertiaEMI, AxLozouet et al., 2001
NeritopsisEMI, ALozouet et al., 2001
NihoniaEMILozouet & Canevet, 2008;
NucleolariaUOIDolin & Lozouet, 2004
OniscideaEMALozouet et al., 2001
OtopleuraEMI 
PachyrissoinaEMILozouet et al., 2001
PagodatrochusEMILozouet, 1998
PalisadiaOILozouet, 1999
PeasiellaEMILozouet et al., 2001
PerotrochusPlAHarasewych, 2002; Landau et al., 2003
PhenacovolvaUOIDolin & Lozouet, 2004
PholadomyaPlA 
PhyllocomaEMI, PLozouet et al., 2001
PinctadaPlI, A, PMonegatti & Raffi, 2001; Wada & Tëmkin, 2008
PisulinellaEMILozouet, 2004
PlacunaUOIMatsukuma, 1987
PlaziatiaEMAx, PDolin & Lozouet, 2004
PlesiotrochusEMILozouet et al., 2001
PleuroplocaPlAM.A. Snyder & Geerat J. Vermeij, in prep.
PolinicesEMI, A, P 
PonderiaOILozouet, 1998
ProjenneriaEMIxHarzhauser et al., 2007
PseudolatirusUMI 
PupaEMILozouet et al., 2001
PyrazisinusEMAxReid et al., 2008
RansoniellaEMIDolin & Lozouet, 2004
RetizafraEMILozouet, 1999
RhinoclavisEMIHoubrick, 1978
ScabricolaEMILozouet et al., 2001
ScaliolaEMILozouet, 1998
SconsiaEMIx, ABeu, 2005, 2010
ScutusOILozouet, 1999
SeptiferPlIMonegatti & Raffi, 2001
StephopomaOI, AxLozouet, 1999; Gibson-Smith & Gibson-Smith, 1982
StyliferinaEMILozouet et al., 2001
TectariusEMILozouet et al., 2001
TectusEMIWilliams et al., 2008
TerebraliaEMI, AxHoubrick, 1991; Lesport & Cahuzac, 2002; Reid et al., 2008
TessellataEMIDolin & Lozouet, 2004
TibiaEMIKronenberg & Burger, 2002
TrapeziumEMIMaestrati & Lozouet, 1995
TrisidosOI 
TudiclaEMI 
TurbinellaOI, A, PxVredenburg, 1924; Vokes, 1984, 1998
TyphisOID’Attilio & Hertz, 1988
VanikoroEMA, I, PLozouet, 1998
VaricospiraEMILozouet et al., 2001
VasumEMI, A, PVokes, 1966
VitulariaEMI, AxLozouet et al., 2001; Vokes, 1977a
VolemaEMILozouet et al., 2001; Vermeij & Raven, 2009
VolvatellaEMI, AValdes & 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).
Last appearance in MediterraneanNumber of refugial taxa
TotalIAP
Late Oligocene171371
Early to Middle Miocene5449159
Late Miocene121232
Early Pliocene11783

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.

Conclusions

The tropical history of the Mediterranean shows that the consequences of future warming will involve much more than the poleward spread of warm-adapted taxa. The future biota of the Mediterranean in particular, and of the world in general, depends on the species pools from which spreading taxa are drawn as well as on the nutritional and evolutionary regimes in both the donor and recipient regions. The intense anti-predatory selection to which shallow-water IWP species have been exposed throughout the Neogene and beyond has yielded a biota that is likely to be competitively more vigorous than that in the eastern Atlantic, where defensive and other specializations are much less well expressed (Briggs, 1967; Vermeij, 1978). The Mediterranean could become a fascinating meeting place for species from the tropical IWP and Atlantic, regions whose biotas have had separate and contrasting histories for at least 16 million years. Forecasting is perilous, but knowledge of the past can illuminate the biogeographical future.

Acknowledgements

I am most grateful to Pierre Lozouet and an anonymous referee for their detailed and helpful comments on this paper; to Bernard Landau for helpful discussions and references; and to Janice Cooper for valuable technical assistance.

Biosketch

Geerat J. Vermeij is an evolutionary biologist and palaeobiologist with interests in biogeography, extinction, molluscan systematics and adaptive morphology, and major patterns in the history of life. He works particularly with fossil and living molluscs but has written widely on other groups and topics, including economics.

Editor: Christine Maggs

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