PDF - MPB - Marine PalaeoBiogeography

Bull. Soc. géol. Fr., 2009, t. 180, no 4, pp. 295-307
How did they get here? The biogeography of the marine molluscs
of the Azores
SÉRGIO P. ÁVILA1,2,3, CARLOS MARQUES DA SILVA4, RALF SCHIEBEL5, FABBRIZZIO CECCA6,
THIERRY BACKELJAU7 and ANTÓNIO M. DE FRIAS MARTINS1,3
Key-words. – Pleistocene, Recent, Mollusca, Azores, routes of dispersal, Palaeobiogeography.
Abstract. – The geographical location of the Azores, midway between Europe and America, poses problems relative to
their colonization and the biogeographic affinity of the biota presently living there. In the way of the Gulf Stream, originating off American shores, the Azorean biota, marine and terrestrial alike is predominantly European. To explain this
distributional paradigm the present study investigates the Neogene fossil record of Santa Maria, Azores in order to establish the biogeographical relationships of the Pleistocene to Recent littoral molluscan fauna of this archipelago. The
bulk of the Azorean malacofauna, both in the Pleistocene (71.3%) and in Recent times (75.6%) is biogeographically related with the eastern Atlantic, and that the Pleistocene (Eemian) fossil fauna is basically the same as the Recent fauna,
with a few losses of tropical species and of shallow water bivalves associated to fine sand substrates.
It is hypothesized that during Pleistocene glacial-interglacial cycles, short-duration events have occurred during
which short-lived oceanic currents must have been established, especially during or shortly after glacial terminations.
During these short-term events, the arrival of species to the Azores may have been increased and facilitated by temporary sea-surface currents that no longer exist now. Probable routes of dispersal to the archipelago of the Azores are also
discussed, as well as the possible influence of the Pleistocene glaciations in the shallow water marine molluscs of these
islands.
Comment sont-ils arrivés ici ? Biogéographie des mollusques marins des Azores
Mots-clés. – Pléistocène, Actuel, Mollusques, Azores, Chemins de dispersion, Paléobiogéographie
Résumé. – La localisation géographique des Azores, à mi-chemin entre l’Europe et l’Amérique, pose des problèmes relatifs à leur colonisation et les affinités biogéographiques des biotas vivant là actuellement. Sur le tracé du Gulf Stream,
qui prend naissance sur les côtes américaines, les biotas azoréens, aussi bien marins que continentaux sont principalement européens. Pour expliquer ce paradigme de distribution, la présente étude porte sur l’enregistrement fossile néogène de Santa Maria, Azores, pour établir les relations biogéographiques des faunes de mollusques littoraux du
Pléistocène à l’Actuel de cet archipel. La majeure partie de la malacofaune azoréenne, à la fois au Pléistocène (71.3 %)
et à l’Actuel (75.6 %) est biogéographiquement en relation avec l’Est Atlantique, et les faunes fossiles du Pléistocène
(Eemien) sont dans l’ensemble les mêmes que celles de l’Actuel avec des pertes d’espèces tropicales et de bivalves
d’eau peu profondes associées aux substrats de sables fins.
L’hypothèse est émise que durant les cycles glaciaire-interglaciaire du Pléistocène, de courts événements ont eu
lieu durant lesquels des courants océaniques temporaires ont du s’établir, spécialement durant et peu de temps après les
fins de glaciation. Durant ces événements courts, les arrivées d’espèces aux Azores ont pu augmenter et être facilitées
par des courants de surface temporaires qui n’existent plus maintenant. Les chemins de dispersions probables vers l’archipel des Azores sont également discutés, ainsi que l’influence possible des glaciations pléistocènes sur les mollusques
d’eaux profondes de ces îles.
INTRODUCTION
It is known since the 19th century that the marine fauna of
the Northeast Atlantic archipelagos of Macaronesia (Azores,
Madeira, Selvagens and Canaries) has very diverse biogeo-
graphical affinities [MacAndrew, 1854; Ávila, 2000a, 2005;
Morton and Britton, 2000; Wirtz et al., 2003]. Due to its geographical location, the archipelago of the Azores is of crucial
importance to infer colonization patterns, to establish the
biogeographic historical relationships with related biotas and
1. Departamento de Biologia, Universidade dos Açores, 9501-801 Ponta Delgada, Azores, Portugal
2. Centro do IMAR da Universidade dos Açores, 9901-862 Horta, Azores, Portugal
3. MPB, Marine Palaeobiogeography Working Group of the University of the Azores, Rua da Mãe de Deus, 9501-801 Ponta Delgada, Azores, Portugal
4. Departamento e Centro de Geologia, Faculdade de Ciências, Universidade de Lisboa, Bloco C6, Campo Grande, 1749-016 Lisboa, Portugal
5. School of Earth and Ocean Science, National Oceanography Centre, Southampton, European Way, Southampton SO14 3ZH, United Kingdom
6. Université “Pierre et Marie Curie” – Paris VI, CNRS-UMR 5143 “Paléobiodiversité et Paléoenvironnements”, Tour 56-46, 5ème étage, case 104,
4, place Jussieu, 75252 Paris cédex 05, France
7. Royal Belgian Institute of Natural Sciences, Department of Invertebrates, Malacology Section, Vautierstraat 29, 1000 Brussels, Belgium
Manuscrit déposé le 30 novembre 2007 ; accepté après révision le 5 mars 2009.
Bull. Soc. géol. Fr., 2009, no 4
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ÁVILA S. P. et al.
to propose hypotheses on processes of dispersal, colonization
and speciation that occurred in these insular habitats.
In the Azores, Santa Maria Island is the only place
where both marine and terrestrial Neogene fossils are
found. Since the pioneer work of Mayer [1864], most of the
studies hitherto have focused on the Miocene-Pliocene marine taxa that are abundant in several outcrops [see Ávila et
al., 2002 for a list of references]. Therefore attention has recently moved to the Pleistocene marine molluscs of Santa
Maria [García-Talavera, 1990; Callapez and Soares, 2000;
Ávila et al., 2002].
Data about the Pleistocene molluscs from Santa Maria,
herein reported, will be used to compare and discuss the
Pleistocene and the Recent biogeographical relationships of
the shallow water (< 50 m) Azorean marine molluscs. Probable routes of dispersal to the archipelago of the Azores,
as well as the influence of the Pleistocene glaciation-interglaciation cycles are also discussed.
MATERIALS AND METHODS
Two Pleistocene marine fossiliferous outcrops are known at
Santa Maria : Lagoinhas, located in the north coast of the
island at +7.4 m above present sea-level and with a lateral
extension of less than 100 m; and Prainha, near the beach of
Praia Formosa, about 5 km east of Vila do Porto, with fossiliferous layers that extend for 800 m along the seashore at
the present height of +2 to +4 m (fig. 1). Ávila et al. [2002]
detailed and discussed the stratigraphic succession established by Zbyszewsky and Ferreira [1961, 1962] and by García-Talavera [1990] for the outcrop of Prainha, and by
Callapez and Soares [2000] for Lagoinhas. Ávila et al.
[2008a] have recently dated the basal sequence at Prainha
as corresponding to the Marine Oxygen Isotope Substage 5e
(MIS5e) (117-130 m.y.).
One hundred and three bulk samples were collected at
Prainha and two samples at Lagoinhas from February 2000
to June 2002 [Ávila et al., 2002]. New fossil material was
collected at the Lagoinhas outcrop in February 2003. Ten
bulk samples of sandy fossiliferous sediments (1 kg each)
were washed through a 0.5 mm mesh sieve. All mollusc remains found were sorted and identified. Recent collecting
from the fossiliferous strata of Prainha and Lagoinhas during the 2nd and 3rd Workshops “Palaeontology in Atlantic
Islands” (2005 and 2006) provided additional material. The
samples are deposited in the fossil collection of the Department of Biology of the University of the Azores (DBUA-F)
(the complete list of the samples is available at
http://www.uac.pt/~fosseis/DBUA-F.pdf).
The mode of larval development of the gastropods represented in the analyzed samples was inferred trough SEM
images of the protoconch morphology [Jablonski and Lutz,
1980]. This procedure was extended to most of the micro-molluscs shells obtained.
The palaeobiogeographical relationships of the Santa
Maria Pleistocene shallow-water marine molluscs were established by comparing the Prainha and Lagoinhas database
with data from the western Atlantic (Atlantic shores of Canada, U.S.A and the Caribbean), eastern Atlantic (Atlantic
shores of Europe and west Africa), the Mediterranean, and
the archipelagos of Macaronesia [for sources of data see
Ávila, 2000a, 2005].
Bull. Soc. géol. Fr., 2009, no 4
Abbreviations used in text
DBUA-F – reference collection of the fossil marine molluscs of the Azores
(Department of Biology of the University of the Azores, Ponta Delgada,
São Miguel Island, Azores) (http://www.uac.pt/~fosseis/DBUA-F.pdf).
DBUA – reference collection of the Recent marine molluscs of the Azores
(Department of Biology of the University of the Azores, Ponta Delgada,
São Miguel Island, Azores) (http://www.uac.pt/~fosseis/DBUA.pdf).
RESULTS
Ávila et al. [2002] reported 95 species from the outcrops of
Prainha and Lagoinhas (80 Gastropoda and 15 Bivalvia) of
which six were considered as dubious records (5 Gastropoda and 1 Bivalvia). The records of Tricolia pullus azorica
DAUTZENBERG, 1889 and of Bulla amygdala DILLWYN,
1817 (=B. mabillei LOCARD, 1897) previously reported by
Zbyszewsly et al. [1961] and García-Talavera [1990], but
not found by Ávila et al. [2002] are now confirmed.
Thirteen new records, some illustrated in figures 2-4
(three found at Prainha and the remaining 10 at Lagoinhas)
increase the number of species to 108 (92 Gastropoda and
16 Bivalvia), of which seven gastropods are considered dubious records (their identification needs confirmation): Rissoa similis SCACCHI, 1836; Rissoa ventricosa DESMAREST,
1814; Alvania canariensis (d’ORBIGNY, 1840); Alvania pagodula (BUCQUOY, DAUTZENBERG and DOLLFUS, 1884); Pusillina philippi (ARADAS and MAGGIORE, 1844); Pusillina
radiata (PHILIPPI, 1836) and Gibbula cineraria (LINNAEUS,
1758). In particular, Rissoa ventricosa and Pusillina radiata, both reported to the Prainha outcrop by García-Talavera
[1990], are most likely to be misidentifications, as these are
species with a strong connection to seagrasses beds, which
are unlikely to have occurred in the Azores (in the present,
there are also no seagrasses beds off the Azores). Thus, 101
is the updated number of species currently known from the
Pleistocene of Santa Maria Island (fig. 5, tabl. I).
The new records are: Cerithiopsis minima (BRUSINA,
1865); Littorina saxatilis (OLIVI, 1792); Alvania abstersa
VAN DER LINDEN and VAN AARTSEN 1994; Alvania formicarum GOFAS, 1989; Pusillina inconspicua (ALDER, 1844);
Nassarius incrassatus (STRØM, 1768); Columbella adansoni MENKE, 1853; Philippia hybrida (LINNAEUS, 1758);
Odostomella doliolum (PHILIPPI, 1844); Odostomia duureni
AARTSEN, GITTENBERGER and GOUD, 1998; Odostomia cf.
kuiperi AARTSEN, GITTENBERGER and GOUD, 1998 and the
bivalves Striarca lactea (LINNAEUS, 1758) and Pinna rudis
LINNAEUS, 1758 (tabl. I).
Seventeen, out of the 101 Pleistocene species presently
reported from Santa Maria Island, are endemic to the Azores, four are widespread in the Macaronesian archipelagos
and only 11 occur in the western Atlantic, most of them, in
the Caribbean area. In contrast, 71 species that were found
at Prainha and Lagoinhas also occur in the Pleistocene deposits from the eastern Atlantic/Mediterranean European
shores (tabl. I).
DISCUSSION
Biogeographical relationships of the Pleistocene
(Eemian) and Recent Azorean malacofauna
The location of the Azores in the middle of the north Atlantic renders this archipelago susceptible to colonization by
THE BIOGEOGRAPHY OF THE MARINE MOLLUSCS OF THE AZORES
TABLE I. – Checklist and geographical distribution of the 101 species reported to the Pleistocene outcrops of Prainha and Lagoinhas (Santa Maria
Island, Azores). AZO end – endemic species to the Azores. A – species/taxa collected by the authors; B – species/taxa reported but not collected by the authors.
TABL. I. – Liste et distribution géographique des 101 espèces reconnues
dans les affleurements du Pléistocène de Prainha et de Lagoinhas (Île de
Santa Maria, Azores). AZO end – espèces endémiques des Azores. A – espèces/taxa récoltés par les auteurs ; B – espèces/taxa reportés ici mais
non récoltés par les auteurs.
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TABLE I. – (following)
TABL. 1. – (suite)
species from both sides of the Atlantic. Several authors concluded that, notwithstanding the fact that the present day
prevailing currents in the Azores region would favour colonization from the western Atlantic, most of the recent littoral marine Azorean molluscs are biogeographically related
with the eastern Atlantic shores [Mac Andrew, 1854; Ávila,
2000a, 2005; Ávila and Albergaria, 2002]. Even considering only the Azorean endemic species, with the Rissoidae
accounting for almost half of the total number of endemisms [Ávila, 2000b, 2005], the present benthic littoral malacofauna of the Azores is clearly dominated by species in
common to European and/or Madeira and Canary Islands
coasts. Of the 299 (Recent) species of molluscs reported
from the Azores by Ávila [2005], 39 (13.0%) occur also at
the western Atlantic, whereas of the 101 taxa reported from
Pleistocene sediments of Santa Maria, 11 species were present in the western Atlantic (10.9%) (tabl. II). The bulk of
the Azorean malacofauna, both in the Pleistocene (71.3%)
and in Recent times (75.6%) is biogeographically related
with the eastern Atlantic. In the present time, Stramonita
haemastoma haemastoma (LINNAEUS, 1766), Charonia variegata (LAMARCK, 1816), Phalium granulatum (BÖRN,
1778), Conus ermineus BÖRN, 1778 and Polynices lacteus
(GUILDING, 1834) are amphi-Atlantic species [García-Talavera,
1981] as well as Skeneopsis planorbis (O. FABRICIUS,
1780). Laursen [1981] reported the larvae of Polynices lacteus
TABLE II. – Pleistocene and Recent biogeographical relationships of the
mollusc fauna from Prainha and Lagoinhas (Santa Maria, Azores).
TABL. II. – Relations biogéographiques pléistocènes et actuelles des faunes de mollusques de Prainha et Lagoinhas (Santa Maria, Azores).
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ÁVILA S. P. et al.
FIG. 1. – Geographical location of Santa Maria Island
in the Azores archipelago (A) and location of the sampling sites, Prainha and Lagoinhas (B). (c) Secção de
Geografia, Universidade dos Açores.
FIG.1. – Localisation géographique de l’île de Santa
Maria dans l’archipel des Azores (A) et localisation
des sites d’échantillonnage, Prainha et Lagoinhas
(B). (c) Secção de Geografia, Universidade dos Açores.
in the waters surrounding the Azores and, although Morton
et al. [1998] reported the adults of this species to the Azores, the authors have stated that it was erroneous information (in litt., 2004). The largest fossil specimen of Polynices
lacteus collected at Prainha is 1.8 x 1.4 cm but Ávila et al.
[2002] questioned the existence of viable recent populations
of this species in the Azores. In fact, more than 800 lots of
the DBUA collection (Recent shallow-water marine molluscs of the Azores) were surveyed and not a single specimen of this conspicuous gastropod was found [Ávila et al.,
1998, 2000a, 2000b; Ávila, 2005].
Except for the thermophilic species (the so-called
“Strombus accompanying fauna”) that presumably reached
the Azores during the transition from the Pleistocene marine isotope stage MIS6 to the MIS5e or shortly after that
(tabl. III) due to the higher sea-surface temperatures (SST),
the molluscan assemblages found at Prainha and Lagoinhas
are very similar to those described by Ávila [2000a, 2003]
Bull. Soc. géol. Fr., 2009, no 4
and Ávila et al. [2005] for the Recent littoral marine molluscs of the Azores, with a high number of Azorean species
that presently occur also at the Mediterranean, Portugal,
Madeira and the Canary Islands. This pattern of Recent biogeographical relationships is also observed in other well
studied organisms in the Azores : Porifera, Cnidaria
(Anthozoa), Annelida, Arthropoda (Crustacea), Echinodermata, Pisces [for a review and references see Morton and
Britton, 2000] and it is not consistent with the present pattern of sea-surface circulation of the North Atlantic [Käse
and Siedler, 1982; Gould, 1985; Kleine and Siedler, 1989;
Alves and Simões, 1997; Alves and Verdière, 1999; Alves
et al., 2002; Schiebel et al., 2002], thus a mechanism is needed to explain this apparent contradiction.
Previous authors [Mayer, 1864; Cotter, 1888-1892;
Friedlander, 1929; Agostinho, 1937; Berthois, 1950, 1951,
1953; Ferreira, 1952, 1955; Krejci-Graff et al., 1958; Zbyszewski et al., 1961; Zbyszewski and Ferreira, 1961, 1962]
THE BIOGEOGRAPHY OF THE MARINE MOLLUSCS OF THE AZORES
TABLE III. – Stratigraphic distribution and mode of larval development
(p – planktotrophic; np – non-planktotrophic) of the thermophilous species
collected in the Pleistocene of Prainha and Lagoinhas (Santa Maria Island,
Azores) and that subsequently locally disappeared from the Azores. The
stratigraphy of the outcrops follows Ávila et al. [2002]: a basal strongly
cemented calcareous conglomerate (unit A1), overlaid by a calcareous
algae mat (unit A2) and above a non-depositional hiatus surface, a sandy
beach deposit (unit B1).
TABL. III. – Distribution stratigraphique et mode de développement des
larves (p – planctotrophique ; np – non planctotrophique) des espèces
thermophiliques récoltées dans le Pléistocène de Prainha et Lagoinhas
(Île de Santa Maria, Azores) et qui disparaissent ensuite localement des
Azores. Stratigraphie des affleurements d’après Ávila et al. [2002] : à la
base un conglomérat calcaire fortement cimenté (unité A1), surmonté par
un tapis algaire calcaire (unité A2) et au-dessus une surface de hiatus sans
dépôt, un dépôt de sable de plage (unité B1).
all agreed that also the Miocene to Pliocene mollusc fauna
from Santa Maria has eastern Atlantic affinities. Preliminary results from our work at Santa Maria since 1998 show
that more than 96% of the Miocene-Pliocene molluscs of
Santa Maria are biogeographically related with the eastern
Atlantic.
Geological and oceanographical data
The Azores is an archipelago of about 8 Ma (Santa Maria
Island) [Madeira, 1986; Serralheiro et al., 1987; Serralheiro
and Madeira, 1990; Serralheiro, 2003]. As volcanic oceanic
islands, these once empty habitats had to be colonized from
elsewhere. The nearest colonizing source is the Madeira archipelago, presently at about 900 km southeast, but other
plausible sources are the Iberian and West European Atlantic shores, the Mediterranean, the western African shores,
the Canary Islands and also the Caribbean region.
The general pattern of oceanic circulation in the Northern Atlantic has been roughly the same since the closure
of the Isthmus of Panama, a complex, slow and progressive
process that begun about 13 Ma and finished with the complete separation between the Pacific and the Atlantic between 3.1 and 2.7 Ma ago [Coates and Obando, 1996; Haug
and Tiedermann, 1998]. Intermittent connections between
those oceans may have persisted into the Late Pliocene and
possibly during Early and Middle Pleistocene interglacial
periods [Beu, 2001; Landau et al., 2007]. The Gulf Stream
is the major hydrographical feature influencing the climate
in the Azores region. During glacial periods this large
sea-surface current was stronger than at present, with both
higher velocity and volume, due to the latitudinal descent of
the Polar Front [Crowley, 1981; Wunsch, 2003]. Moreover,
wind-velocities were higher than nowadays [Crowley and
North, 1991]. As a consequence, during the glacial episodes, the probability of western Atlantic specimens (larvae
and/or juveniles/adults) reaching the Azores would be
299
higher (warm-water Caribbean species, for instance). However, for the establishment of viable, reproductive populations in the Azores Islands, this would require the existence
of optimal SSTs both for the survival of larvae and, later,
for the accomplishment of successful reproductive phases
[Raffi, 1986]. Should these optimal thermal conditions not
exist the newly arrived molluscs would simply originate
“pseudopopulations” in the sense of Bouchet and Taviani
[1992] or “dependent populations” [Boehlert et al., 1994],
the maintenance of which would rely solely on the regular
arrival of new colonizers.
How to reach an oceanic island? Processes of dispersion
The dispersion of many benthic marine invertebrates is
achieved by means of pelagic larvae [Strathman, 1974],
which are dependent on the main sea-surface currents.
Other plausible means of dispersion are by foresy, that is,
transported by birds attached to their feathers, a common
feature in the case of some intertidal molluscs nowadays
present in the Azores [Ávila, 2000a], by rafts of egg-masses, juveniles or adults of small-sized species attached to
seaweeds [Highsmith, 1985; Ávila, 2006], to carapaces of
marine turtles [Frazier et al., 1985], pumice [Jokiel, 1984],
logs, and other suitable floating materials [Jokiel, 1990].
Gittenberger et al. [2006] have recently shown that terrestrial snails were transported by birds as far as from Europe
to the Azores islands. Birds are frequently blown off course
by strong winds. Strong easterly winds originating from
northwestern Africa and extending over the Atlantic as far
as the Caribbean Sea are a common feature, and are recorded by the presence of Saharan dust [Chester, 1971; Reis et
al., 2002; Petit et al., 2005]. It is therefore likely that at
least some of the intertidal species of the malacofauna of
Santa Maria (about 2% of the total Pleistocene species; Ávila, unpubl. data) have been introduced by birds, which have
been flown or blown over to the Azores from the western
shores of Europe. However, and with the possible exception
of some of the intertidal species, all of the others certainly
reached these islands by larval dispersion or by rafts. As the
Azores are not at midway between Europe and America, but
closer to Europe and Africa, in spite of the Gulf Stream, it
is more likely that larvae can reach the Azores more easily
from east (via the Macaronesian bridge, as discussed below)
than from the Caribbean.
Glacial terminations
During Pleistocene glacial-interglacial cycles, short-duration events have occurred during which short-lived oceanic
currents must have been established, especially during
and/or shortly after glacial terminations. Fifteen such cycles
have occurred during the last million years [Wilson et al.,
2000]. The penultimate interglaciation begun about
130,000 y ago and was preceded by a rapid glacial termination (Termination II, 132,000-126,000), a 6,000 y event during which sea level rose by several tens of meters
[Broecker and Henderson, 1998; Waelbroeck et al., 2002].
During Termination I (19,500-6,000 y) sea level rose by
120-130 m [Yolohama et al., 2000; Lambeck and Chappel,
2001; Clark and Mix, 2002]. During these short-term
events, the arrival of species to the Azores (especially
from the east Atlantic) due to range expansion processes
may have been increased and facilitated by temporary sea
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ÁVILA S. P. et al.
surface currents that no longer exist now. This possibility is
supported by Gerber et al. [1989] data, who studied several
Pleistocene outcrops from Porto Santo Island (Madeira archipelago) of similar age to that of the Prainha and Lagoinhas mollusc assemblages, and who reported Polynices
lacteus, Cantharus variegatus (GRAY, 1839) and one Conus
species, all of them having locally disappeared from Madeira archipelago. At Tenerife (Canary Islands) the Pleistocene
stratigraphic sequence of Tachero presents similarities in
both age and taxonomic composition, with those of Prainha
and Lagoinhas in the Azores [García-Talavera et al., 1978;
2006, pers. comm]. Both show a biogenic limestone bed
(40 cm thick at Tachero, formed mostly by remains of the
Melobesia calcareous algae) at the base of the sequence,
followed by a sandy layer. Of the 94 species reported by
García-Talavera et al. [1978 : 99] for Tachero (72 Gastropoda, 21 Bivalvia and one Cephalopoda), 16 also occur at
Prainha : 13 Gastropoda and 3 Bivalvia. Most of the gastropods identified have a planktotrophic larval development
(tabl. IV).
FIG. 2. – A, B: Alvania abstersa (DBUA-F 149/170-5); C Alvania abstersa (DBUA-F 149/170-4): D-F: Alvania formicarum DBUA-F 2/102-1; G: Pusillina inconspicua (DBUA-F 149/171-2); H, I: Pusillina inconspicua (DBUA-F 149/171-1); J-L: Odostomella doliolum (DBUA-F149/172-1).
FIG. 2. – A, B : Alvania abstersa (DBUA-F 149/170-5) ; C : Alvania abstersa (DBUA-F 149/170-4) : D-F : Alvania formicarum DBUA-F 2/102-1 ; G :
Pusillina inconspicua (DBUA-F 149/171-2) ; H, I : Pusillina inconspicua (DBUA-F 149/171-1) ; J-L : Odostomella doliolum (DBUA-F149/172-1).
Bull. Soc. géol. Fr., 2009, no 4
THE BIOGEOGRAPHY OF THE MARINE MOLLUSCS OF THE AZORES
Modes of larval development and dispersal ability
It is usually assumed by marine biologists that gastropods
with a planktotrophic larval development show wider geographical ranges than those with a non-planktotrophic development [Scheltema, 1971, 1977, 1986a, 1986b, 1989;
Jablonski and Lutz, 1980, 1983]. Some notorious exceptions are known – e.g.: Lasaea adansoni [GMELIN, 1791], a
brooding bivalve [Ó Foighil, 1989], and temperate intertidal
small-sized gastropods with non-planktotrophic development [Ávila, 2005, 2006; Ávila et al., 2005], that disperse
attached to drifting seaweeds – but, in average conditions,
the rule holds for most of marine molluscs. Thus, in oceanic
islands geographically located far away from source populations, we would expect to find a high proportion of species with a planktotrophic larval development (p), relative
to the number of non-planktotrophic ones (np), and that is
precisely what happens with the Recent molluscs of the
Azores. From a total of 146 Prosobranchs presently reported to these islands, 62 (42.5%) are planktotrophic species,
54 (37.0%) are non-planktotrophic species and it was not
possible yet to determine the mode of larval development
for the remaining 30 species (20.5%) (Ávila, unpub. data).
Omitting the endemic stock (27 np-species and 2 p-species)
and the 30 species with undetermined mode of development, the proportions are 69.0% of planktotrophic species
and 31.0% of non-planktotrophic species.
However, that is not the case with the species that locally disappeared from Santa Maria, as a consequence of the
last glaciation (tabl. V). We must stress that these thermophilic species could not occur in the Azores during MIS6
(that is, before the beginning of Termination II), therefore
they must have arrived to the Azores during or shortly before MIS5e. As none of the different modes of development
(p or np) is apparently favoured (53.8% of p-species versus
46.2% of np-species), in contrast with the figures for the
Recent malacofauna, where an excess of p-developers occurs (69.0%), relative to np-developers (31.0%), this seems
to support the idea of a short-temporal window assisting the
TABL. IV. – Mode of larval development (p – planktotrophic; np –
non-planktotrophic) of the Pleistocene gastropod species collected at Tachero (Tenerife, Canary Islands) by García-Talavera et al. [1978] and also
reported to the Pleistocene of Santa Maria Island (Azores) by Ávila et al.
[2002].
TABL. IV. – Mode de développement des larves (p – planctotrophique ; np –
non planctotrophique) des espèces de gastéropodes pléistocènes collectés
à Tachero (Tenerife, Îles Canaries) par García-Talavera et al. [1978] et
également retrouvées sur l’Île de Santa Maria (Azores) par Ávila et al.
[2002].
301
TABLE V. – Mode of larval development (p – planktotrophic; np –
non-planktotrophic; ? – probable mode of larval development) of the Pleistocene gastropod species reported to Santa Maria Island (Azores) that locally disappeared during the last glaciation.
TABL. V. – Mode de développement des larves (p – planctotrophique ; np –
non planctotrophique; ? – mode développement probable des larves) des
espèces pléistocènes de gastéropodes pléistocènes signalées dans l’Île de
Santa Maria (Azores) et qui disparaissent localement durant la dernière
glaciation.
arrival of both p and np-developers to the Azores. During
this time frame, short-lived oceanic currents (different from
the ones that exist in the present times) must have been established, especially during or shortly after glacial Terminations, promoting the dispersal of species to the Azores. If
the direction of these currents was similar to the present
ones, we would expect exactly the reverse: i.e. short time
dramatically favouring the more active p-colonisers, and
longer time-windows allowing progressively also the less
efficient np- np-developers. Thus, the expected likelihoods
will dramatically change, if the currents are in the direction
of the Azores. In this case, the proportion “np/p” will increase, and that is precisely what we see in the fossil record
of Santa Maria.
TABLE VI. – Approximate surface area (km2) of the islands of the Azores,
Madeira and Canary Islands (18,000 y) and in the present. * The former island of Mahan is equivalent nowadays to the islands of Fuerteventura and
Lanzarote, and the islets of La Graciosa and Los Lobos [García-Talavera,
1999; Ávila, 2005].
TABL. VI. – Surface approximative (km2) des îles des Azores, de Madère et
des Canaries il y a 18,000 ans et actuellement. * L’ancienne île de Mahan
est l’équivalent actuel des îles de Fuerteventura et de Lanzarote et des
îlots de La Graciosa et Los Lobos [García-Talavera, 1999 ; Ávila, 2005].
Bull. Soc. géol. Fr., 2009, no 4
302
ÁVILA S. P. et al.
FIG. 3. – A : Littorina saxatilis (DBUA-F 149/170-3); B, C: Nassarius incrassatus (DBUA-F 149/170-2); D: Bulla mabillei (DBUA-F 148); E, F: Odostomia cf. kuiperi (DBUA-F 149/171-4); G-J: Philippia hybrida (DBUA-F 137/156-1).
FIG. 3. – A : Littorina saxatilis (DBUA-F 149/170-3) ; B, C : Nassarius incrassatus (DBUA-F 149/170-2) ; D : Bulla mabillei (DBUA-F 148) ; E, F :
Odostomia cf. kuiperi (DBUA-F 149/171-4) ; G-J : Philippia hybrida (DBUA-F 137/156-1).
Ávila et al. [2002; 2008b] have shown that, besides the
thermophilic species, only those species of littoral endobenthic bivalves usually associated to fine sandy substrata, such
as Ensis minor (CHENU, 1843) and Lucinella divaricata
(LINNAEUS, 1758), did locally disappear from Santa Maria
Island during the last glaciation. The endemic Azorean species (where the minute Rissoidae account for almost half)
were not affected by the drop of SSTs and the associated
sea level fall [Ávila, 2005].
Bull. Soc. géol. Fr., 2009, no 4
At the peak of the last glaciation, sea level was about
120-130 m lower than at present [Lambeck and Chappel,
2001]. As a consequence, the area of the islands of the Macaronesian archipelagos was larger than today (tabl. VI) and
a number of seamounts nowadays located between the
southwest of Iberia and Madeira were true islands (fig. 6).
The distance between each of these palaeoislands located
between Madeira and Iberia would be of only 200-300 km.
Therefore, these islands may have played an important role
THE BIOGEOGRAPHY OF THE MARINE MOLLUSCS OF THE AZORES
303
FIG. 4. – A: Sinezona cingulata (DBUA-F 139/126-2); B: Pinna rudis DBUA-F 147 (96 x 66 mm); C, D: Odostomia duureni (DBUA-F 137/151-3);
E: Striarca lactea (teratological specimen) (DBUA-F 137/160-1); F: Conus cf miruchae DBUA-F 89); G: Trachypollia nodulosa (DBUA-F 3/115-1);
F: Odostomia (DBUA-F 139/126-5); H, I: Auriculinella bidentata (DBUA-F 149/171-3); J: Pedipes pedipes (DBUA-F2/114-1).
FIG. 4. – A : Sinezona cingulata (DBUA-F 139/126-2) ; B : Pinna rudis DBUA-F 147 (96 x 66 mm) ; C, D : Odostomia duureni (DBUA-F 137/151-3) ;
E : Striarca lactea (spécimen) (DBUA-F 137/160-1) ; F : Conus cf miruchae (DBUA-F 89) ; G : Trachypollia nodulosa (DBUA-F 3/115-1) ; F : Odostomia (DBUA-F 139/126-5) ; H, I : Auriculinella bidentata (DBUA-F 149/171-3) ; J : Pedipes pedipes (DBUA-F2/114-1).
in the processes of dispersion, especially of the intertidal
and shallow water molluscs. Thus an increase in the number
of successful migrants of littoral species from Iberian shores towards Madeira during glacial periods is expectable, taking advantage on the smaller distances and favourable
currents and winds. By contrast, the fossil record of Santa
Maria shows that during interglacial periods, warm-water
species from Caribbean and African shores did reach the
Azores, e.g. several species of Conus [Ávila et al., 2002;
Ávila, 2005].
It seems to us that the predominant routes will be different during glacial and interglacial periods. The similarities
Bull. Soc. géol. Fr., 2009, no 4
304
ÁVILA S. P. et al.
FIG. 5. – Cumulative number of species correctly reported to the Pleistocene outcrops of Prainha and Lagoinhas (Santa Maria Island, Azores).
FIG. 5. – Nombre cumulé d’espèces avec enregistrements validés dans les affleurements pléistocènes de Prainha et Lagoinhas (Île Santa Maria, Azores).
found in the fossil record of Santa Maria (Azores) and Porto
Santo (Madeira) (interglacial period, both with a MIS5e attributed age) seems to point to a colonization of the Azores
via Madeira. However, this is not consistent with recent
DNA investigations, which indicate a younger connection
between Azores and Portugal and an ancient connection
between the Azores and Madeira [Gonçalves et al., 2000; Ó
Foighil et al., 2001].
CONCLUSIONS
Prior to the final closure of the Isthmus of Panama and the
development of the Gulf Stream, the main sea surface currents in the Atlantic Ocean had an east-west predominant
direction; therefore, it is expectable that, before the onset of
FIG. 6. – Oceanic islands 18,000 y [adapted from García-Talavera, 1999].
FIG. 6. – Iles océaniques il y a 18 000 ans [adapté de García-Talavera,
1999].
Bull. Soc. géol. Fr., 2009, no 4
the Pleistocene glaciations, European species more easily
reached the Azores region than they do today. The eastern
Atlantic biogeographical relationships of the Azorean fauna
that we see nowadays are precisely the remnants of that ancient signal. Only after the installation of the Gulf Stream
and its associated system of currents, was possible the arrival to the Azores of species from the Caribbean. This is the
reason why, from more than 130 species of molluscs reported to the late Miocene of the Azores, only a few species are
also reported from the Caribbean; all others are reported
from Miocene outcrops of Europe and western Africa (Ávila et al., unpubl. data), whereas in the Pleistocene and in the
Recent, the percentage of Azorean species of molluscs that
are reported from the Caribbean is much higher (11 and
13%, respectively) (tabl. II).
At the peak of the last glaciation, the area of the islands
of the Macaronesian archipelagos was larger than today and
a number of seamounts nowadays located between the
southwest of Iberia and Madeira were true islands, probably
playing an important role in the processes of dispersion, especially of the intertidal and shallow water molluscs. An increase in the number of successful migrants of littoral
species from Iberian shores towards Madeira during glacial
periods is expected, taking advantage on the smaller distances and favourable currents and winds. During Pleistocene
glacial-interglacial cycles, short-duration events have occurred during which, short-lived oceanic currents must have
been established, especially during or shortly after glacial
terminations. During these short-term events, the arrival of
species to the Azores due to range expansion processes may
have been increased and facilitated by temporary sea surface currents that no longer exist today. With favourable
sea-surface currents and winds, both planktotrophic and
non-planktotrophic species (these via rafts) successfully arrived to the Azores and the fossil record of Santa Maria
Island testifies this.
Acknowledgements. – The authors thank Mr. Pombo (Vila do Porto) for
useful information about the fossils and outcrops of Santa Maria Island.
Thanks are also due to Emilio Rolán, Serge Gofas, Marien Faber, Jeroen
THE BIOGEOGRAPHY OF THE MARINE MOLLUSCS OF THE AZORES
Goud, Jacobus van Aartsen, Anselmo Peñas, Constantine Mifsud, Marco
Oliverio, Henk Dijkstra, Giancarlo Paganelli and António Monteiro for
helping on the identification of some species.
The Clube Naval de Santa Maria is acknowledged for providing sea
transportation to survey the shorelines of Santa Maria Island. We would
like to thank the organization of the “Workshop Fósseis de Santa Maria”,
that was held at Vila do Porto (21 to 27 of June 2002) and all the students
that helped in the collecting during this period, as well as Direcção Regional da Ciência e Tecnologia (Açores), Direcção Regional do Ambiente
(Açores), Direcção Regional da Juventude (Açores) and Câmara Municipal
de Vila do Porto, for financial support.
305
The first author also thanks Miguel Matias for helping in the collecting of samples in February 2003 at Lagoinhas.
Jorge Medeiros (CIRN/Universidade dos Açores) is acknowledged for
the SEM photos. We also thank António Moniz (Secção de Geografia,
Universidade dos Açores) for the maps of the Azores and Santa Maria Island.
S.P. Ávila was supported by grant SFRH/BPD/22913/2005 (FCT –
Fundação para a Ciência e Tecnologia) of the Portuguese government. Research at IMAR-DOP/UAc (UI&D #531 and ISR LA#9) is funded by
FCT/MCTES– Lisbon and DRCT/Azores through pluri-annual and programmatic funding schemes (part FEDER).
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