On the stratigraphical and palaeobiogeographical significance of Borelis melo melo (Fichtel & Moll, 1798) and B. melo curdica (Reichel, 1937) (Foraminifera, Miliolida, Alveolinidae)

The stratigraphical and palaeobiogeographical significance of Borelis melo melo (Fichtel & Moll, 1798) and B. melo curdica (Reichel, 1937) is re-assessed in the light of a taxonomic review. Borelis melo melo ranges at least throughout the Miocene, whereas B. melo curdica is restricted to the late Early to Middle Miocene. Both sub-species occur only in the Indo-Pacific Province in the late Early Miocene (‘early’ Burdigalian), but in both the Indo-Pacific and Mediterranean provinces in the latest Early–early Middle Miocene (‘middle’ Burdigalian–Langhian), implying a marine (re-)connection between the two regions at this time.


INTRODUCTION
The genus Borelis is a stratigraphically important constituent of the larger benthic foraminiferal (LBF) faunas of the Eocene-Holocene (see, for instance, Adams, 1970). It is represented in all of the low-latitude shallow-water palaeobiogeographical provinces of the period, namely the Mediterranean, Indo-Pacific and Caribbean provinces (Adams, 1967;Jones, 1999, and additional references cited therein), which latter two, incidentally, were contiguous prior to the formation of the Isthmus of Panama in the Pliocene. Modern LBF species live in areas with minimum sea-surface temperatures greater than 18(C, and are essentially restricted to the tropics (Langer & Hottinger, 2000). They also host photosynthetic algal symbionts, and are restricted to the photic zone. A detailed ecological study in the Gulf of Aqaba revealed that Borelis hosts B-3 diatom symbionts and is restricted to depths of 5-65 m (Reiss & Hottinger, 1984).
At least sixteen nominal species and sub-species were considered by Samanta et al. (1990) or are considered by the present authors to be attributable to Borelis (note that, following Samanta et al. (1990) and other authors cited therein, a number of additional nominal species from the Upper Cretaceous and Lower Tertiary of the Caribbean Province have been excluded).
Unfortunately, the precise nature of the type species, Nautilus melo Fichtel & Moll, 1798, which was first described and illustrated, inadequately by modern standards, as long ago as the late eighteenth century, remained poorly known until comparatively recently, with the result that many nominal species described in the interim are candidate junior synonyms.
The purpose of this paper is to review the taxonomy of the sub-species Borelis melo melo and B. melo curdica, and, in the light of this review, to re-assess their stratigraphical and palaeobiogeographical significance.

SYSTEMATIC MICROPALAEONTOLOGY
Order Miliolida Calkins, 1909Family Alveolinidae Ehrenberg, 1839 Diagnosis. Wall porcellaneous, imperforate. Test free, typically large (macroscopically visible), spherical to ellipsoidal depending upon degree of elongation along axis of coiling. Proloculus followed by spiral tube or flexostyle; later chambers initially irregularly coiled, at least in microspheric generation, later becoming planispiral. Chambers numerous, may be divided into one or more rows of chamberlets by means of secondary partitions or septula paralleling direction of coiling; those of upper (attic) row(s) smaller than those of lower row; septula of adjacent chambers either continuous or alternating. Basal layer thickening ('flosculinization') may be developed. External apertures generally arranged in one or more rows; apertural teeth present or absent. Synonym. Neoalveolina Silvestri, 1928[Alveolina bradyi Silvestri, 1927=Nautilus melo Fichtel & Moll, 1798subsequent designation (Bakx, 1932)].
Diagnosis. Chamberlets generally arranged in single row, but incipient attic chamberlets separated by Y-shaped septula developed in some forms; septula of adjacent chambers continuous. External apertures generally arranged in single row, but a second row of intercalar apertures developed in one form. Basal layer thickening ('flosculinization') not developed.

Wadi Hauran
Authors' observations on material in the IPC collection in the NHM, Slide PF54342).
[No more refined stratigraphic interpretation possible].

Red Sea Coast, Saudi Arabia
Al Bad Formation Midyan area, Red Sea coast, NW Saudi Arabia (Dullo et al., 1983).

Gulf Coast, Qatar
Dam Formation Al-Saad & Ibrahim (2002) -questionable in view of poor quality of photograph.
[Probably early Middle Miocene, Langhian. Overlies zonule of Miogypsina cushmani, restricted to Early Miocene, Burdigalian (planktonic foraminiferal N7) in Western Tethys (Cahuzac, 1984;Cahuzac & Poignant, 1997)]. 'Middle Miocene' El Abyar, Libya (Sartorio & Venturini, 1988 Remarks. The following nominal species differ from Borelis melo melo essentially only in their marginally greater axial elongation, and are regarded as at least possibly synonymous (as they appear to fall within the range of variation exhibited by Borelis melo melo): + Alveolina pulchra d'Orbigny, 1839, originally described from the Recent of Cuba in the Caribbean, and also recorded in the Recent elsewhere in the equatorial Atlantic and in the Indo-Pacific, and in the Pleistocene and Miocene. Adams (1970) noted that pulchra 'may grade into B. melo'. + Alveolina melo sensu Brady, 1884 (see also Jones, 1994) from the Recent of Ascension Island and Bermuda in the Atlantic. Alveolina bradyi Silvestri, 1927 was evidently intended by Silvestri (1927Silvestri ( , 1928) as a new name for A. melo sensu Brady, 1884, which he interpreted as distinct from melo sensu stricto.
However, Silvestri's species concept, as indicated by his synonymy and his plates, includes some specimens of undoubted melo s.s., including some from the type locality, with the result that most subsequent authorities have synonymixed bradyi with melo. + Borelis primitivus Cole, 1957, originally described from the Tertiary e (?Te 1 -4 , Late Oligocene) of Eniwetok Atoll in the West Pacific.
The following nominal species differ in their significantly greater axial elongation, and are regarded as probably distinct: + Neoalveolina pygmaea schlumbergeri Reichel, 1937, originally described from the Recent of Mayotte, NW of Madagascar in Table 3. Stratigraphical distribution of Borelis melo curdica in the Indo-Pacific Province.
[No more refined stratigraphic interpretation possible].

Stratigraphical and evolutionary significance
These distribution data can be interpreted as indicating that Borelis melo melo evolved into B. melo curdica, with its 'more advanced' (certainly, more complex) structure of incipient attic chamberlets, Y-shaped septula and staggered row of external apertures, in the late Early Miocene, in the Indo-Pacific Province (Fig. 1).
Borelis melo curdica could conceivably have then evolved into Flosculinella bontangensis, with true attic chamberlets, in the Middle Miocene, in the Indo-Pacific Province. Importantly, Flosculinella bontangensis has been described (although unfortunately not illustrated) from the Middle Miocene of Fars Province in southeastern Iran, immediately post-dating Borelis melo curdica (James & Wynd, 1965).
Interestingly, Flosculinella bontangensis has been independently interpreted as having then in turn evolved into Alveolinella praequoyi, with an additional row of attic chamberlets, also in the Middle Miocene, in the Indo-Pacific Province (Wonders & Adams, 1991).

Palaeobiogeographical significance
The interpreted absences of Borelis melo curdica from the Indo-Pacific, and of Flosculinella from the Mediterranean, in the late Early Miocene, Burdigalian, were among the observations that led the late C. G. ('Geoff') Adams and his co-workers to suggest that the former Tethyan Sea connection between the two provinces had become interrupted by this time, by the formation of a land bridge between the converging Arabian and Eurasian Plates (Adams et al., 1983(Adams et al., , 1999. Indeed, there is a wealth of terrestrial vertebrate evidence to indicate that there was a land bridge between Arabia and Eurasia in the late Early Miocene (Orleanian Land Mammal Age), which facilitated the dispersal not only of the primitive elephant Gomphotherium -after which it is colloquially known -but also of other less well-documented groups, such as fresh-water fish (see, for instance, Otero & Gayet, 2001). Corroborative evidence is provided by the existence of an emergence surface over much of Arabia (Adams, 1969). It is likely that the emergence surface and land bridge was generated by uplift of the Western Arabian Highlands by thermal doming associated with rifting in the Red Sea (Jones & Racey, 1994). Fred Rögl and Fritz Steininger and their co-workers speculated, but were unable to prove to Adams' satisfaction, that there might have been a later reconnection between the Indo-Pacific and Mediterranean provinces, possibly in the early Middle Miocene, Langhian, prior to the final disconnection in the late Middle Miocene, Serravallian (see, for instance, Rögl, 1998Rögl, , 1999a; see also Jones, 1999). Perhaps, significantly, this putative reconnection would have been coincident with a global climatic optimum and associated glacio-eustatic sea-level highstand.
The evidence outlined above of the occurrence of both Borelis melo curdica and B. melo melo only in the Indo-Pacific Province (at least in the Middle East) in the late Early Miocene, 'early' Burdigalian, supports Adams' interpretation of an interruption of the earlier marine connection between the Indo-Pacific and Mediterranean provinces at this time (Fig. 2a).
It is further submitted, however, that the occurrence of both sub-species, not only in the Indo-Pacific Province (in the Middle East) but also throughout the Mediterranean in the latest Early-early Middle Miocene, 'middle' Burdigalian-Langhian, supports Rögl & Steininger's interpretation of a (re-)connection, or at least a partial connection or filter, between the Indo-Pacific and Mediterranean provinces at this time (Fig. 2b).

CONCLUSIONS
1. Borelis melo melo and B. melo curdica are distinguishable from one another essentially on the basis of the level of development of their internal chamberlets and external apertures. 2. Borelis melo melo ranges at least throughout the Miocene. B. melo curdica is restricted to the late Early to Middle Miocene. 3. Both sub-species occur only in the Indo-Pacific Province in the late Early Miocene, 'early' Burdigalian, but in the Indo-Pacific and Mediterranean provinces in the latest Early-early Middle Miocene, 'middle' Burdigalian-Langhian. Their occurrence in both the Indo-Pacific and Mediterranean provinces in the latest Early-early Middle Miocene points to a marine (re-) connection between the two provinces at this time.