A marine bird (sulidae, Aves) from the Langhian (middle Miocene) of Penedo beach (Setúbal Peninsula—SW Portugal) and its paleoenvironmental context

The fossil remains of birds from the Miocene of Portugal are scarce, encompassing a total of twelve specimens, from nine paleontological outcrops located in Leiria (central Portugal), southern sector of Setúbal Peninsula and along the lower Tagus Basin. This study focuses on a new specimen found in the Praia do Penedo Norte (Sesimbra) coastal cliff corresponding to a coracoid bone, attributed to Morus sp., a sulid bird, biostratigraphically framed by calcareous nannofossils within the middle Miocene (Langhian).


Introduction
There are three extant species of the genus Morus: Morus bassanus, Morus capensis and Morus serrator. Morus species are large seabirds that live on coastal areas and normally breed in large colonies, along offshore islands or in mainland coastal cliffs. After the breeding season, these birds disperse over a wide area (Ospina-Alvarez, 2008;Svensson et al., 2009;Veron & Lawlor, 2009). Nowadays, Morus bassanus lives in both sides of the North Atlantic, the range of the Morus capensis extends from the coastal waters off the Gulf of Guinea on the west coast of Africa, to Mozambique, on the east coast. Morus serrator lives in Western Australia, and in the North and South Islands of New Zealand (Medway, 1993;Ospina-Alvarez, 2008;Stephenson, 2007;Veron & Lawlor, 2009).
In all world there are eleven species of Morus described in the fossil record of America and Europe. This work reports another presence of Morus in Europe and constitutes the first to be reported in the Miocene of Iberian Peninsula. The European Cenozoic deposits have yielded a considerable number of avian remains, including those of seabirds (Mlíkovský, Mayr, 2005;Tyrberg, 1998Tyrberg, , 1999Warheit, 2002). Seabirds are an ecologically important group of birds characterized by their dependence to the marine environment (Harrison, 1985;Schreiber & Burger, 2002;Gaston, 2004), whose fossil record in Europe, although scarce, ranges from the late Paleocene to the Recent (Mlíkovský, 2009). The oldest sulid record in Europe is from the Messel Pit WHS (Germany), in a middle Eocene lacustrine formation, where was described the species Masillastega rectirostris (Mayr, 2002;Mlikovsky, 2007). From the Miocene there are five sulid species (including the genus Morus) described in Europe, France, Austria and Romania. Unfortunately, European Miocene sulids lack a modern taxonomic revision, which prevents a closer evaluation of this record (Mlikovsky, 2009). Eleven species within the genus Morus have been described: eight in North America; one, in South America and two, in Europe (France and Romania) (Stucchi et al., 2016).
In the present study, we describe a proximal fragment of a coracoid of a sulid bird from the middle Miocene of Portugal (Figs. 1), discovered by one of the authors (CNC), in 1996, at the basal beds of the cliff of the Praia do Penedo Norte (Sesimbra, Setúbal Peninsula).

Geological setting
The Praia do Penedo Norte coastal cliffs are mainly cut in Miocene fine silty-clay sandstones with basal units more cemented as very fossiliferous biocalcarenites. These units belong to the southern sector (Setúbal Peninsula) of the Mio-Pliocene Lower Tagus basin and are part of the northern limb of the fold-fault of the Betic-oriented Arrábida mountain chain, that develops further south (Fig. 1). The Praia do Penedo Norte lowermost units are particularly enriched in the greenish phyllosilicate glauconite which indicates sediment starvation conditions associated to the main transgressive sequence of the beginning of the middle Miocene marine cycle of the Neogene of Portugal (Cachão & Silva, 2000).
The lithostratigraphy of Praia do Penedo Norte is constituted composed mainly by dark silty-clay fine sandstones, yellowish micaceous fine sandstones, locally known as "areolas", and cemented biocalcarenites. The coracoid was found on bed C 11 (Fig. 2), on a condensed section constituted by glauconite-rich biocalcarenites, with abundant body fossils of both marine vertebrates and invertebrates, nowadays subjected to intense anthropic erosion due to ongoing activity of private collectors of Miocene shark teeth.

Materials and methods
This study is based on a coracoid collected at Praia do Penedo Norte (Sesimbra) and curated in the paleontology collection of CPGP (numbered CPGP.13.96.2). In the laboratory (LAP), the bone fragment was photographed and measured followed by biometric, taxonomic and taphonomic studies, through a comparison, analysis of the main characteristics of the studied fossil with two coracoids (LAP.2016.3 and LAP.2017.1) from the extant northern gannet Morus bassanus and stored in the anatomical comparison collection of CPGP. The osteological nomenclature used follows Baumel and Witmer, 1993. The measurements were made in millimetres. To determine the bird fossil's age 6 samples were equally spaced and sequentially collected from the base to the uppermost layers of the stratigraphic sequence of Praia do Penedo Norte. For each sample a smear slide was prepared following procedures specific for siliciclastic-rich sediments (see Johnson et al., 2012). One to two 30 mm columns of the smear slide were screened with a petrographic microscope (with cross polars or nicols) at × 1250 magnification, to characterize the assemblage of calcareous nannofossils and register the presence of index fossils. Taxonomic identifications follow Nannotax (www. mikro tax. org/ Nanno tax3) diagnostical guidelines.

Paleoecology
The Praia do Penedo Norte succession is cropping out in the Miocene cliffs, with a set of a diversified assemblage of fossils, both of invertebrates and marine vertebrates, where marine facies are present (Manuppella et al., 1999). Water column may had been significant depth due to the quantity of nektonic vertebrate groups represented ranging from a wide variety of sharks and fishes to cetaceans. However, the coast should not be very far due to the presence of dark glauconiterich internal molds of early Miocene bivalves reworked and included in some of the basal units of the sequence. Samples collected for micropaleontology revealed concentrations of calcareous nannofossils (less than 10 per field of view along the rippled smear slides) compatible with a neritic marine paleoenvironment, over middle continental shelf. The lowermost sample from the section has the highest abundancies and diversity of calcareous nannofossils (see Supplementary data), compatible with the deepest paleobathymetry of the entire section. Abundance and diversity diminish gradually towards the top of the section in response to the regressive

Biostratigraphy of calcareous nannofossils
Despite the scarcity on oceanic index species such as Discoaster spp. due to paleoenvironmental reasons, the lowermost sample from the section (Penedo I) contained common Helicosphaera ampliaperta associated to rare H. magnifica. These helicoliths co-occurence restrain this assemblage the calcareous nannofossil biozone NN3 (Martini, 1971), more or less equivalent to the middle Burdigalian (see Fig. 3).
Penedo II sample discloses the occurrence of (very rare) Sphenolithus heteromorphus which, in association with the still present and common H. ampliaperta (commom), indicates a younger age, compatible with biozone NN4 (Martini, 1971), equivalent to the late Burdigalian to early Langhian (see Fig. 3).
Penedo III already contains the small helicolith Helicosphaera walbersdorfensis while has no trace of H. ampliaperta and no S. heteromorphus. This, together with the presence of small to medium size reticulofenestrids (i.e., still without large Reticulofenestra pseudoumbilicus) indicates an age roughly compatible with biozone NN5 (Martini, 1971) (see Fig. 3).

Systematic palaeontology
Locality and horizon Praia do Penedo Norte Bed C11 from the depositional sequence, Langhian in age based on the calcareous nannofossil biozonation (see above).
Measurements: the fossil has a maximum length of 41.5 and a maximum width of 18.1 mm. Five osteological measures (see Fig. 5) were defined in order to compare with the bones of the extant remains of Morus bassanus (Table 1).
Description and comparisons: CPGP.13.96.2 (Fig. 3) has a pointed border of the cotyla scapularis. The sacapularis cotyla has a sub oval shape, with a pointed distal end, the process acrocoracoid is narrow and the lamina elliptica articularis has a drop shape. It has four pneumatic foramina in the triosseal canal. The process acrocoracoideus is not complete (Fig. 6), because this area is broken, probably caused by necrophagy (Fig. 7).

Discussion and conclusion
The broken part (see Fig. 6) of the processus acrocoracoideus do not seem to be the result of erosion resulting from postmortem transport, as this is one of the most resistant bone zones for erosion. The fact that it presents the same characteristics of similar traces in recent bones, resulting from gnawing, we think that this breakage was the result of the action of necrophagous animals. This necrophagy action may also have disassembled the skeleton.
The presence of seabirds in the Miocene of Praia do Penedo Norte is consistent with the fossil record of this paleontological site, where remains of marine vertebrates abound. The marine paleoenvironments over the continental shelf, as the calcareous nannofossils found in the sequence Praia do Penedo Norte indicate, are also in agreement with the environments frequented by birds of the genus Morus. The biostratigraphic calcareous nannofossil framework dates this specimen as Langhian (middle Miocene, .

3
The fossil coracoid now studied presents the main characteristics observed in coracoids of the genus Morus, as observed in the comparative study: pointed border of the cotyla scapularis, oval shape of the sacapularis cotyla, the narrow process acrocoracoid and the drop shaped facies articularis clavicularis.