Connectivity and climate control fish distribution today
as well as in the geological past. We present here the Aquitanian (early
Miocene) marine fish of the Mesohellenic Basin, a restricted basin at the
border between the proto-Mediterranean and Paratethyan seas. Based on fish
otoliths, we were able to identify 19 species from 17 genera, including two
new species:
Connectivity between marine realms largely controls the fate of fish populations and biodiversity (Worm and Tittensor, 2018). Early Miocene proto-Mediterranean biodiversity is particularly interesting because, at that time, the basin's connection with the Indo-Pacific realm ceased to exist (Rögl, 1998; Bialik et al., 2019; Torfstein and Steinberg, 2020; Sun et al., 2021), while the marine biodiversity hotspot was shifting toward the southeast (Renema et al., 2008) and the climate was cooling (Cornacchia et al., 2018), marking the onset of a subtropical gradually oligotrophic regime in the proto-Mediterranean Sea. However, the early Miocene fossil fish record from the Mediterranean area is particularly sparse. Moreover, very few studies have focused on the fish otolith record (Steurbaut, 1979, 1982, 1984; Reichenbacher and Cappetta, 1999; Reichenbacher, 2004; Hoedemakers and Batllori, 2005), despite its importance for revealing the evolution of fish faunas and fish biogeography (Agiadi et al., 2011, 2017, 2018). At the crossroads between the proto-Mediterranean Sea, the Atlantic Ocean, the North Sea, the Paratethys, and the Indo-Pacific realm, the Mesohellenic Basin (MHB) during the early Miocene, a molassic basin at the northern part of the proto-Mediterranean, directly at the intersection with the Paratethys epicontinental sea, offers a unique opportunity to explore the effects of interbasinal connectivity on fish faunas.
In this study, we identify the fossil fish otoliths found in the Aquitanian
(lower Miocene) sediments of the Felli section (Grevena Prefecture, NW Greece)
that were deposited in the MHB. The reconstructed assemblage is the first
record of fishes from the eastern part of the Aquitanian (
The study area is located in Grevena Prefecture, NW Greece, where the molassic sedimentary sequence of the MHB is exposed (Fig. 1; Zelilidis et al., 2002; Ferrière et al., 2004). The MHB was a synorogenic molasse-type basin (Kilias et al., 2015), a separate paleogeographic area from the late Eocene until the middle Miocene, between the internal and external Hellenides, ENE and WSW, respectively. It was a narrow, 300 km long trench, filled with up to 4.5 km of sediments, which have been separated into the Krania, Eptachori, Pentalofos, Tsotyli, and Ondria formations (Brunn, 1956; Wielandt-Schuster et al., 2004; Ferrière et al., 2013; Kilias et al., 2015), deposited parallel to each other (except for the Krania Formation) along the eastern margin of the trough (Kilias et al., 2015). The studied sediments belong to the Pentalofos Formation, consisting in general of upper Chattian–lower Miocene sandstones to silty marlstones (Mavridis et al., 1985; Ferrière et al., 2004; Wielandt-Schuster et al., 2004; Kilias et al., 2015). The Felli section, which is our study section, includes only the uppermost part of the Pentalofos Formation corresponding to the Aquitanian according to Mavridis et al. (1985). The Pentalofos Formation overlies the Eptachori Formation and is overlain, conformably in the Grevena area, by the Tsotyli Formation (Fermeli and Ioakim, 1992).
We sampled a small section by the Aliakmon River banks, located east of
Felli village, SE of Grevena City (40
We adopted specific descriptive characters for the otoliths of Congridae
(Schwarzhans, 2019) and Pleuronectiformes (Schwarzhans, 1999). We followed
the fish classification scheme of Nelson et al. (2016). We made the
following measurements on the identified otoliths (reported in mm; Fig. 2):
OL, otolith length; OH, otolith height; AL, antirostrum length; RL, rostrum
length; CL, colliculum length; OCL, ostial colliculum length; CCL, caudal
colliculum length; OSL, ostium length; CaL, caudal length. In addition, in
Congridae, it proved significant to measure the sulcus angle (
Schematic diagram of the measurements obtained on the otoliths.
OL, otolith length; OH, otolith height; AL, antirostrum length; RL, rostrum
length; CL, colliculum length; OCL, ostial colliculum length; CCL, caudal
colliculum length; OSL, ostium length; CaL, caudal length,
In this section, we describe and explain the species identification of the fossil otoliths from the Felli section. The measurements for all identified otoliths are available in the Supplement. The studied material has been deposited at the Athens Museum of Palaeontology and Geology – Vertebrates Collection (AMPG(V)).
Infraclass Teleostei Müller, 1845 sensu Arratia, 1999 Order Anguilliformes Berg, 1943 Family Congridae Kaup, 1856 Genus urn:lsid:zoobank.org:act:4B603ED2-93BE-429E-B4EC-8D5F45A9C24C
registered on 21/7/2021 Fig. 3A–D 2004
Photographs of the identified otoliths from the Felli section.
Figure 3A, AMPG(V) 2361, Aquitanian, Felli section, level 11,
Grevena Prefecture, Greece; OL, 3.40; OH, 2.80; CL, 2.49 mm;
Two specimens, AMPG(V) 2362–3, same data as holotype; one specimen, AMPG(V) 2364, Aquitanian, Felli section, level 12, Grevena Prefecture, Greece.
After the MHB, where the type section sediments were deposited.
Elongated otoliths with OL/OH of 1.16–1.26. The sulcus extends
almost to the distal edge, with CL/OL of 0.58–0.74, and
Elongated, thick spindle-shaped otoliths with an elongated central sulcus that opens toward the dorsal rim through an intricate ostial channel. The ostial channel is placed almost at the proximal edge of the sulcus and is perpendicular to it. The dorsal depression is well expressed. The dorsal rim is curved in the distal part.
Aquitanian of the western proto-Mediterranean and the MHB.
These otoliths have a more elongated sulcus than
Genus urn:lsid:zoobank.org:act:EF4B2DCC-4246-45AB-840E-1BC29C675410
registered on 21/7/2021 Fig. 3G–J
Figure 3G, AMPG(V) 2365, Aquitanian, Felli section, level 11,
Grevena Prefecture, Greece; OL, 2.62; OH, 1.44; CL, 1.170;
Nine specimens, AMPG(V) 2366–74, same data as holotype.
Due to the distinct elongated shape of its otoliths.
Elongated otoliths with OL/OH of 1.60–2.06. The angle of the
sulcus relative to the otolith length plane is 10–20
These otoliths are elongated with a long sulcus that forms an angle to the otolith length direction, which opens posterodorsally through a wavy ostial channel. The posterior edge is slightly protruding dorsally. The ventral rim forms an angle.
Aquitanian of the proto-Mediterranean Basin.
The otoliths of
Fig. 3K–L 1979 “genus aff. 1984 2004
Fifteen specimens from level 11 and three specimens from level 12.
Aquitanian of the Aquitaine Basin (SW France; Steurbaut, 1979, 1984) and the MHB, and Burdigalian of northern Italy (Nolf and Brzobohaty, 2004).
The orientation of the sulcus relative to the posterior–anterior
axis is angular, with an 11–24
Order Stomiiformes Regan, 1909 Family Phosichthyidae Weitzman, 1974 Genus
Two otoliths from level 11 and one otolith from level 12.
These otoliths resemble
Order Myctophiformes Regan, 1911 Family Myctophidae Gill, 1893 Genus
Five otoliths from level 11.
The state of preservation of these otoliths does not permit their identification to species level.
Genus Fig. 4A
Photographs of the identified otoliths from the Felli section.
One otolith from level 11.
Compared to
Order Beryciformes Regan, 1909 Family Holocentridae Richardson, 1846 Genus Fig. 4B–C 1979 1984
One otolith from level 11 and one otolith from level 12.
Aquitanian–Burdigalian of SW France (Steurbaut, 1979, 1984) and Aquitanian of the MHB.
Order Ophidiiformes Berg, 1937 Family Carapidae Poey, 1867 Genus Fig. 4D 1979 1984 2004
One otolith from level 11.
Lower Miocene of Belgium (Huyghebaert and Nolf, 1979), SW France (Steurbaut, 1984), northern Italy (Nolf and Brzobohaty, 2004), and the MHB.
The sulcus reaches both the proximal and almost the distal tip,
similar to
Order Batrachoidiformes Family Batrachoididae “Batrachoidida” Fig. 4F 1984 “genus Apogoninarum” 2013 “Batrachoidida”
Two otoliths from level 11.
Aquitanian of SW France (Steurbaut, 1984) and the MHB.
These otoliths are elongate with a higher anterior than posterior part and a prominent anterodorsal high. The sulcus is divided into a large, oval ostium that almost reaches the anterior rim, and a smaller, also oval-shaped cauda that is situated slightly dorsally. The specimens examined here resemble very much those figured by Steurbaut (1984) from the Oligocene–lower Miocene of France and reassigned by Nolf (2013) to Batrachoididae.
Order Kurtiformes Jordan, 1923 Family Apogonidae Günther, 1859 Genus Fig. 4E 1982 1984
One otolith from level 11.
Aquitanian of SW France (Steurbaut, 1982) and the MHB.
This specimen is significantly shorter than those assigned to
Order Blenniiformes Bleeker, 1860 Family Blenniidae Rafinesque, 1810 Genus Fig. 4G
One otolith from level 11.
This otolith is triangular in shape with a sulcus divided into an
oval-shaped ostium and a thinner but approximately equal in length oval
cauda that slightly turns towards the dorsal side. These characteristics
make this specimen similar to “
Order Pleuronectiformes Bleeker, 1859 Family Bothidae Smitt, 1892 Genus Fig. 4H 1952 1962 1979 1980 1981 1984 1992 1999 2004
One otolith from level 11.
Miocene of the Styrian Basin (Weinfurter, 1952), middle Miocene of NW Germany (Weiler, 1962), lower–middle Miocene of the Aquitanian Basin (Steurbaut, 1979, 1984), Miocene of Portugal (Steurbaut and Jonet, 1981), middle Miocene (Badenian) of Poland (Radwanska, 1992), lower Miocene of northern Italy (Nolf and Brzobohaty, 2004) and southern France (Nolf and Cappetta, 1980), and Aquitanian of the MHB.
This small otolith is rectangular in shape, with rounded angles.
The sulcus is sloping posteroventrally and approximately straight, divided
into a long ostium and a rectangular, short cauda. In contrast to the
specimen figured by Nolf and Brzobohaty (2004), the otolith found in Felli
shows a more regular rectangular shape. Our specimen is quite similar to the
modern species
Family Soleidae Bonaparte, 1832 Genus Fig. 4I 1906 1979 1984 1989 1989 1992 1999 2004
Two otoliths from level 11 and one otolith from level 12.
Lower Miocene of Italy (Nolf and Brzobohaty, 2004), the Aquitanian Basin (Steurbaut, 1984), and the MHB. Middle Miocene (Badenian) of Poland (Radwanska, 1992).
The otoliths of
Order Perciformes Bleeker, 1859 Family Serranidae Swainson, 1839 Genus Fig. 4J–K 1984 2013
Two otoliths from level 11 and two otoliths from level 12.
Lower Miocene of the Aquitanian Basin (Steurbaut, 1984) and the MHB.
These otoliths have a long sulcus, comprised of a small circular
ostium and a long cauda, which turns toward the ventral area and opens in the
posterior end. The dorsal rim is straight. Compared to the modern species
Family Cepolidae Rafinesque, 1810 Genus Fig. 4L 1984 2013
Two otoliths from level 11.
Lower Miocene of the Aquitanian Basin (Steurbaut, 1984) and the MHB. Priabonian–lower Oligocene of SE France (Nolf and Girone, 2008; Girone and Nolf, 2009).
These otoliths are boat-shaped and have open, divided sulcus. The
ostium is oval–rectangular and has an oval colliculum, whereas the cauda is
oval-shaped, with an oval colliculum, and placed more dorsally than the
ostium. There is a pronounced ventral fissure. These specimens have distinct
posterior and posterodorsal angles that only appear on the otoliths of
Order Spariformes Bleeker, 1876 Family Sparidae Rafinesque, 1810 Genus Fig. 4M–N
Six otoliths from level 11.
These otoliths are oval-shaped, with a small circular–oval ostium
and a long straight cauda. The ventral area is distinctly larger than the
dorsal area, and its rim is rounded.
Genus
One otolith from level 11 and one otolith from level 12.
These otoliths are fusiform in shape with a well-curved ventral rim and a sulcus divided into a triangular ostium and a long straight cauda, which is curved at the posterior end.
Genus Fig. 4O
One otolith from level 11.
This otolith is characterized by a pronounced ventral angle. The
sulcus is divided into a triangular ostium and a long cauda, which curves at
its posterior end. The dorsal area forms a clear angle in the anterior part.
There is some resemblance to
Genus Fig. 3M–O
Nine otoliths from level 11 and seven otoliths from level 12.
The general shape of the otoliths is fusiform. They have a straight
sulcus and a triangular ostium, which is characteristic of all
Paleogeographic map of the proto-Mediterranean, showing its connections to the Paratethys, Atlantic, and Indo-Pacific realms, and the location of the Mesohellenic Basin (MHB) and the Felli section (modified after early Burdigalian scheme of Popov et al., 2004), and list of the species identified at Felli color-coded to indicate their paleobiogeographic distribution.
The fish fauna of the Aquitanian MHB is quite diverse. We identified 19
species from 17 genera, including 2 new species:
The geological events that led to the formation of the proto-Mediterranean have shaped the distribution of marine taxa (Hou and Li, 2018; Worm and Tittensor, 2018). In the area of the Western Tethys, the late Eocene–middle Miocene MHB (Fig. 5) constituted a marine corridor at the border between the proto-Mediterranean and the Paratethys (Rögl, 1998); the proto-Mediterranean Sea developed due to the closure of the western part of the Tethys Ocean (Bialik et al., 2019; Torfstein and Steinberg, 2020). At this time, the proto-Mediterranean Sea, including the MHB, transited from a global biodiversity hotspot to a subtropical marine sea (Renema et al., 2008). Therefore, any faunal exchanges between the proto-Mediterranean, the Paratethys, the North Sea, the Atlantic, and the Indo-Pacific realms would be expressed in this study area.
Possibly due to the warm Aquitanian climate (Zachos et al., 2001; Westerhold
et al., 2020), the distribution ranges of North Sea and NE Atlantic fish
species included the MHB in the south. Indeed, this is supported by the
distribution of the identified fish species (Fig. 5). Most fish species in
the MHB were also present in the NE Atlantic, and, in fact,
In the early Neogene, the Mediterranean–Iranian biogeographical province of mollusks (Harzhauser et al., 2002) covered part of the Western Tethys region. The molluscan fauna in this province had a similar taxonomic composition with those of the North Atlantic of France and the Paratethys (Harzhauser et al., 2002; Lozouet, 2014), as in the case of fishes. Shallow marine faunas from the Indo-West Pacific show high degrees of endemism in the early Miocene (Harzhauser et al., 2007, 2017), whereas a turnover in the composition of nearshore mollusks is evident in the Oligocene to early Miocene in the Indian Ocean (Harzhauser et al., 2009).
The molluscan fauna of the Felli section is most similar to shallow marine and
coastal assemblages from the NE Atlantic and the Paratethys (Thivaiou et
al., 2019). However, in contrast to fishes (for which we do not have an
Indo-Pacific fossil record to compare with), the molluscan fauna of the Felli
section also includes genera that are characteristic of subtropical to
tropical environments (Houbrick, 1991; Janssen et al., 2011), such as the
widespread coastal mudflat
The fish fauna of the early Miocene MHB was in general influenced by the connectivity of the proto-Mediterranean to its surrounding marine basins. The early Miocene fish fauna of the proto-Mediterranean, as revealed by the otolith assemblage of the Felli section, was a mixture of Atlantic, Paratethyan, North Sea, and Mediterranean endemic elements. Unfortunately, the fossil record so far for this interval has been scarce. Nevertheless, the present findings offer some insight into the early Miocene evolution of the Mediterranean marine fish fauna. Future research should aim to fill in the considerable gaps in the record for the early–middle Miocene, especially in the Indo-Pacific realm.
The supplementary data are available open-access with this article.
The supplement related to this article is available online at:
KA was responsible for data curation, formal analysis, investigation, methodology, resources, and writing; DT for conceptualization, funding acquisition, investigation, methodology, resources, and writing; and EK for investigation, resources, and writing.
The authors declare that they have no conflict of interest.
Publisher's note: Copernicus Publications remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This research has been co-financed by Greece and the European Union (European Social Fund-ESF) through the operational program “Human Resources Development, Education and Lifelong Learning 2014–2020” in the context of the project “Mollusc and fish migrations in the dynamic environments of the early to middle Miocene in the Mediterranean” (MIS 5047960). The authors would like to thank Gary Stringer and the anonymous reviewer for their constructive comments.
This research has been supported by the Ministry of National Education and Religious Affairs (grant no. MIS 5047960).
This paper was edited by Florian Witzmann and reviewed by Gary Stringer and one anonymous referee.