Umbrina canariensis Valenciennes, 1843

Umbrina canariensis Valenciennes, 1843 View in CoL

Figure 28f View Fig

1993 Umbrina aff. canariensis Valenciennes, 1843 — Schwarzhans: Fig. 88–90.

2003 Umbrina canariensis Valenciennes, 1843 —Mendiola & Martínez: pl. 2, Figs. 3–7 View Fig View Fig View Fig View Fig View Fig , pl. 3, Figs. 1 View Fig , 2 View Fig .

2003 Umbrina aff. canariensis Valenciennes, 1843 —Mendiola & Martínez: pl. 4, Figs. 1–4 View Fig View Fig View Fig View Fig .

Material 43 specimens, Dar bel Hamri, Zanclean (figured specimen SMF PO 101.272 ) .

Discussion Several large and well preserved specimens have now been obtained from Dar bel Hamri confirming the identitiy of these otoliths, which previously have been only tentatively allocated as U. aff. canariensis (see Schwarzhans, 1993).

Diversification level and environmental assessment Ninety-six otolith-based species have been identified based on 4375 specimens collected from four locations along the Oued Beth and one location near Asilah ( Table 1), whereby 4250 otoliths were obtained from a single location, the coquina at the base of section 1, approximately 1.5 km south of Dar bel Hamri, with 95 species. Terefore, only location 1 near Dar bel Hamri qualifies for a quantitative assessment of the bony fish fauna. However, only subsample 1 with 1202 specimens can be quantitatively evaluated because subsample 2 was screened off at 2 mm mesh diameter and thus small species are not adequately represented in it. Percentages in the following therefore reflect only subsample 1 ( Table 1). Te two most common species are Afroscion trewavasae (19.55%) and Diaphus maghrebensis (16.39%), together accounting for 35.94% of the entire assemblage ( Table 1). Te diversification index is 31 of the most common species to reach the threshold of 90% of all identified species. Tis is an exceptionally high diversification index and in fact the highest ever recorded in any otolith assemblage. Tis high diversity is probably a result of several interrelating effects, such as environment, sedimentary facies, water depth, rich and diverse food supply at various trophic levels, and the biogeographic situation (see below).

Te coquina of Dar bel Hamri, from where the otoliths were obtained, has been deposited in a subaqueous environment, probably at moderate depth on the middle to lower shelf. Coquina accumulations observed in Late Miocene/Early Pliocene sediments of Portugal, the Huelva Basin in Spain, and the Rharb Basin in Morocco have been interpreted by Gonzales Delgado et al. (1994) as caused by winnowing from storm activities in shallow marine environments below the wave base. However, the composition of the otolith assemblage points to a deeper environment in a middle to lower shelf position that would be below the storm wave base. Te majority of the 43 extant fishes occurring as fossils in Dar bel Hamri occur at water depth of 50 to 100 m (55.8%), another 18.6% in water shallower than 50 m and the remainder in water deeper than 100 m ( Table 2). About 58% of the 43 extant fishes occurring as fossils in Dar bel Hamri have a demersal life habitat ( Table 2) making them relatively reliable depth indicators. Te winnowing responsible for the formation of the coquina and the accumulation of fossils in the sediment at Dar bel Hamri instead could have been caused by subaqueous currents, possibly as a result of tidal reflux. Such explanation is supported by the report of a Late Miocene/Early Pliocene channel observed on seismic sections due east of Dar bel Hamri ( Capella et al., 2017). Te current and winnowing at the base of the early Zanclean may also have been responsible for some reworking and erosion of directly underlying sediments of (late) Messinian age in the area. Furthermore, the current activity could have led to an increase in the availability of food in the trophic chain. In combination with the water activity this in turn could have led to an unusually high percentage of large, adult fishes as expressed in the high percentage of relatively large otoliths in the coquina. Te most abundant species, Afroscion trewavasae , is a sciaenid of a group that today feeds primarily on small, mostly nektonic fishes and large invertebrates. Te abundance of such a fish, particularly with adult specimens, is unusual and supports the hypothesis of an increased food supply in the depositional environment. Te abundance of large otoliths also increases the potential for their identification, which is somewhat counterbalanced by a nearly ubiquitous mild to moderate mechanical erosion, which one would expect in such a facies. Te other, stratigraphically comparable locations at Sidi Mohamed ech Chleuh, Kef Nsour and Jebel Zebbouj have yielded much fewer otoliths and are dominated by myctophids. Te myctophid otoliths in these locations were mostly well preserved including the frail denticles along the ventral rim of Diaphus otoliths, and thus indicate no or very little erosion in a more calm and possibly also deeper environment. Asilah has yielded even fewer otoliths, which are often somewhat leached hampering identification. Tis small assemblage contains only species also known from Dar bel Hamri.

Lyellian percentage

Fourty-three species identified by means of otoliths in the Early Pliocene of Dar bel Hamri are also known from today. Tis compares to 39 fossil species and 14 that cannot be identified to species level. Disregarding the latter which could either represent extant or extinct species, the Lyellian percentage thus amounts to 52.4%. A calculation on the same basis for the otolith assemblage recently described from the Pliocene of Estepona near Málaga, southern Spain, by van Hinsbergh and Hoedemakers (2022) arrives at a Lyellian ratio of about 67%. An evaluation of the Lyellian percentage for goby otoliths in the Mediterranean arrived at 70% ( Schwarzhans et al., 2020). Overall, the Lyellian percentage of otolith associations in the Zanclean of the Mediterranean is in the order of 72% and for the Piacenzian 78%. However, articulated skeletons exhibit a lower Lyellian percentage in the Early Pliocene of the Mediterranean than otoliths ( Landini & Sorbini, 1992, 2005), which may be regarded as an expression of the generally more conservative approach in otolith research. Overall, the Lyellian percentages of Early Pliocene otolith associations vary between about 50% (tropical West Atlantic Sciaenidae , Morocco) and about 75% ( New Zealand) (see Schwarzhans, 2019a). Tus, the Moroccan otolith-based fauna described here is remarkable for a comparably low Lyellian percentage, which will be discussed further in the chapter below about a potential “Maghrebian bioprovince” during the Pliocene.

Te ratio of extant versus extinct species is unevenly distributed among the families represented. Considering families with at least three identifiable species, one can note that extinct taxa prevail in the Myctophidae (5 extinct species in a total of 8 species), Gobiidae (4 in 5), Bothidae (3 extinct species), Trachinidae (with 2 extinct species in 3) and Uranoscopidae (3 extinct species in 4). I interpret the low yield of extant species in the Early Pliocene of these families as an indication of a dynamic speciation in the recent geologic past. Te dynamic recent speciation is matched with observations made about Pliocene myctophid otoliths from tropical America ( Schwarzhans & Aguilera, 2013). In respect to gobies, the extant–extinct ratio is somewhat mixed. Schwarzhans et al. (2020) calculated a Lyellian percentage of about 70% for the Gobiidae in the Early Pliocene of the Mediterranean. A calculation from the species list provided by van Hinsbergh and Hoedemakers (2022) for the Pliocene of Estepona near Málaga, southern Spain, arrived at about 62%. Tus, the yield of extinct gobiid species in Dar bel Hamri is distinctly higher than in Mediterranean locations, even though all except one of the species ( Deltentosteus planus ) found in Morocco are also known from the Mediterranean. I find no ready explanation for this discrepancy. Conversely, the yield of extinct species is low in the Congridae (1 extinct species in 4), Carapidae (1 extinct species in 3), Soleidae , and Sciaenidae (1 extinct species in 5) and particularly in the Sparidae (2 extinct species in 15). Te high percentage of extant species in the Early Pliocene record of these families could indicate that much of the speciation that led to the extant fauna occurred earlier. However, the low yield of extinct taxa in the family with the most species in Dar bel Hamri, the Sparidae , could have a different cause. Otoliths of the Myctophidae ( Brzobohatý & Nolf, 1996, 2000; Schwarzhans, 2013b; Schwarzhans & Aguilera, 2013) and of the Gobiidae ( Schwarzhans et al., 2020; Bratishko et al., 2023 ms, and literature cited in both studies) have been studied extensively and have in part been calibrated by finds of otoliths in situ ( Bedini et al., 1986; Reichenbacher & Bannikov, 2021, 2022; Schwarzhans et al., 2017). As a result, the character analysis of otoliths of these two groups is more advanced than in Sparidae and aids the recognition of species. Comparable studies of otoliths are lacking in the case of the Sparidae , and it is, therefore, possible that the species identification is not as accurate as in the Myctophidae and Gobiidae and could in fact be too conservative.

Comparison with Mediterranean assemblages from the Pliocene: implications for fish remigration from the Northeast Atlantic into the Mediterranean after the Messinian Crisis

Te terminal Miocene in the Mediterranean is well known for the late Messinian Salinity Crisis (MSC) that was caused by the closure of the Mediterranean Sea to the northeastern Atlantic in the West during that time. Both seas became fully reconnected again beginning with the Pliocene. Since the first article on the MSC (“When the Mediterranean dried up” by Hsü, 1972), a large body of research has been published on the subject, and what precisely happened—whether marine life was extinguished in the Mediterranean during the event, the water budget, base level drop, and so on—is still very much under discussion (e.g., Roveri et al., 2014, 2016; Ben- Mosche et al., 2020; Gvirtzman et al., 2022; and literature cited in these articles). Recently, Carnevale and Schwarzhans (2022) showed that stenohaline marine fishes lived in the Mediterranean through the MSC, at least periodically, as evidenced by articulated fish skeletons and otoliths, which is in contrast to a study by Andreetto et al. (2021), who postulated that all marine fossils found in sediments of the MSC interval resulted from reworking of pre-MSC rocks. Te reworking hypothesis cannot be maintained for the explanation of the presence of articulated skeletons of marine fishes in MSC rocks. Another subject of continued dispute is the role of re-flooding of the Mediterranean with the onset of the Early Pliocene (Zanclean) ( Bache et al., 2012; Garcia-Castellanos et al., 2009; Micallef et al., 2018; and literature cited in these articles).

During the Pliocene, the Rharb Basin was a funnel-shaped embayment that represented the relict of the last connection of the Atlantic with the Mediterranean

( Fig. 29 View Fig ) ( Achalhi et al., 2016; Capella et al., 2017; de Weger et al., 2020a, 2020b, 2020c; Flecker et al., 2015; Flinch, 1993; Martin et al., 2014; Pérez-Asensio, 2021). Te Rharb Basin is ideally situated to investigate the composition of the fauna during the late stage of the Atlantic–Mediterranean connection and the fauna during the re-flooding when the Rharb Basin represented the reservoir from which a proportion of the remigration must have been recruited. Little is known so far about the Late Miocene fish fauna of the Rharb Basin from the few otoliths collected from outcrops at Kef Nsour and Chaba Kaudiat el Mogen, which are all known in the Early Pliocene as well, except for Diaphus draconis . Te Early Pliocene fish fauna from Dar bel Hamri and the other studied locations is significant and allows for a correlation with time-equivalent assemblages from the Mediterranean. Indeed, there have been many studies about Pliocene otolith associations in the Mediterranean realm ( Fig. 30 View Fig ): from Italy for example Dieni (1968), Weiler (1971), Schwarzhans (1978a), Anfossi and Mosna (1979), Nolf and Cappetta (1988), Girone (2006), Nolf and Girone (2006); from Greece Agiadi et al., (2013, 2017, 2019a, 2019b); from southern France Schwarzhans (1986), Nolf and Cappetta (1988); from southern Spain Nolf and Martinell (1980), Nolf et al. (1988), Mendiola and Martínez (2003), van Hinsbergh and Hoedemakers (2022). Tese many articles contrast with only two otolith associations described from the adjacent Atlantic: one from the Piacenzian of central Portugal described by Nolf and da Silva (1997) and the other this study from Morocco. Many of the Zanclean otolith assemblages described from the Mediterranean realms originate from deep marine settings with predominant meso- to bathypelagic and bathydemersal fishes, while the Portuguese and Moroccan faunas are characterized by middle to lower shelf fishes associated with a few upper slope elements. Te assemblage described from Estepona in southern Spain by van Hinsbergh and Hoedemakers (2022) is the most important for comparison, because it is rich (209 species, 107 thereof in the Zanclean), includes faunal elements of the lower shelf similar to Morocco, and is located just about 50 km to the east of the Strait of Gibraltar. Te nearest location studied in Morocco is Asilah, about 50 km to the west of the Strait of Gibraltar and about 130 km from Estepona. Dar bel Hamri is 190 km south of the Strait of Gibraltar and about 260 km from Estepona. However, Dar bel Hamri is much closer to Estepona than the other nearest Mediterranean locations (450 km to Guardamar, described by Mendiola & Martínez, 2003, and 850 km to Papiol near Barcelona, described by Nolf et al., 1998).

Fifty of the 82 identified species in the Early Pliocene of the Rharb Basin have also been recorded from time-equivalent strata of the Mediterranean ( Table 1; 61%), thereof 39 species in the Zanclean and/or Piacenzian of Estepona ( Fig. 29 View Fig ). Tis ratio is consistent with the similarity coefficient calculated by Ben Moussa (1994) for Pliocene bivalves of Morocco in comparison with Mediterranean localities. Nevertheless, the fish fauna shows a lower correlation than one might expect over such a small distance and under the consideration of the recruitment of the Mediterranean fauna from the adjacent Northeast Atlantic during the Early Pliocene re-flooding event. It appears that not all species of the Northeast Atlantic were actually able to migrate into the Mediterranean, and furthermore there could be environmental differences at play in the locations that could mask faunal exchange. However, it is worth elucidating those 32 species that have not been found in the Mediterranean. Tirteen of those represent extant species, of which today 5 occur in the Atlantic off Morocco, 7 primarily south of the Mauritanian upwelling zone in the tropical East Atlantic and 1 in the tropical West Atlantic. Another 19 species, including all of the new species, could be considered potentially endemic to the area (a “Maghrebian bioprovince”, see below). Pterothrissus darbelhamriensis of those potentially endemic species may in fact represent an allopatric vicariant species of the Mediterranean P. compactus at the time. Pterothrissus darbelhamriensis was already considered by Schwarzhans (1981) as vicariant to P. compactus from the Mediterranean (known from the Tortonian [ Fig. 9 h, j View Fig ] until Zanclean [ Fig. 9f–g, i View Fig ]). It has now also been identified from the Piacenzian of Estepona ( van Hinsbergh & Hoedemakers, 2022), but this is not considered contradictory to the interpretation, since it could represent a late immigrant from the Northeast Atlantic into the adjacent region of the Mediterranean. Te recognition of a vicariant species in the Northeast Atlantic and the Mediterranean in the Zanclean (and ideally since the Late Miocene) supports the hypothesis of in situ survival of marine fish taxa in the Mediterranean, but it is so far restricted to a single conclusive case. Te more important outcome of the correlation of Northeast Atlantic and Mediterranean fishes of the Early Pliocene times is that a substantial number of Atlantic fish taxa apparently did not migrate into the Mediterranean during the re-flooding. Tis non-migratory effect could be caused by a warmer climate in the Rharb Basin than at the Strait of Gibraltar, as can be inferred from the presence of some southern elements then present in Morocco and putative endemic species. Tey are primarily the species with tropical East Atlantic affinities that have not been found in the Mediterranean.

Comparison with extant fish faunas and its implications Te otolith association of the Early Pliocene of Dar bel Hamri and nearby locations contains 43 species that still exist today. Te majority of them are distributed over the subtropical to temperature zones (74.4%), 30.2% thereof exclusively in the subtropical zone ( Table 2). Te distribution of only 20.9% of the species range into the temperate zone, and 25.6% are exclusively tropical ( Table 2). Tirty-two species (74.4%) of the extant fishes occurring as fossils in Dar bel Hamri live today in the same general area (i.e., in the Northeast Atlantic off the coasts of Morocco) ( Table 3); and 9 species (20.9%) live today in the tropical East Atlantic, chiefly south of Mauretania.

Clearly, the high content of persistent species indicates a high degree of continuity in the faunal composition of species occurring today and during the Early Pliocene in the region, but tropical West African species, which do not live off Morocco anymore or occur rarely as stray specimens, also contributed a significant component. Teir presence indicates that the water temperatures in the sea off northwestern Morocco were significantly warmer in the Early Pliocene than they are today. Similar conclusions were drawn by Avila et al. (2016) on the basis of molluscs found in Late Miocene and Early Pliocene sediments on the Azores and many previous studies of molluscs cited therein. If the sea off northwestern Africa was warmer in the Early Pliocene than it is today, this must have had consequences for the paleo-currents in the region. Today’s faunal provinces along the northwestern coast of Africa are driven by the cool Canary Current, the permanent coastal upwelling between Cape Yubi and Cape Blanc, and further offshore by the position of the Intertropical Convergence Zone ( Matsuzaki et al., 2011; Michel et al., 2011). Te change from a tropical sea off Morocco to the current subtropical situation dominated by the cool Canary Current and separation from the tropical West African sea by the coastal upwelling system probably occurred during the Late Pliocene. Studies of the mollusc faunas from the Mediterranean, the Azores and the Canary Islands have revealed the disappearance of tropical taxa between 4.2 and 3.0 Ma (i.e., latest during the mid-Piacenzian cooling event) ( Avila et al., 2016, and literature cited therein). Even though indications for upwelling along the Northwestern African coast appear to have been present since the Early to Middle Miocene (Diester-Haas & Schrader, 1979), one has to assume that during the Late Miocene and Early Pliocene its intensity was insufficient to keep (some) tropical West African fishes from living in the Rharb Basin. However, some degree of separation still must have been effective, since most Early Pliocene fishes exhibit a clear subtropical Northeast Atlanto-Mediterranean relationship. In respect to the total of 74 biogeographically interpretable species (excluding fossil mesopelagic and bathydemersal fishes of uncertain biogeographic affinities), 42 species corresponding to 56.8% are identical or related to extant species in the same area ( Table 3). Twenty-three species (31.1%) are identical or related to tropical East Atlantic species ( Table 3). Nineteen species (25.6% of above 74 species) are putative endemics during the Early Pliocene of Dar bel Hamri; they are mostly related to extant Mediterranean, tropical East Atlantic and South African species ( Table 3). Of about 600 marine bony fish species recorded from Morocco, the Canary Islands, Madeira and the Azores today, only about 30 (5%) represent northward extensions of species with primarily tropical East Atlantic distribution patterns (calculated from Froese & Pauly, 2022). Te relationships of the 31 extinct otolith-based fish species at Dar bel Hamri (of the 74 biogeographically interpretable species) on a stand-alone basis are naturally less certain. Te largest group among them is 19 species (25.6%) that have not been recorded from Mediterranean localities and hence are considered of potentially endemic nature ( Table 3).

When investigating the probable provenances of the more exotic species ( Table 3; Fig. 31 View Fig ), some more remote relationships are notable. Paratrisopterus glaber shows the closest relationship with northern Atlantic/North Sea Basin taxa. Tree species (4.1%) exhibit affinities to the tropical West Atlantic ( Paraxenomystax cf. bidentatus , Myripristis ouarredi and Verilus mutinensis ), three (4.1%) to South Africa ( Centroberyx vonderhochti , Uranoscopus hoedemakersi and Afroscion trewavasae ), and two (2.6%), namely Brotula aff. multibarbata and Laeops rharbensis , to the Indo-West Pacific ( Table 3). A somewhat special case is that of the genus Rhynchoconger which has had a long history in Europe since Eocene times. Its latest representatives are R. carnevalei in the Early Pliocene of the Mediterranean and R. pantanellii in the Pliocene of the Mediterranean and Northeast Atlantic. Te nearest occurrence of the genus today is in the central West Atlantic, but otoliths found in Holocene dredge samples in the Gulf of Guinea ( Schwarzhans, 2013a) indicate that the disappearance of the genus from the East Atlantic is either very recent or false. Te occurrence of another species with a West Atlantic relationship, Verilus mutinensis , is of a different nature, as it probably represents a vicariant East Atlantic/Mediterranean species ranging from the Late Miocene Tortonian ( Bassoli, 1906) to the middle Pleistocene Calabrian ( Agiadi et al., 2018) before the lineage became extinct in the East Atlantic. As for the Indo-West Pacific affinity, Brotula aff. multibarbata could possibly represent a fossil species (subject to further material becoming available) and in any case represents a clade not present anymore in the Atlantic ( Froese & Pauly, 2022).

Te South African link is particularly interesting and perhaps unexpected, as it also contains the most common otolith-based species ( Afroscion trewavasae ) of the entire assemblage. Te extant A. thorpei is geographically restricted to a rather small area in southeast Africa (Sasaki in Heemstra et al. 2022). Te occurrence of A. trewavasae in Morocco and Portugal clearly represented a vicariant species, and the distribution of Afroscion in southeast Africa must thus be considered a relict occurrence. Tis coincides with South Africa representing a classical region for (secondary) endemism (http://lntre asures.com/rsa.html). Te same explanation may hold for Uranoscopus hoedemakersi , which is thought to represent a vicariant species to the extant U. archionema off southeastern Africa. Centroberyx is a slightly different case as it is today known from seven species with a disjunctive distribution pattern, richest in Australia and New Zealand with an outlier species each in Japan, Taiwan, and South Africa ( Froese & Pauly, 2022). Centroberyx is a genus with a long history reaching back into Cretaceous times and is well known from European basins until the Eocene, after which it becomes rather sparse (e.g., Schwarzhans & Jagt, 2021). Its current distribution is clearly a relict of a formerly much wider pattern. In Europe, the last record so far was C. manens Nolf & Brzobohatý, 2004 , from the Middle Miocene. Te large specimens of Centroberyx vonderhochti in the Pliocene of the Rharb Basin represent a different lineage from C. manens , that is probably related to the extant C. spinosus (Gilchrist, 1903) from South Africa (see Schwarzhans & Jagt, 2021).

Was there a “Maghrebian bioprovince” during the Early Pliocene?

Today’s fish fauna in the seas around Morocco and the Macaronesian archipelago (Canary Islands, Madeira, Azores) includes about 600 species, of which about 30 species (5%) can be considered endemic and another 5% as primarily tropical West African fishes that also occur rarely to the north of the Mauritanian upwelling system (calculated from Froese & Pauly, 2022). Tis bioprovince has been named the subtropical Mediterranean–Moroccan Province by Avila et al. (2016). Most of the 560 or so non-endemic indigenous fishes have distribution ranges northward to the Bay of Biscay or the British Isles, into the Mediterranean, and/or southward to various extents.

Te situation was quite different in the Early Pliocene (and Late Miocene), when the Moroccan coast was under warmer climatic conditions and the Transition Zone was located further north. Based on analysis of the molluscan fauna, Avila et al. (2016) postulated a Pliocene Mediterranean–West African Province that stretched from the Azores to the southern tip of Portugal and incorporated the entire Mediterranean and the Gulf of Guinea. Te fish fauna from the Rharb Basin, however, indicates that some degree of differentiation existed in this large area at least toward the Mediterranean, and is also inferred toward tropical West Africa ( Fig. 32 View Fig ). Te Early Pliocene otolith-based fish fauna of the Mediterranean is exceptionally well known and includes more than 200 identified taxa. Te recent monograph of the otolith assemblage from Estepona in southwest Spain not far from the Strait of Gibraltar is particularly important for correlation. Only half (52%) of the otolith taxa identified in the Rharb Basin were also identified from the Pliocene in the Mediterranean. Nineteen species in the Rharb Basin are potential endemics, which is much higher than endemic species in the region today (25.6% vs. 5%), even taking into account uncertainties in the fossil data coverage. Tere is no comparable Early Pliocene otolith assemblage known from the Gulf of Guinea realms, the nearest being from the Middle Miocene of Gabon ( Schwarzhans, 2013c). However, it can be stated that the tropical West African influence in the Early Pliocene fish fauna of the Rharb Basin is significant at about 31.1% (species also occurring today and those related to extant West African species). Tis compares to about 5% of species off Morocco today shared with tropical West Africa.

Tus, the assessment of the otolith-based fish fauna in the Rharb Basin does not justify combining it with the Early Pliocene Mediterranean nor with tropical West African fauna, the latter deduced from the extant faunal composition. I therefore postulate the presence of an Atlantic Moroccan bioprovince during the Early Pliocene, and potentially Late Miocene, which I propose to name the “Maghrebian bioprovince.”