Protoconch morphology, environmental constraints, and larval development

The morphological features of the gastropod larval shell, or protoconch, offer valuable insights into the developmental strategies of both extant and extinct gastropod species. In Euthria, this is no exception. While these features may exhibit variations across different families, there are consistent traits associated with planktotrophic protoconchs in gastropods with feeding planktonic larvae and non-planktotrophic ones (i.e., those with non-feeding larvae). Representatives of species with planktotrophic development often display a distinctive high, multispiral conical protoconch comprising two to nine whorls.. By contrast, non-planktotrophic species typically exhibit a paucispiral protoconch consisting of 0.5 to two smooth whorls (e.g., Jackson, Reference Jackson1974; Stanley, Reference Stanley1979; Jablonski, Reference Jablonski1986; Vendetti, Reference Vendetti2007). As a general rule, species with short larval phases are less likely to disperse widely and tend to form genetically isolated populations, leading to species that are geographically restricted and geologically short-lived, whereas planktotrophic development prevents genetic isolation and leads to species with a greater geographic range and geological longevity (Jackson, Reference Jackson1974; Stanley, Reference Stanley1979; Jablonski, Reference Jablonski1986). Conversely, planktotrophy—in larvae with longer planktic phases—diminishes genetic isolation, being associated with species with expanded geographic distribution and geological longevity (Jackson, Reference Jackson1974; Stanley, Reference Stanley1979; Jablonski, Reference Jablonski1986).

It is widely accepted that the predominant direction of evolutionary change in mode of development is from species with planktotrophic larvae to those with non-planktotrophic development. Moreover, it is thought to be rare or practically impossible for planktotrophic larvae to evolve from non-planktotrophic ones without being obviously distinct from their planktotrophic ancestor (Collin, Reference Collin2004; Collin et al., Reference Collin, Shishido, Cornejo and Lesoway2021). Non-planktotrophic development has evolved independently on multiple occasions (Ponder and Lindberg, Reference Ponder and Lindberg1997), and when this happens, those characters involved in feeding and swimming in the ancestral planktotrophic form are often reduced or lost in benthic nonfeeding larvae or in direct developers (Collin, Reference Collin2004). This pattern of evolution in mode of development is biased in the direction from planktotrophic to non-planktotrophic (Strathmann, Reference Strathmann1985; Hart, Reference Hart2000) and is widely considered irreversible (Collin et al., Reference Collin, Chaparro, Winkler and Véliz2007).

All extant Atlantic and Mediterranean Euthria species show rather bulbous protoconchs with 1.25 to 2.5 whorls (Rolán et al., Reference Rolán, Monteiro and Fraussen2003). These characteristics suggest non-planktotrophy. However, we have not found any papers on present-day Euthria gastropods confirming this conclusion by direct observation.

Euthria species documented in the European Neogene fossil record have recently been the subject of comprehensive reviews with protoconch data and, in some cases, illustrations (Lozouet, Reference Lozouet1999, Reference Lozouet2021; Van Dingenen et al., Reference Van Dingenen, Ceulemans and Landau2017; Landau et al., Reference Landau, Ceulemans and Van Dingenen2019a; Harzhauser and Landau, Reference Harzhauser and Landau2024; Landau and Harzhauser, Reference Landau and Harzhauser2024; hoc opus: summary Table 1). Among the species investigated, only the French Atlantic E. pseudomarginata Peyrot, Reference Peyrot1928, spanning the upper Oligocene to Lower Miocene of the Aquitaine Basin, the Euthria sp. 1 as identified by Lozouet (Reference Lozouet2021) from the upper Oligocene of the French l’Adour Basin, and E. brunettii Harzhauser and Landau, Reference Harzhauser and Landau2024, originating from the Middle Miocene Paratethys, exhibit shells featuring characteristics suggestive of planktotrophic development, namely, tall multispiral protoconchs with small nuclei.

Table 1.

Euthria species in Oligocene–Pliocene European assemblages that have recently been reviewed and their protoconchs reliably described and/or illustrated, their geological distribution, and number of protoconch whorls. Data from Lozouet (Reference Lozouet1999, Reference Lozouet2021), Van Dingenen et al. (Reference Van Dingenen, Ceulemans and Landau2017), Landau et al. (Reference Landau, Ceulemans and Van Dingenen2019a), Harzhauser and Landau (Reference Harzhauser and Landau2024), Landau and Harzhauser (Reference Landau and Harzhauser2024)

These data suggest that Euthria evolved away from its primitive planktotrophic mode of development no later than the Late Miocene. Similar shifts away from planktotrophy during the Late Miocene to the present are documented in various gastropod genera within European present-day faunas. Landau and Harzhauser (Reference Landau and Harzhauser2024) reported a similar loss of planktotrophy in Aplus De Gregorio, Reference De Gregorio1885 (Buccinoidea, Pisaninae) from the Pliocene to the present, and possibly in Colubraria Schumacher, Reference Schumacher1817/Cumia Bivona e Bernardi, Reference Bivona e Bernardi1838 (Buccinoidea, Colubrariidae), two genera distinguished solely by the presence of paucispiral protoconchs in the latter.

Puillandre et al. (Reference Puillandre, Sysoev, Olivera, Couloux and Bouchet2010) reported a gradual loss of planktotrophy, inferred from protoconch morphology, in the deep-water gastropod genus Bathytoma Harris and Burrows, Reference Harris and Burrows1891 (Conoidea, Borsoniidae) in the western Pacific. Protoconch characteristics varied across time: Eocene Bathytoma species exhibited protoconchs with 3.5–4.5 whorls, Oligocene species had 3.0–3.5 whorls, Pliocene ones showed 3.0 whorls, and contemporary species, now limited to the Indo-Pacific, display protoconchs with 1.5 whorls and a large nucleus. Notably, all but one present-day species exhibits restricted distributions. In the same family Borsoniidae, Landau and Harzhauser (Reference Landau and Harzhauser2022b) documented the loss of planktotrophy in Asthenotoma Harris and Burrows, Reference Harris and Burrows1891 from the Miocene to the Pliocene. Furthermore, Landau et al. (Reference Landau, Harzhauser and Giannuzzi-Savelli2022, p. 161) described a similar trend for Clathromangelia di Monterosato, Reference di Monterosato1884 (Conoidea, Raphitomidae) from the Middle Miocene to present. Within the genera Clavatula s.l. Lamarck, Reference Lamarck1801, Perrona Schumacher, Reference Schumacher1817, and Tomellana Wenz, Reference Wenz and Schindewolf1943 (Conoidea, Clavatulidae), some upper Oligocene (Lozouet, Reference Lozouet2021) and Miocene (Harzhauser et al., Reference Harzhauser, Landau and Janssen2022) species exhibited multispiral protoconchs. Contrastingly, species from the Pliocene to the present showed paucispiral protoconchs (Landau and Harzhauser, Reference Landau and Harzhauser2022a).

Within the Mediterranean Raphitomidae Bellardi, Reference Bellardi1875, Oliverio (Reference Oliverio1996) and Giannuzzi-Savelli et al. (Reference Giannuzzi-Savelli, Pusateri and Bartolini2018) proposed a speciation event during the early Pleistocene, leading to the emergence of species pairs exhibiting either planktotrophic or non-planktotrophic development. Oliverio (Reference Oliverio1996) also identified similar species pairs in gastropod genera such as Alvania Risso, Reference Risso1826, Rissoa Desmarest, Reference Desmarest1814, Vitreolina di Monterosato, Reference di Monterosato1884, Columbella Lamarck, Reference Lamarck1799, Nassarius Duméril, Reference Duméril1805, Mangelia Risso, Reference Risso1826, and Haedropleura Bucquoy, Dautzenberg, and Dollfus, Reference Bucquoy, Dautzenberg and Dollfus1883, suggesting a widespread occurrence of this phenomenon among Mediterranean prosobranchs. He considered the Pleistocene climatic deterioration a potential trigger for this phenomenon. Moreover, Oliverio (Reference Oliverio1996) noted that during phases of low sea level, the isolation of the western and eastern subbasins of the Mediterranean resulted in distinct developments. The gastropods of the western subbasin exhibited higher planktotrophy, while in the eastern subbasin they predominantly displayed non-planktotrophic development. This divergence underscores the impact of historical sea-level fluctuations on the reproductive strategies of Mediterranean prosobranch gastropods.

The presence of such species pairs in Euthria was not identified during this study. However, it is posited that the underlying forces fostering the loss of planktotrophy, whether manifested spatially (as seen in Raphitoma, Alvania, Rissoa, and so on) or chronologically (as observed in Euthria, Aplus, Colubraria, and so on), remain consistent. The isolation of populations, as discussed by Oliverio (Reference Oliverio1996), has occurred multiple times for Paratethyan species, driven by pronounced, geodynamically amplified fluctuations in relative sea levels (Harzhauser and Piller, Reference Harzhauser and Piller2007; Kováč et al., Reference Kováč, Hudáčková, Halásová, Kováčová and Holcová2017). Furthermore, the loss of planktotrophy during the Pliocene correlates with the onset of a global cooling trend (Westerhold et al., Reference Westerhold, Marwan, Drury, Liebrand and Agnini2020), akin to the Pleistocene event described by Oliverio (Reference Oliverio1996). The decline in sea surface temperatures appears to have exerted stress on the larvae of certain gastropods, prompting a shift to a non-planktotrophic mode of development in species of genera such as Asthenotoma, Bathytoma, and Euthria. Concurrently, numerous planktotrophic species became extinct. The limited dispersal capabilities of the non-planktotrophic species ultimately gave rise to endemic radiations among Euthria in the Cape Verde Archipelago (Fraussen and Swinnen, Reference Fraussen and Swinnen2016). This phenomenon is exemplified by the genus Lautoconus di Monterosato, Reference di Monterosato1923, which underwent an extraordinary endemic radiation, boasting nearly 50 species confined exclusively to this southern Macaronesian archipelago. Notably, the species of this genus also adopted non-planktotrophic development as their reproductive strategy (Duda and Rolán, Reference Duda and Rolán2005).

The impact of water temperature on development strategy is commonly referred to as Thorson’s (Reference Thorson1950) rule, which posits that higher latitudes and lower temperatures promote lecithotrophy and larger eggs, while planktotrophic species will thrive in tropical waters. Numerous studies have examined and verified Thorson’s rule for prosobranch gastropods, including works by Thorson (Reference Thorson1950), Picken (Reference Picken1980), Clarke (Reference Clarke1992), Gallardo and Penchazadhe (Reference Gallardo and Penchaszadeh2001), Collin (Reference Collin2003), and Pappalardo et al. (Reference Pappalardo, Rodríguez-Serrano and Fernández2014). However, during the Miocene and Pliocene, the Paratethys, the Mediterranean, and the adjacent Atlantic region were notably situated at lower latitudes, falling outside the traditional scope of Thorson’s rule. Nonetheless, the presumed loss of planktotrophy due to the decline of SSTs in the Central Paratethys and the Mediterranean Sea during this period might have been influenced by similar mechanisms.

Diversity and endemicity in Neogene to Recent Euthria

Today, Euthria is present in the Mediterranean Sea and the eastern Atlantic, extending down to Angola (Schoenherr and Rolán, Reference Schoenherr and Rolán2017), exhibiting a remarkable center of diversity around the Cape Verde Islands, where more than 22 endemic species have been identified (Rolán et al., Reference Rolán, Monteiro and Fraussen2003; Fraussen and Swinnen, Reference Fraussen and Swinnen2016). Endemicity along the West African coast is not as extreme as in the Cape Verde Archipelago, with Euthria annegretae Schroenherr and Rolán, Reference Schoenherr and Rolán2017 from Angola. The realization of the diversity of the genus coupled with local high endemism in present-day faunas has occurred only relatively recently. Rolán (Reference Rolán1987) provided the first comprehensive overview, identifying Euthria cornea (Linnaeus, Reference Linnaeus1758) in the Mediterranean and seven species from the Cape Verde Islands, one left in open nomenclature. Fraussen (Reference Fraussen1999) echoed this assessment, listing the same number of Atlanto-Mediterranean species while introducing six new Western Indo-Pacific species. Subsequent studies have consistently underscored the genus’s highly endemic character in the Cape Verde Archipelago (Rolán et al., Reference Rolán, Monteiro and Fraussen2003; Monteiro and Rolán, Reference Monteiro and Rolán2005; Fraussen and Swinnen, Reference Fraussen and Swinnen2016). In this context, the reason for the presence of only one species in the present-day Mediterranean, Euthria cornea (Linnaeus, Reference Linnaeus1758), exhibiting a remarkable degree of variability in shell morphology remains unclear. This becomes particularly perplexing considering that all fossil and remaining extant species exhibit relatively limited intraspecific variation in shell morphology. Despite being highly variable in shell shape and widely distributed in the Mediterranean, preliminary molecular data on E. cornea do not suggest the presence of more than one species (P. Bouchet, personal communication, 2024).

Today, E. cornea inhabits marine environments of normal salinity at depths ranging from 5 to 30 m, predominantly on rocky substrates. There is no available literature indicating that E. cornea has adapted to successfully exploit alternative habitats, such as muddy, sandy, or brackish environments. This observation is further reinforced by personal accounts (K. Fraussen, personal communication, 2024). It is reported to be a carnivorous scavenger (Syrides, Reference Syrides2019), feeding primarily on polychaetes and gastropods (Taylor, Reference Taylor1987). This species exhibits significant variability; axial sculpture may fade early in ontogeny or strengthen on later whorls with the development of tubercles at the shoulder. Moreover, variation in adult shell shape and size is much more marked than in any of its extant congeners (see Fraussen and Swinnen, Reference Fraussen and Swinnen2016). While certain forms can be attributed to distinct provenances, more frequently, specimens with diverse shapes and color patterns coexist (K. Fraussen, personal communication, 2024). Euthria cornea possesses a protoconch consisting of 1.5 whorls with a bulbous apex characteristic of non-planktotrophic development (Brunetti and Della Bella, Reference Brunetti and Della Bella2016, fig. 4D). Its geological history extends back only to the early Pleistocene, Calabrian. Furthermore, in the Mediterranean and in the Iberian shores of the Gulf of Cadiz, it occurs at the northern limit of its water temperature tolerance range, in the present-day subtropical Mediterranean–Moroccan Province (sensu Raffi et al., Reference Raffi, Stanley and Marasti1985; da Silva and Landau, Reference da Silva and Landau2007), given that Euthria is a relatively thermophilic genus.

Therefore, it is likely that E. cornea evolved from a Mediterranean Pliocene ancestor, and it appears to be the only species to have survived to the present day in the Mediterranean and the adjacent Atlantic coast of southern Portugal. However, the reason E. cornea should have become so abundant, variable, and widespread in that region today is unclear. It is important to emphasize that non-planktotrophic development does not preclude dispersal, yet E. cornea is confined mostly to the northern part of the Mediterranean–Moroccan Province. Nevertheless, as far as we are aware, molecular confirmation that all Mediterranean E. cornea records pertain to a single species is currently lacking.

Similarly, the recognition of both the diversity and the endemicity of the genus in the European fossil record has also emerged rather recently. Brunetti and Della Bella (Reference Brunetti and Della Bella2016) revised the Plio-Pleistocene biodiversity of the genus from Neogene basins of northern Italy, documenting four species from the Pliocene (Euthria perpiniana [Fontannes, Reference Fontannes1879], E. plioelongata [Sacco, Reference Sacco1890], E. ceddensis Brunetti and Della Bella, Reference Brunetti and Della Bella2016, E. adunca [Bronn, Reference Bronn1831]). In the past, many Neogene records of these species have been misassigned to the extant E. cornea, although it has a confirmed geological record dating back only to the early Pleistocene Calabrian, occurring only in the Mediterranean and on the northern shores of the Gulf of Cadiz (Brunetti and Della Bella, Reference Brunetti and Della Bella2016).

In their review of the Atlantic Upper Miocene and Lower Pliocene gastropod fossil record from the Loire Basin in northwestern France, Landau et al. (Reference Landau, Ceulemans and Van Dingenen2019a) reported two Euthria species from the Tortonian Assemblage I of Van Dingenen et al. (Reference Van Dingenen, Ceulemans, Landau and da Silva2015) (Euthria presselierensis Landau, Ceulemans, and Van Dingenen, Reference Landau, Ceulemans and Van Dingenen2019a, and E. recurvata [Millet, 1865]), both exclusive to this assemblage and endemic to the Neogene Ligerian Gulf (sensu Landau et al., Reference Landau, da Silva, Van Dingenen and Ceulemans2020). In addition, they identified two species within the Zanclean Assemblage III (Euthria palumbina Van Dingenen, Ceulemans, and Landau, Reference Van Dingenen, Ceulemans and Landau2017, exclusive to Assemblage III, and E. turonensis Peyrot, Reference Peyrot1938, both endemic to the Ligerian Gulf but the later also known from the Middle Miocene Langhian in the Loire Basin).

Lozouet (Reference Lozouet2021) examined the Buccinoidea from the Atlantic upper Oligocene of southwestern France, revealing a similar level of endemicity. He identified six species documented exclusively from the Chattian Oligocene and the uppermost Chattian and Lower Miocene of the l’Adour Basin (E. lanotensis Lozouet, Reference Lozouet1999, E. pseudomarginata Peyrot, Reference Peyrot1928, E. raulini Peyrot, Reference Peyrot1928, E. tarusatensis Lozouet, Reference Lozouet2021, alongside two species left in open nomenclature).

Revision of Euthria in the Middle Miocene Paratethyan assemblages showed the genus to be not only diverse, represented by 14 species, but also highly endemic, with all species restricted to the Paratethys (Euthria brunettii Harzhauser and Landau, Reference Harzhauser and Landau2024, E. walaszczyki Harzhauser and Landau, Reference Harzhauser and Landau2024, E. dellabellai Harzhauser and Landau, Reference Harzhauser and Landau2024, E. depressospira Bandat, Reference Bandat1943, E. diluvii [Eichwald, Reference Eichwald1830], E. fuscocingulata [Hoernes and Auinger, Reference Hoernes and Auinger1890], E. frausseni Harzhauser and Landau, Reference Harzhauser and Landau2024, E. obelixi Harzhauser and Landau, Reference Harzhauser and Landau2024, E. odiosa Harzhauser and Landau, Reference Harzhauser and Landau2024, E. puschii [Andrzejowski, Reference Andrzejowski1830], E. stuetzii [Naumann, Reference Naumann1852], E. subnodosa [Hoernes and Auinger, Reference Hoernes and Auinger1890], E. viciani Kovács, Reference Kovács2018, and E. zboroviensis Friedberg, Reference Friedberg and i Lódkonogi1912). In the same work, Harzhauser and Landau (Reference Harzhauser and Landau2024) realized that the specimens from the Serravallian Middle Miocene Karaman Basin of Turkey assigned to Euthria curvirostris (de Grateloup, Reference de Grateloup1845) by Landau et al. (Reference Landau, Harzhauser, İslamoğlu and da Silva2013) did not represent that species, but a new endemic one described as E. yesimae Harzhauser and Landau, Reference Harzhauser and Landau2024.

A study of the genus from the westernmost Mediterranean lower Piacenzian Upper Pliocene Estepona Basin assemblages of southern Spain (Landau and Harzhauser, Reference Landau and Harzhauser2024) resulted in similar findings; the genus was diversified and highly endemic, represented by five species (Euthria iberoadunca Landau and Harzhauser, Reference Landau and Harzhauser2024, E. inflatissima Landau and Harzhauser, Reference Landau and Harzhauser2024, E. pliovirginea Landau and Harzhauser, Reference Landau and Harzhauser2024, E. pouweri Landau and Harzhauser, Reference Landau and Harzhauser2024, and one left in open nomenclature). In that paper, the authors also realized that the specimens from the Lower Pliocene Atlantic Guadalquivir Basin of southwestern Spain reported under the name Euthriofusus cf. E. virgineus (de Grateloup, Reference Deshayes1832 [sic]) by Landau et al. (Reference Landau, da Silva and Mayoral2011) do not correspond to Euthria virginea (de Grateloup, Reference de Grateloup1833). Instead, they represent another endemic: Euthria onubensis Landau and Harzhauser, Reference Landau and Harzhauser2024. Similarly, those identified as E. cornea (Linnaeus, Reference Linnaeus1758) also represent an endemic species, E. lucenica Landau and Harzhauser, Reference Landau and Harzhauser2024.

Molluscan endemicity in the Pliocene of Western Iberia

Thus, for each revisited Neogene basin, an endemic assemblage of Euthria species emerged. This prompted the authors to re-evaluate material from the Upper Pliocene (lower Piacenzian) Mondego Basin of Portugal, with an emphasis on the Vale de Freixo fossil assemblage. Unfortunately, gastropod fossils with larger shells are scarce in these deposits. Nonetheless, two Euthria species are represented. Due to the scarcity of material, only one well-preserved specimen of each is so far known, but considering the genus’s morphological traits and biogeographical context discussed earlier, their formal description is crucial as it addresses a gap in knowledge concerning its biodiversity along the Pliocene European Atlantic frontage. The Mondego fossil assemblage is the only Pliocene record known along the European Atlantic coast between the Ligerian Basin in northwestern France (Landau et al., Reference Landau, da Silva, Van Dingenen and Ceulemans2020) and the Guadalquivir Basin of southwestern Spain (Landau et al., Reference Landau, da Silva and Mayoral2011), being paramount for testing the emerging scenario of a diverse yet highly endemic gastropod group in Neogene Atlanto-Mediterranean faunas.

Until recently, few endemic mollusks have been recognized from the Pliocene of the Mondego Basin. In the past century, a handful of new species were described from the localities of Mina, São Pedro de Moel, and Matos, Marinha Grande region by Cox (Reference Cox1936, Reference Cox1941). However, in recent years the revision of various groups has led to the description of new taxa, suggesting that about 12% of the gastropod species are endemic to the Mondego Basin Pliocene and 25% of the Polyplacophora (Table 2).

Table 2.

Molluscan species described as new and known only from the Pliocene of the Mondego Basin fossil assemblages of west-central Portugal, endemics.

¹ Considered subjective junior synonym of T. turrita (Borson, Reference Borson1820) by Landau et al. (Reference Landau, da Silva and Gili2009).

² Considered subjective junior synonym of Amalda elongata (Deshayes, Reference Deshayes1830) by Landau and da Silva (Reference Landau and da Silva2006).