The oldest platylepadid turtle barnacle (Cirripedia, Coronuloidea): a new species of Platylepas from the Lower Pleistocene of Italy

Coronuloid barnacles are epibionts of several marine vertebrates (including cetaceans and sea turtles) as well as invertebrates, and are assigned to two families of turtle barnacles (Chelonibiidae Pilsbry, 1916 and Platylepadidae Newman & Ross, 1976) and one family of whale barnacles (Coronulidae Leach, 1817). Chelonibiids and coronulids have a scanty, albeit signifi cant fossil record extending back to the Eocene and Pliocene, respectively; in turn, the fossil record of platylepadids is limited to a single record from the Upper Pleistocene. Here we report on an isolated carinolateral compartment of Platylepas Gray, 1825, the type genus of the family, from Lower Pleistocene (Gelasian) epibathyal deposits exposed at Milazzo (Sicily, Italy). This specimen is here designated holotype of a new species, †Platylepas mediterranea sp. nov. We argue that, like most extant members of Platylepas, †P. mediterranea sp. nov. lived partially embedded in the skin of a sea turtle. This record of an extinct platylepadid – the fi rst from the Mediterranean region and the second worldwide – pushes back the fossil record of Platylepadidae to the lowermost Quaternary, thus possibly supporting an even earlier (e.g., European Journal of Taxonomy 516: 1–17 ISSN 2118-9773 https://doi.org/10.5852/ejt.2019.516 www.europeanjournaloftaxonomy.eu 2019 · Collareta A. et al. This work is licensed under a Creative Commons Attribution License (CC BY 4.0). R e s e a r c h a r t i c l e urn:lsid:zoobank.org:pub:F1771E0A-0C42-41C9-AD57-2ADD58AF7E29


Introduction
Extant turtle and whale barnacles (Cirripedia Burmeister, 1834, Thoracica Darwin, 1854, Coronuloidea Leach, 1817) are epibiotic organisms that attach themselves to the external surface of several saltwater and estuarine vertebrates (including toothed and baleen whales, sea turtles, sea cows, crocodiles, snakes and bony fish) and invertebrates (including crabs, horseshoe crabs and crayfish) (Hayashi 2013, and references therein).By living on mobile host substrates, these sessile filter-feeding crustaceans can exploit a continuous flow of water laden with nutrient particles while at the same time lowering the risk of predation (Seilacher 2005).Currently, coronuloid barnacles are assigned to three families, namely Coronulidae, Chelonibiidae and Platylepadidae (Ross & Frick 2011).Whereas coronulids are obligate phoronts of cetaceans (hence their vernacular name, whale barnacles), chelonibiids and platylepadids (collectively known as turtle barnacles) exhibit more generalist host habits, although most species live preferentially or exclusively on the skin, carapace or plastron of sea turtles.The fossil history of Chelonibiidae dates back to the Paleogene (with the earliest representative of the family, †Emersonius cybosyrinx Ross in Ross & Newman, 1967, from the upper Eocene Williston Limestone of Florida, USA), whereas coronulids seemingly appeared later, starting with †Coronula bifida Bronn, 1831 in a few Upper Pliocene deposits worldwide (e.g., Marquet et al. 2009).In turn, the fossil record of Platylepadidae, a widely distributed and well-diversified family of small-sized, warm-water coronuloids, with at least fourteen extant species in six genera (Ross & Frick 2011), is much less extensive and, in fact, comprises merely the holotype of †Platylepas wilsoni Ross, 1963 from the Upper Pleistocene Pamlico Formation of Florida, USA.
In the present paper we report on the presence of a member of Platylepas Gray, 1825, the type genus of the family, in Lower Pleistocene marine deposits of the central Mediterranean Basin.The single specimen known is a right carinolateral compartment; it is here designated holotype of a new species and its paleontological significance is briefly discussed.

Diagnosis
As for the subfamily, until new genera are referred here.

Range and distribution
Early Pleistocene (Gelasian) to Recent.Recorded as fossil from the Lower Pleistocene (Gelasian) of Sicily, southwest Italy (present paper) and the Upper Pleistocene of Florida, southeastern USA ( †P. wilsoni).Currently known as an epizoic phoront found on several marine vertebrates (such as turtles, sea snakes, sirenians and fish) occurring in tropical and warm-temperate seas (between ca 45° N and ca 45° S latitude).†Platylepas mediterranea sp.nov.

Diagnosis
Wall truncated conical; bi-lamellar; transverse growth lines forming principal sculpture of outer face of compartments; longitudinal septa and canals visible through outer wall, becoming more numerous peripherally; carinolatus three-lobed; sheath extending for less than half of total height of compartment, appressed, not hollowed out from behind, exhibiting distinct transverse grooves; accessory ribs present, corresponding to distinct sulci on outer face of compartments; inner face of compartments smooth, devoid of ridges or septa; radii narrow, sub-straight, and relatively robust; alae thin; inter-compartmental ornamentation absent.

Etymology
From Mare Mediterraneum, the Latin name of the Mediterranean Sea, in allusion to the region where the holotype was found.

Description
MSNC 4562 is an isolated, ca 7 mm tall, near-complete right carinolateral compartment (CL1 or CL2), the external surface of which has been moderately decorticated by wear (Fig. 2a).For this reason, we describe it here starting from the better-preserved and more informative internal surface (Fig. 2b).
When viewed internally, MSNC 4562 exhibits a rather short sheath, extending for less than half of the total height of the compartment (Fig. 2b).The sheath is strongly appressed, i.e., it runs subparallel to the external face of the compartment; its median portion bears a low and broad longitudinal ridge which corresponds to the location of the upper part of the midrib prop (see below).The sheath exhibits a few distinct plicae (here interpreted as growth lines) that extend subparallel to the gently curved (i.e., slightly S-shaped) basal margin of the sheath (Figs 2b,3a).The fossa for the accommodation of the ala COLLARETA A. et al., A new Pleistocene species of Platylepas from Italy (hereinafter referred to as the alar depression) is shallow and its margin is rounded and roughly J-shaped.A few very weak, transversely oriented grooves are observed also within the alar depression.The sheath is massive and not hollowed out from behind.However, a very shallow depression is seen beneath the basal margin of the sheath on the radial side of the midrib prop; conversely, at the alar side of the midrib prop the sheath is solidly filled from behind, and its basal margin is just marked by a horizontal ridge forming a sort of "step" on the inner surface of the compartment (Figs 2b,3a).Below the sheath, the inner surface of the compartment is strongly folded inwards, thus generating a prominent longitudinal midrib prop 3a).This hook-like structure distinctly projects inwards and downwards; it is not filled internally.The transverse section of the midrib prop is roughly drop-shaped (Fig. 3f).The midrib prop runs closer to the alar margin of the compartment than to its radial margin.Therefore, it divides the inner surface of the compartment below the sheath into two areas: the smaller one is distinctly concave and roughly shaped as a longitudinally-elongated semi-cylinder; the larger one is laterally bounded by the sutural edge of the radius (Fig. 2b, f), with a broad accessory fold parallel to the midrib prop.This accessory fold is directed downwards and starts a couple of millimeters below the basal margin of the sheath (Figs 2b,3a).No longitudinal septa occur below the sheath, either close to its base or at the periphery (i.e., close to the preserved portions of the basal margin of the compartment), as this portion of the inner surface is substantially smooth.
On the external surface of the compartment, the midrib prop and the accessory fold correspond to two shallow, yet obvious sulci which distinguish three longitudinally-elongated lobes (Fig. 2a).Although MSNC 4562 is moderately eroded externally, its trilobate aspect is well recognized from the apex of the compartment downwards (Fig. 2e).The external surface of the compartment is ornamented by longitudinal septa, which define longitudinally elongated tubes or canals between them.MSNC 4562 European Journal of Taxonomy 516: 1-17 ( 2019) is therefore tubiferous and bi-lamellar, the outer lamina being produced by the distal coalescence of the septa that extend from the inner wall.However, due to overall abrasion of the terminal T-shaped flanges of the longitudinal septa, a pristine outer wall is only locally preserved (Fig. 3b).Some septa bifurcate downwards so that the interseptal distance remains roughly constant along the whole height of the compartment.This septate sculpture is affected by prominent transverse growth ridges along which the external surface of the compartment widens distinctly (Fig. 2a, c-d).The intersection of the longitudinally elongated septa and the transversely oriented growth ridges is occasionally marked by small knobs on what remains of the outer lamina (Figs 2a, 3b).
The radius is rather narrow and partially preserved.In radial view, it is sub-straight (Fig. 2d) and its basal termination weakly projects inwards.The sutural edge of the radius is relatively robust.The denticulation pattern of the sutural edge is largely eroded; where it is preserved, it appears simple, being in fact comprised of squat, blunt, transversely-oriented septa that originate from the inner margin of the radius and project outwards (Fig. 2d).The ala is thin and distally tapers moderately.The sutural edge of the alar portion of the compartment exhibits short, triangular, wedge-like complementary septa which project inwards from a main septum running along the outer margin of the compartment (Figs 2c, 3a).Therefore, judging from the architecture of the radial and alar sutural margins, the space between two adjacent compartments would have been completely filled.

Comparisons and remarks
MSNC 4562 unambiguously belongs to the monotypical subfamily Platylepadinae based on the presence of a large and prominent midrib prop -observable on the inner surface of the compartment -which corresponds to a distinct sulcus on the external surface of the shell.The general morphology of MSNC 4562 strongly suggests a truncated conical (i.e., volcano-like) rather than peltate shell.Based on its size, a truncated conical shell that measured ca 14 mm in carinorostral diameter could be reconstructed; a slightly larger size estimate (ca 17 mm) could be proposed if the shell were more depressed.These size estimates are largely consistent with measurements of mature specimens of extant P. hexastylos.
On the whole, MSNC 4562 is reminiscent of the extant species P. hexastylos in various aspects of the shell: the structure of the sutural margins of MSNC 4562, for instance, is rather close to that of P. hexastylos.In addition, the outer aspect of MSNC 4562 is similar to that of a specimen of P. hexastylos from Sicily as illustrated by Pilsbry (1916: pl. 67, fig. 4) and to that of numerous other truncated conical individuals of P. hexastylos in which the outer lamina is partially or mostly worn out, thus revealing the septate, bi-lamellar nature of the compartment wall (e.g., Darwin 1854; Pilsbry 1916;Monroe & Limpus 1916;A.C., pers. obs.).However, various characters preserved in MSNC 4562 distinguish this fossil from the extant P. hexastylos.First, whereas in P. hexastylos the shell is very light and thin, MSNC 4562 appears to have been slightly more robust.Secondly, whereas in P. hexastylos the sheath is generally smooth and only occasionally displays weak growth lines, that in MSNC 4562 exhibits evident transverse grooves.Thirdly, in P. hexastylos the sheath is hollowed out from behind, but that in MSNC 4562 is appressed and filled from behind.Fourthly, P. hexastylos bears septa that extend onto the internal surface of each plate up to the level of the basal margin of the sheath or even terminate within the hollowed out portion behind the sheath; in turn, the internal surface of MSNC 4562 is devoid of septa and substantially smooth.Fifthly, whereas compartments of P. hexastylos appear as typically bilobate externally, the external aspect of MSNC 4562 is trilobate -a character that reflects the presence of an accessory rib on the inner surface of the compartment.Although compartments belonging to adult individuals of P. hexastylos occasionally exhibit an accessory rib and an incipient third lobe developing near the base of the shell, the trilobate nature of the external surface of MSNC 4562 is recognizable even close to the orifice, thus suggesting that it represents a structural character rather than an incidental feature incurred during growth.This hypothesis could find some support in the above-mentioned observation that the inner face of MSNC 4562 is smooth and devoid of those ridges and septa which in extant P. hexastylos aid in both fixing the phoront crustacean to its substrate and preventing the collapse of the thin barnacle shell (e.g., Ross & Newman 1967).In this respect, the accessory rib observed in MSNC 4562 could be interpreted as a functional substitute of the fimbriated periphery of the compartments of P. hexastylos, substantially contributing to the stabilization of the relatively robust platylepadid shell to which MSNC 4562 belonged by providing firm anchorage to the underlying host tissue.If this interpretation is correct, a complete adult shell of the platylepadid species from Cala S. Antonino might have displayed up to 18 lobes on its external surface (e.g., three lobes on each CL, four on R, and two on C).
The extant species Platylepas coriacea, P. indicus and P. ophiophila are similar to P. hexastylos in shell shape and structure.MSNC 4562 further differs from P. coriacea by its narrower radius, longer sheath, and the trapezoidal (rather than near-triangular) outline of the paries.It differs from P. indicus, in which both sides of the midrib prop of each compartment bear a distinct ridge, and from P. ophiophila by not displaying three or more secondary ribs lateral to the midrib prop.
MSNC 4562 resembles P. decorata as its sheath is not hollowed out from behind and in lacking longitudinal septa on the inner surface of the compartment.However, MSNC 4562 differs markedly from P. decorata European Journal of Taxonomy 516: 1-17 ( 2019) by exhibiting a thinner wall, a distinctly shorter sheath, sutural edges of the compartment that lack external ornamentation, and a different aspect of the outer wall (e.g., the shell of P. decorata is monolamellar, each compartment being externally ornamented by fine longitudinal columns).Moreover, the shell of P. decorata is more or less cylindrical -a feature different from MSNC 4562, which would best match a truncated conical shell morphology.
MSNC 4562 also resembles †P.wilsoni in exhibiting transverse grooves on the sheath and a basal inner margin of the compartment without septa.However, MSNC 4562 clearly differs from this Late Pleistocene species by having a P. hexastylos-like radius (rather than a hollow tube) and by a clearly different ornamentation of the external surface of the shell (e.g., the outer wall of †P.wilsoni has a shingled appearance).
In conclusion, MSNC 4562 looks both structurally and morphologically more similar to the type species of the genus Platylepas (i.e., P. hexastylos) than to other congeners known to date (e.g., P. decorata).At the same time, MSNC 4562 significantly differs from all the species of Platylepas known to date, thus warranting the erection of a new species - †P. mediterranea sp.nov.
What kind of living substrate did the type specimen of †P.mediterranea sp.nov.attach to?So far, the verified hosts of extant Platylepas spp.include all living genera of sea turtles and sea cows, as well as several forms of sea snakes and a single genus of holostean fish, i.e., the North American gar, Lepisosteus COLLARETA A. et al., A new Pleistocene species of Platylepas from Italy Lacépède, 1803(e.g., Darwin 1854;Lanchester 1902;Krüger 1912;Pilsbry 1916;Nilsson-Cantell 1938;Daniel 1958;Stubbings 1965;Utinomi 1970;Zann 1975;Zann & Harker 1978;Monroe & Limpus 1979;Young 1991;Hernández-Vázquez & Valadez-González 1998;Jones 2004Jones , 2010;;Hayashi et al. 2011;Lazo-Wasem et al. 2011;Hayashi 2012).Lepisosteid gars and sea snakes have never been recorded from the Mediterranean region, either as living individuals or as fossil remains from Cenozoic strata.Sirenians are also absent from the present-day Mediterraean Sea; however, tens of fossil specimens are known from Paleogene and Neogene deposits, predating the latest Pliocene (ca 3 Ma; Sorbi et al. 2012).Having observed this, and also considering that the Italian Plio-Pleistocene record of sea turtles includes several fragmentary indeterminate cheloniids (Chesi & Delfino 2006), we argue that MSNC 4562 might have been attached to a sea turtle.If this line of reasoning is correct, †P.mediterranea sp.nov.could be added to the list of chelonophilic barnacles, to which most extant representatives of the genus Platylepas belong.As noted above, the external aspect of MSNC 4562 strongly recalls that of a specimen of P. hexastylos from Sicily illustrated by Pilsbry (1916: pl. 67, fig. 4).This specimen was briefly characterized by Pilsbry (1916: 287) as follows: "It has steep, convex sides, deep median clefts in the compartments, but the internal midribs are slender and project but little […] The septa are very numerous, sharp, and close […] From the appearance of this barnacle I suspect that it did not live on the shell of a turtle.There is some orange-coloured skin adhering in the furrows of the lower part of the parietes".Interestingly, the description and illustration of that particular specimen provided by Pilsbry (1916), inclusive of the presence of orange-colored shreds of the embedding tissue of its host, perfectly match the aspect of several truncated conical extant specimens of P. hexastylos recovered by one of us (G.I.) and partially embedded in the skin of a loggerhead turtle, i.e., Caretta caretta (Linnaeus, 1758), beached along the coast of Donnalucata (Ragusa, Sicily, Italy) on 25 July 2000.Personal observations by two of us (A.C. and G.I.) on platylepadid phoronts associated with this chelonian individual suggest that truncated conical individuals of P. hexastylos were preferentially found partially embedded in the skin of the turtle, whereas their peltate conspecifics might have been commoner on the carapace and plastron.More generally, within the genus Platylepas, depressed shell morphologies appear to prevail among those forms that tend to adhere superficially to a host (as observed for the typically peltate P. coriacea; see, e.g., Monroe & Limpus 1979), whereas less flattened (up to cylindrical) shell shapes characterize those that manage to become anchored within a soft substrate (as observed for the typically ring-like P. decorata; see, e.g., Zardus & Balasz 2007).Therefore, we suggest that MSNC 4562 lived partially embedded in the skin of a cheloniid sea turtle, as currently observed for many phenotypically similar individuals of P. hexastylos attaching to Caretta caretta in central Mediterranean waters.
Recent phylogenetic analyses (Hayashi et al. 2013;Pérez-Losada et al. 2014) agree in recognizing the genus Chelonibia as occupying a basal position within Coronuloidea, as had been proposed much earlier based simply on morphology (e.g., Foster 1979; Buckeridge 1983).Given the general lack of occurrences of fossil turtle barnacles other than chelonibiids prior to the Upper Pleistocene, some platylepadid genera have occasionally been regarded as Pleistocene or Recent offshoots of Coronulidae (Hayashi et al. 2013).However, morphological considerations discourage the acceptance of this hypothesis, suggesting instead that the extant genus Platylepas is a surviving member of an ancient group of generalist epizoic barnacles (Ross & Newman 1967).According to the divergence time analysis by Hayashi et al. (2013), Platylepas originated during the Early or Middle Miocene.Although no fossil specimen of Platylepas is known from sedimentary deposits from this time interval, Hayashi et al. (2013) argued that a trace of a Platylepas-like barnacle could be detected on the carapace of a fossil sea turtle, i.e., the type specimen of "Euclastes" melii Misuri, 1910, from Miocene strata of the 'Pietra Leccese' (Apulia, southern Italy).Hayashi et al. (2013) based their claim on an illustration provided by Misuri (1910) in the paper in which "E." melii was described.Unfortunately, the whereabouts of the type material is currently unknown; the trace-bearing specimen illustrated by Misuri (1910) may have been lost (Chesi et al. 2007).Therefore, a direct analysis of the trace fossil hinted at by Hayashi et al. (2013) cannot be carried out, leaving their inference unconfirmed at this time.However, our discovery of a new species of Platylepas that is European Journal of Taxonomy 516: 1-17 (2019) phenotypically close to extant P. hexastylos in deposits dated as Early Pleistocene may provide some support to a 'less shallow' evolutionary history for the epizoic barnacles currently grouped in the family Platylepadidae.Considering also the strongly biased nature of the fossil record of thin-walled, smallsized barnacles such as Platylepas spp., a Neogene origin of the platylepadid lineage would appear plausible.

Concluding remarks
As already evoked elsewhere (e.g., Seilacher 1992Seilacher , 2005;;Bianucci et al. 2006;Fertl 2009;Dominici et al. 2011;Hayashi et al. 2013;Pérez-Losada et al. 2014;Collareta et al. 2016aCollareta et al. , 2016bCollareta et al. , 2018a;;Buckeridge et al. 2018), the extant epibiotic organisms included in the superfamily Coronuloidea are regarded as the ultimate product of an outstanding path of co-evolution with their vertebrate hosts.Nevertheless, the fossil record of coronuloid barnacles is still fragmentary and partially unexplored.As a consequence, the Cenozoic steps of such a co-evolutionary path are only vaguely known and largely speculative.The fossil occurrence of Platylepas recorded in the present paper adds new data to previous studies by extending back the fossil history of Platylepadidae to the lowermost Quaternary, thus supporting an earlier (e.g., Neogene) timing for the origin of this family and substantially contributing to our views of the evolutionary history of one of the most diverse and successful lineages of epizoic crustaceans.Further additions to the fossil record of coronuloid barnacles will certainly assist in illustrating how the "evolutionary dream" (sensu Seilacher 1992Seilacher , 2005) ) of riding a whale or a sea turtle could have come true for an amazing lineage of tiny crustaceans.

Fig. 1 .
Fig. 1.Locality map, showing provenance (white star) of the holotype of the new platylepadid (MSNC 4562) described herein.All images from Google Earth.

Fig. 3 .
Fig. 3. †Platylepas mediterranea sp.nov., holotype (MSNC 4562).a. Interno-alar view.Note the strongly appressed sheath exhibiting distinct transverse grooves (arrows) and the short, triangular, wedge-like, transverse septa on the sutural edge of the alar portion of the compartment.b.Close-up of the outer surface of the compartment.The outer lamina is only locally preserved; where it is eroded, longitudinally elongated septa and canals are visible.The intersection between longitudinal septa and transverse growth ridges is occasionally marked by small knobs.