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Review focus Journal of the Geological Society Published Online First https://doi.org/10.1144/jgs2017-164

The Bolca Lagerstätten: shallow marine life in the Eocene

Matt Friedman1* & Giorgio Carnevale2 1 Museum of Paleontology and Department of Earth and Environmental Sciences, University of Michigan, 1109 Geddes Ave, Ann Arbor, MI 48109-1079, USA 2 Dipartimento di Scienze della Terra, Università degli Studi di Torino, via Valperga Caluso 35, 10125, Torino, Italy M.F., 0000-0002-0114-7384 * Correspondence: [email protected]

Abstract: The Eocene limestones around the Italian village of Bolca occur in a series of distinct localities providing a unique snapshot of marine life in the early Cenozoic. Famous for its fishes, the localities of Bolca also yield diverse invertebrate faunas and a rich, but relatively understudied flora. Most fossils from Bolca derive from the Pesciara and Monte Postale sites, which bear similar fossils but are characterized by slightly different taphonomic and environmental profiles. Although not precisely contemporaneous, the age of these principal localities is well constrained to a narrow interval within the Ypresian Stage, c. 50– 49 Ma. This places Bolca at a critical time in the evolutionary assembly of modern marine fish diversity and of reef communities more generally. Received 22 December 2017; revised 7 March 2018; accepted 8 March 2018

The rich fossil sites near Bolca, Italy provide a picture of life in a contains remains of crocodiles, turtles, snakes and plants. The warm, shallow marine setting during the early Eocene, roughly lignites of Vegroni yield a variety of plants. 50 myr ago. Deposited within an archipelago near the western end of the Tethys Ocean, the major localities of Bolca collectively have yielded over 500 species of terrestrial vertebrates, fishes, insects, Stratigraphy and age marine invertebrates and plants. The outstanding significance of the The Pesciara and Monte Postale successions are among the few Bolca Lagerstätten derives from a unique combination of age (near shallow-water Eocene sequences deposited on the Lessini Shelf the dawn of modern reef ecosystems), location (within an ancient (sensu Bosellini 1989), a palaeogeographical feature of the biodiversity hotspot) and taphonomy (exceptional preservation). Southern Alps that was uplifted during the Alpine orogeny. Upon Here we provide an overview of these sites, discussing history, reaching the photic zone during the early Eocene, the Lessini Shelf geology, fossils and significance. acted as a centre of deposition of shallow-water carbonates (Doglioni & Bosellini 1987; Bosellini 1989; Luciani 1989). Eruptive products of extensive magmatic activity accumulated between the late Geological context Paleocene and the middle Eocene (e.g. Macera et al. 2008). Localities Beginning in the early Eocene, these volcanic and volcanoclastic deposits became intercalated with marls and limestones. The village of Bolca lies on the eastern part of Monti Lessini not far Widespread regional faulting and cross-cutting volcanic units from Verona, northern Italy. Monti Lessini represents a southern hinder stratigraphic studies of the Eocene succession of the Bolca prolongation of the Southern Alps (Carminati et al. 2012). Several area. Consequently, the Eocene carbonates of the Lessini Shelf have productive sites characterized by contrasting fossils are known from been collectively assigned to the ‘Calcari Nummulitici’, an informal the Bolca region (Papazzoni et al. 2014; Fig. 1), and are collectively unit poorly constrained in terms of age and depositional setting. known as ‘Monte Bolca’ in older literature although no such place Pesciara consists of a limestone block surrounded by volcanic exists. We refer to this geographically compact collection of deposits (Fig. 1b). The outcrop is less than 20 m thick, covering an environmentally and stratigraphically distinctive localities as the area of a few hundred square metres, and consists of a rhythmic Bolca Lagerstätten, drawing distinctions between the various sites. alternation of finely laminated micritic limestone with fishes and The most famous representative is Pesciara, which has been plants and grainstone bearing benthic fossils (Papazzoni & exploited since the mid-16th century (Box 1) and yields exquisitely Trevisani 2006). Nearly all the fishes, soft-bodied invertebrates preserved marine fishes, plants and soft-bodied invertebrates. It is and plants collected from Pesciara are from five bands of grey, joined by Monte Postale, located nearby and also famous for marine laminated micritic limestone. The succession of Monte Postale fishes and plants. These two localities are the source of most fossils consists of more than 130 m of grainstone that alternates with from the Bolca area in museums, and have yielded over 100 000 massive coralgal limestone and laminated wackestone with fishes exceptionally preserved fossils (e.g. Blot 1969; Box 1). This review and plants similar to those of Pesciara (e.g. Vescogni et al. 2016; focuses on these two localities. Papazzoni et al. 2017). The laminated limestone varies in thickness There are two additional nearby localities included among the depending on position in the succession. However, most layers are Bolca Lagerstätten: Purga di Bolca and Vegroni. These freshwater about 1 m thick, very similar to those of Pesciara. and brackish deposits are classically considered younger than Both the Pesciara and Monte Postale successions were deposited Pesciara and Monte Postale, but their stratigraphic correlation with in the early late Ypresian. Calcareous nannofossils and larger the more famous horizons is problematic (Papazzoni et al. 2014). benthic Foraminifera indicate that the Pesciara succession corre- Purga di Bolca consists of lignites around a volcanic neck, and sponds to the upper part of that of Monte Postale. Monte Postale

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M. Friedman & G. Carnevale

Fig. 1. Location and geology of Pesciaria and Monte Postale, the principal Lagerstätten of Bolca. (a) Location of Bolca in Italy. (b) Topographic map of region immediately NW of the village of Bolca. Colours indicate different geological units: yellow, Spilecco Limestone; green, laminated and bedded limestone; blue, massive limestone; orange, volcanic rocks. Intensity of shading indicates either rock exposed in outcrop (dark) or inferred (light). Adapted from Trevisani (2015). spans the entire NP 13 and CNE 5 calcareous nannoplankton zones are rare, with palms represented only by fruits (complete palms are (Papazzoni et al. 2017), corresponding to a large part of the Shallow found at Vegroni; Giusberti et al. 2014a). Leaves and leaflets, Benthic Zone (SBZ) 11 in the time interval between c. 50.5 and especially of legumes, are the most common remains of dicots, but 48.96 Ma (see Agnini et al. 2014). This corresponds to the early twigs, fruits and flowers are also known. Specimens of whole plants Eocene climatic optimum (EECO in the sense of Luciani et al. are known, but some of these are regarded as restorations or 2016). Pesciara has been assigned to the uppermost part of SBZ 11, composites (Wilde et al. 2014). In addition to these remains, corresponding to the basal portion of NP 14 and CNE 6, between Pesciara also yields amber (Trevisani et al. 2005). As in the 48.96 and c. 48.5 Ma. macroflora, angiosperms dominate the microflora, with rare gymnosperm pollen and fern spores (Kedves & Zsivin 1970). In drawing comparisons with approximately coeval fossil floras Floral and faunal composition (e.g. lacustrine deposits of Messel), Wilde et al. (2014) noted lower Study of different components of the Bolca fossil assemblages is diversity in the Pesciara–Monte Postale macroflora combined with a uneven. The fishes of Pesciara and Monte Postale have been the distinctive composition in terms of both taxa and organs. They subject of nearly continuous investigation for centuries. The so- attributed these features to a taphonomic filter arising from fluvial called ‘minor fauna’, comprising non-fishes, of Pesciara and Monte transport to the ocean and subsequent shallow marine wave action, Postale are poorly known by comparison (Carnevale et al. 2014; and also acknowledged the potentially important role of storms in Giusberti et al. 2014b). Similarly, relatively little work has built transporting some plant remains. upon foundational palaeobotanical studies from the 19th century (Wilde et al. 2014). Invertebrates Plants Jellyfishes and corals Marine plants and macroalgae Medusae from Pesciara comprise complete specimens preserving delicate features (Giusberti et al. 2014b; Fig. 2d). Corals are a Floating or fully marine monocots such as seagrasses are the most common component of the benthic fauna, represented by broken common elements of the Pesciara–Monte Postale flora (Wilde et al. material in the coarse-grained carbonates intercalated between the 2014; Fig. 2a). Brown and red algae are represented by macrofossils laminites and in the fossiliferous laminated wackestone of Monte and biomarkers (Schwark et al. 2009). Postale (Tang 2002; Marramà et al. 2016a; Fig. 1b and c).

Terrestrial plants Ferns are absent, and gymnosperms are limited to long, needle-like Annelids leaves. The terrestrial flora of Pesciara–Monte Postale is dominated Annelids from Bolca include four species of polychaete placed in by angiosperms, specifically dicots (Fig. 2b). Terrestrial monocots two genera, and a single species of leech (Giusberti et al. 2014b). Downloaded from http://jgs.lyellcollection.org/ by guest on September 30, 2021

The Eocene Bolca Lagerstätten

Box 1. History of collecting at Bolca The first documented report of a fossil from the Bolca Lagerstätten dates to the 16th century, and notes material belonging to the ambassador of the Holy Roman Empire to the Venetian Republic (Mattioli 1550). Nearly a century later, the first illustration of a fossil from Bolca appeared in a catalogue of the collection of a Veronese apothecary (Ceruti & Chiocco 1622; Fig. 2a). Bolca fossils and their origin were extensively debated during the 18th century. It is also at this time that large collections were amassed by noblemen in Verona, including Vincenzo Bozza, Ottavio Canossa and Giovanni Battista Gazola (Fig. 2b). By the end of 1791, Gazola’s own museum contained over a thousand well- preserved fossil fishes, plus numerous plants and invertebrates. The abbot Giovanni Serafino Volta studied the Bozza collection and assigned most of the fishes to modern tropical species in his lavishly illustrated catalogue (Volta 1796–1809). The revolutionary armies of Napoleon confiscated about 600 fossils from the Gazola collection during the occupation of Verona in 1797. Subsequently transported to Paris, these specimens were studied by de Blainville (1818) for an account in Nouveau Dictionnaire d’Histoire naturelle, and later by Louis Agassiz, who reviewed Volta’s identifications (Agassiz 1835) and provided further descriptions in his monumental Recherches sur les Poissons fossiles (Agassiz 1833–1844). The first detailed analysis of the fossil plants from Bolca was provided by Abramo Bartolomeo Massalongo in a series of monographic studies (e.g. Massalongo 1850, 1851, 1859) and further improved and expanded by Meschinelli & Squinabol (1892). The most extensive collections of fossils from the Bolca Lagerstätten remain in Italy, particularly in Verona and Padua. Large collections outside Italy, such as those in Paris, have interesting histories. Fossils at the Naturhistorisches Museum, Vienna, were presented by Massalongo to Emperor Franz Joseph I following an assassination attempt in 1853; material at the Natural History Museum, London, derives largely from the purchased collections of William Willoughby Cole, 3rd Earl of Enniskillen, and Sir Philip de Malpas Grey Egerton in the late 1800s; Bolca specimens at the Carnegie Museum of Natural History, Pittsburgh, were acquired in 1903 from the Belgian Baron de Bayet, executive secretary to King Leopold II. Fossils from Pesciara–Monte Postale are otherwise found in numerous smaller collections throughout the world, often tracing their origins to early ‘cabinets of curiosities’.

Fig. 2. Historical aspects of palaeontology of the Bolca localities. (a) The first fossil fish to be figured from Bolca, the squirrelfish Berybolcensis leptacanthus, MCSNV T.177 (top), with historical illustration from Ceruti & Chiocco (1622) (bottom). (b) One of two galleries dedicated to the display of fossil fishes from Bolca in the museum of Giovanni Battista Gazola.

Arthropods Fishes Pesciara and Monte Postale yield a diversity of terrestrial and marine Beginning with the first major accounts by Volta (1789, 1796– arthropods (Fig. 3c and e). Insects include thysanuruans, odonatans, 1809), the fish fauna of Pesciara and Monte Postale has been the trichopterans, coleopterans, orthopterans, heteropterans, hymenop- subject of numerous broad overviews (Blot 1980; Bannikov 2014; terans and dipterans, with the last group being the most common Carnevale et al. 2014). (Giusberti et al. 2014b). Other terrestrial arthropods include a scorpion and possible pseudoscorpion. Marine crustaceans domin- ate the minor fauna, and include three isopod genera, two Sharks and rays stomatopod genera and 12 decapod genera (Giusberti et al. 2014b). Chondrichthyans are rare and little studied relative to the more famous ray-finned fishes, comprising fewer than 20 species Molluscs (Carnevale et al. 2014; Marramà et al. 2017a,b; Fig. 4a). Nevertheless, the Pesciara–Monte Postale fauna is the most Bivalves and gastropods are abundant in the coarse limestones diverse assemblage of articulated chondrichthyans known from between laminites, but are uncommon within the laminites the Cenozoic. Batoids are represented by rhinobatids, narcinids, themselves. However, six bivalve genera and some undescribed platyrhinids, dasyatids, myliobatids and urolophids. Sharks include forms, plus two gastropod genera, are reported from the laminites. carchariniforms and a lamniform known only from teeth. Rare cephalopods include decapodiform coleoids and a nautiloid Chimaeroids are represented by a single isolated fin-spine (Giusberti et al. 2014b). belonging to the genus Ischyodus (Marramà et al. 2017a). Extensive soft-tissue preservation in sharks visualized using Lophophorates ultraviolet light (Fanti et al. 2016) indicates potential for Lophophorates are limited to six terebratulid specimens and a single substantially more anatomical detail than available in historical bryozoan from Pesciara (Giusberti et al. 2014b). accounts (Fig. 5). Downloaded from http://jgs.lyellcollection.org/ by guest on September 30, 2021

M. Friedman & G. Carnevale

Fig. 3. Plants and invertebrates from the Bolca Lagerstätten. (a) Seagrass similar to Phyllospadix or Posidonia, Museo Civico di Storia Naturale, Verona (MCSNV) fB47. (b) Leaf generally assigned to the mallow Sterculia, MGP-PD (Museo di Geologia e Paleontologia, Università degli Studi di Padova) 20V. (c) The spiny lobster Justinia desmaresti, MCSNV 23. (d) The medusa Simplicibranchia bolcensis, MCSNV m.B.2. (e) Hymenopteran insect, MCSNV i.c.2NS. Scale bars represent 50 mm, with the exception of (e), where the scale bar represents 5 mm. Photographs courtesy of: plants, G. Roghi (Istituto di Geoscienze e Georisorse, CNR, Padova); invertebrates, R. Zorzin (MCSNV).

Non-acanthomorph ray-finned fishes pleuronectiforms (flatfishes), siganids (rabbitfishes), scatophagids Roughly 30 species constitute the non-acanthomorph ray-finned (scatties), priacanthids (bigeyes), sparids (porgies), lutjanids fishes of Pesciara–Monte Postale. These include late-surviving (snappers) and pomacentrids (damselfishes). Joining these taxa pycnodonts, deep-bodied neopterygians abundant during the are groups associated with more open-water habitats, including Mesozoic (Blot 1987; Fig. 4b). Other Mesozoic elements include beloniforms (halfbeaks and flying fishes), scombrids (tunas and Platinx, the last known member of Crossognathiformes, an early mackerels), xiphioids (billfishes) and palaeorhynchids (an extinct diverging teleost clade (Arratia & Tischlinger 2010; Sferco et al. billfish group), as well as several groups of uncertain relationships 2015). No fewer than nine families of eels represent Elopomorpha to modern lineages (e.g. exelliids). (Blot 1978), and are joined by three osteoglossomorph species. The latter are noteworthy as extant examples are freshwater, Terrestrial vertebrates although several taxa are known from marine deposits in the Paleogene (e.g. Bonde 2008). The most common fish specimens Reptiles found in the Bolca Lagerstätten (Landini & Sorbini 1996, table 1), A turtle and two genera of boid snakes are known from Pesciara clupeomorphs have only recently been studied in detail (e.g. (Carnevale et al. 2014). Reptiles are more common at Purga di Marramà & Carnevale 2015a,b, 2016; Fig. 4c). Ostariophysans, a Bolca, and include crocodiles in need of taxonomic revision, a dominant group of primarily freshwater fishes, include the snake and two genera of freshwater turtles (Giusberti et al. 2014a). anatomically primitive Chanoides (Patterson 1984). No ‘prota- ’ canthopterygians , stomiiforms (dragonfishes) or myctophiforms Birds (lanternfishes) are known, and aulopiforms (lizardfishes and kin) Birds are limited to isolated feathers from Pesciara. Whereabouts of are represented by a single species (Marramà & Carnevale 2017; skeletal remains reported in historical accounts are unknown Fig. 4d). (Carnevale et al. 2014). Acanthomorphs Taphonomy Taxonomically, the ichthyofauna is dominated by spiny-rayed teleosts, or acanthomorphs (Fig. 4e–l). Non-percomorphs from Fossils from Pesciara–Monte Postale, particularly the fishes, are Bolca include lampridiforms, a zeiform and holocentroids usually found as part and counterpart with complete squamation, (Carnevale et al. 2014; Davesne et al. 2017). Percomorphs traces of pigmentation and phosphatized soft tissues (e.g. Wilby & make up the vast majority of fish species from the Bolca Briggs 1997; Fig. 5). Controlled excavations carried out in Pesciara Lagerstätten, and include familiar inhabitants of modern reefs: and Monte Postale show that preservation and abundance of fossils apogonids (cardinalfishes), acanthurids (surgeonfishes), caran- differ between the two sites as a consequence of contrasting gids ( jacks), syngnathiforms (pipefishes and allies), labrids depositional environments (Marramà et al. 2016a). (wrasses), tetraodontiforms (pufferfishes and allies), ephippids Exceptionally preserved fossils are abundant in the finely (spadefishes), sphyraenids (barracudas), lophiiforms (anglerfishes), laminated micritic limestone of Pesciara, where they constitute the Downloaded from http://jgs.lyellcollection.org/ by guest on September 30, 2021

The Eocene Bolca Lagerstätten

Fig. 4. Fishes from the Bolca Lagerstätten. (a) The numbfish Titanonarke molini, Museo Civico di Storia Naturale, Verona (MCSNV) IG.VR.67290; (b) the pycnodont Nursallia veronae, MCSNV II.D.173; (c) the round herring Trollichthys bolcensis, Natural History Museum, London (NHMUK) PV OR 37227; (d) the barracudina Holosteus esocinus, Museum national d’Histoire naturelle, Paris (MNHN) BOL 175; (e) the surgeonfish Eorandallius elegans, MCSNV VIII.C.58; (f) the moonfish Mene oblonga, Naturhistorisches Museum, Vienna (NHMW) 1853.XXVII.28; (g) the perch-like fish of unclear affinities Ceratoichthys pinnatiformis, MCSNV T.950; (h) the cornetfish Urosphen dubia, NHMUK PV P 15638; (i) the batfish Eoplatax papilio, MCSNV I.G. 24573; ( j) the mackerel Godsilia lanceolata, MCSNV T.89; (k) the monkfish Caruso brachysomus, MNHN BOL 42; (l) the triggerfish relative Protobalistum imperiale, MCSNV T.21. Scale bars represent 50 mm. vast majority of the collected specimens. The current taphonomic blooms might represent one of the main causes of death of marine model for fishes invokes rapid accumulation of corpses on an anoxic organisms from Pesciara (Marramà et al. 2016a). bottom, where a well-developed microbial biofilm delayed their Most fossils from Monte Postale are incomplete or strongly decomposition, protected them from scavengers and bottom disarticulated (c. 90% of fish specimens) to the degree that they currents, and promoted rapid mineralization. Tetany exhibited by cannot be identified at genus or species level. This incompleteness numerous fish specimens (e.g. Fig. 4c) suggests that toxic algal and disarticulation, as well as the disruption of fins, S-shaped Downloaded from http://jgs.lyellcollection.org/ by guest on September 30, 2021

M. Friedman & G. Carnevale

in a silled depression with restricted bottom circulation, a short distance from the coast at a depth of many tens of metres. According to those researchers, coral reefs and seagrass beds were present in close proximity. Based on an integrative approach using facies analysis and foraminiferal palaeoecology, Papazzoni & Trevisani (2006) proposed deposition in a subtropical lagoon close to an emerged area and characterized by seasonal changes of water circulation that modulated oxygen concentrations near the seafloor. What is agreed upon by all the recent studies is that sediments of Pesciara reflect a peri-reefal system subject to the ecological influence of both coastal environments and the open sea, and that the deposition of the fossiliferous micritic limestone took place in a low-energy basin characterized by permanent bottom dysoxia or anoxia (Marramà et al. 2016a). Sometimes conspicuous primary production was dominated by diatoms (Schwark et al. 2009), which constituted the base of the trophic chain of the Pesciara assemblage and sustained large shoals of the sardine Bolcaichthys catopygop- terus (Marramà & Carnevale 2015a). Roughly half of fossil specimens from the laminated wackestone of Monte Postale are remains of algae and plants, followed by fishes (about 30%) showing different degrees of completeness, and abundant invertebrates (corals, molluscs and crustaceans). Fishes primarily consist of small epibenthic species and rarer large taxa (Marramà et al. 2016a). The laminated wackestone of Monte Postale originated in a lagoon surrounded by coralgal buildups made of corals, calcareous algae and encrusting foraminifera (Vescogni et al. 2016). The peri-reefal areas were densely vegetated by seagrass beds and mangroves, the latter dominated by the mangrove palm Nypa (Marramà et al. 2016a).

Evolutionary and palaeoecological significance The Bolca Lagerstätten provide critical snapshots of reef-associated marine ecosystems and adjacent terrestrial areas in the early Cenozoic. As such, they are a unique line of evidence bearing on the origin and early history of modern reefs, which represent major hotspots of marine biodiversity. As a result of previous research, the importance of the Bolca localities is clearest for fishes and derives Fig. 5. Examples of exceptional preservation of fossils from the Bolca from three main features apart from excellent preservation: early Lagerstätten. (a) Preservation of pigmentation (p), soft tissues and gut Eocene age, unique environmental setting and palaeogeographical contents in the triakid shark Galeorhinus cuvieri, Museo Geologico location. With respect to age, the principal Bolca sites postdate the Giovanni Capellini, Bologna (MGGC) 1976; specimen shown in right Cretaceous–Paleogene (K–Pg) mass extinction by roughly 15 myr, lateral view and illuminated in ultraviolet light. Dashed-line rectangle providing a glimpse into a mature ecosystem following an interval indicates area shown in (b). (b) Close-up view of abdominal cavity of of evolutionary recovery (see Erwin 2001; Box 2, Fig. 6). With specimen in (a), including spiral valve of intestine (sv) and skeleton of the respect to environmental setting, Pesciara–Monte Postale show barracuda Sphyraena bolcensis representing gut contents (gc). Images substantially higher species richness of fishes than, and contrasting courtesy of T. Miyashita (University of Alberta). (c) Pigmentation patterns taxonomic composition to, other Ypresian deposits that can be in the eel Paranguilla tigrina, Museo di Geologia e Paleontologia, considered Lagerstätten in their own right (Danata Formation, Università degli Studi di Padova (MGP-PD) 26288; specimen shown in left lateral view. Image courtesy of S. Castelli and L. Giusberti (MGP- Turkmenistan; Fur Formation, Denmark; London Clay Formation, PD). Scale bars: (a) 75 mm; (b) 25 mm; (c) 20 mm. UK; Friedman et al. 2016); it is possible that this is due to close association with reefs. With respect to palaeobiogeography, the Bolca sites are ideally positioned for capturing a high-diversity curving of the vertebral column and the unidirectional dispersion of marine assemblage of Paleogene age. High species richness of scales around the body are indicative of episodic disturbance and benthic foraminifera, corals and molluscs in the late Eocene of the mixing of the bottom. These occasional events resulted in the western Tethys, the area including Bolca, suggests that this region development of normal aerobic conditions on the bottom that was an ancient biodiversity hotspot, comparable with today’s Indo- eventually allowed the settling of a moderately diverse benthic Pacific (Renema et al. 2008; Fig. 7a). fauna, revealed by relatively abundant bioturbation tracks and Modern coralgal reef ecosystems trace their origins to the early crustacean and mollusc remains (Marramà et al. 2016a). Paleogene (Kiessling 2009; Bellwood et al. 2017). Temporally, the Bolca Lagerstätten fall near the end of a second wave of reef Palaeoenvironment invasions by modern teleosts as inferred on the basis of comparative phylogenetic data (Price et al. 2014), and their fauna is often hailed The differences in taphonomy and of the fish assemblages as the earliest modern reef-fish assemblage (Bellwood 1996; themselves suggest different palaeoenvironmental settings for the Bellwood & Wainwright 2002). Such comparisons are not without two principal Bolca localities. Landini & Sorbini (1996) hypothe- merit, but there are differences from living reef faunas (Fig. 7b–d). sized that deposition of the laminated limestone of Pesciara occurred Some major groups of reef-associated fishes such as butterflyfishes Downloaded from http://jgs.lyellcollection.org/ by guest on September 30, 2021

The Eocene Bolca Lagerstätten

Box 2. Bolca and the evolutionary radiation of acanthomorphs Acanthomorphs, or the spiny-rayed teleosts, include nearly one in three living vertebrate species and the majority of fish species. Their diversity in form is commensurate with their diversity in kind, with modern acanthomorphs assuming morphologies as divergent as those of flounders, seahorses, anglerfishes, tunas and mudskippers. The majority of acanthomorphs in turn belong to a group known as percomorphs, a species-rich radiation that has long vexed systematists as the unresolved ‘bush at the top’ of the teleost tree of life. The first acanthomorphs appear in the fossil record at the beginning of the Late Cretaceous, around 100 myr ago, represented by deeply branching lineages such as lampridiforms and beryciforms (Davesne et al. 2014, 2016; Fig. 6). The oldest definitive percomorphs make their debut tens of millions of years later, near the end of the Late Cretaceous, and belong to early diverging groups such as syngnathiforms, ophidiiforms and possibly batrachoidiformes (Carnevale & Johnson 2015). Although some basal phylogenetic splits had clearly taken place by the Late Cretaceous, acanthomorphs remained comparatively minor components of marine faunas of this age, rarely making up more than a third of all fish species at any given fossil locality (Patterson 1993a; Friedman et al. 2016). Highly selective extinction among marine fishes occurred at the end of the Cretaceous (Friedman 2009). Faunas of the earliest Cenozoic remain poorly known, but largely include acanthomorph groups already known from the Late Cretaceous (Alvarado-Ortega et al. 2015; Adolfssen et al. 2017). A series of deposits from near or shortly after the Paleocene–Eocene Thermal Maximum in Europe and western Asia provide the first evidence of acanthomorph-dominated faunas with highly diversified percomorph lineages (Patterson 1993a; Friedman et al. 2016; Bannikov et al. 2017). For the most part, these deposits represent open- water settings, with abundant representatives of pelagic groups but showing only modest diversity of nearshore or reef-associated lineages. Pesciara–Monte Postale postdate the earliest of these assemblages by roughly 6 myr, and further mark the shift to percomorph-dominated marine fish faunas. Significantly, the Bolca localities capture the first (and in a few cases, only) body fossil occurrences of many reef-fish clades (Fig. 6). Increased taxonomic dominance of acanthomorphs in the early Paleogene is associated with a substantial increase in morphological diversity as measured by overall body shape (Friedman 2010), although there is some evidence for an earlier onset of cranial diversification (Sallan & Friedman 2012). Pesciara and Monte Postale are unquestionably exceptional, but the pattern of increased anatomical diversity among acanthomorphs in the early Paleogene appears robust to the exclusion of these sites from quantitative analyses(Friedman 2010).

Fig. 6. Time-calibrated molecular phylogeny of extant acanthomorph teleosts, adapted from Near et al. (2013). Percomorph acanthomorphs highlighted in orange. Concentric rings represent Cretaceous–Paleogene (K–Pg) boundary (dashed line) and the age of the principal fish-bearing Bolca localities of Pesciara and Monte Postale (continuous black line). Filled circles indicate extant family-level clades known from Bolca. A black filled circle indicates that material from these sites represents the first body-fossil appearance for the group in the geological record.

and parrotfishes are not found at Pesciara–Monte Postale, and only (Bellwood 1996; Bellwood et al. 2017; Fig. 7c). There are appear later in the Cenozoic (Bellwood & Schultz 1988; Carnevale varying degrees of overlap between fossils of the Bolca 2006). Associated with the lack of some modern groups are Lagerstätten and their modern reef-dwelling relatives, as gauged remarkable examples of evolutionary convergence between Eocene by geometric morphometric quantification of body shape (Bellwood and extant reef fishes (Tyler & Bannikov 2005). Contrasts in terms of et al. 2014a; Marramà et al. 2016b), as well as differences in diversity of genus-level lineages within families, as well as relative ecomorphologically relevant traits such as eye size (Goatley et al. abundance of individuals within families, are also apparent 2010), mandibular mechanics (Bellwood 2003; Bellwood & Hoey Downloaded from http://jgs.lyellcollection.org/ by guest on September 30, 2021

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Fig. 7. The fossil fishes of the Bolca Lagerstätten represent an early coral reef assemblage. In panels comparing multiple localities, Bolca is represented by a star. (a) Patterns of biodiversity in Tethys during the Eocene as inferred based on benthic Foraminifera. The area including Bolca represents a ‘hotspot’ enclosed by dashed line. Adapted from Renema et al. (2008).(b) Principal components ordination of modern reef-fish assemblages and the Pesciara–Monte Postale ichthyofauna, based on taxonomic composition. Adapted from Bellwood (1997).(c) Differences between genus-level diversity within major extant reef-fish families in a modern rocky reef in the eastern Pacific (top) and Pesciara–Monte Postale (bottom). Other modern reef ecosystems show similar contrasts to these Eocene sites. Adapted from Bellwood et al. (2017).(d) Morphological disparity (multivariate variance) of modern reef-fish faunas and that of Pesciara–Monte Postale, assessed from a geometric morphometric analysis of body shape and fin position. Adapted from Marramà et al. (2016b).

2004), jaw protrusion (Bellwood et al. 2015) and dental morphology To a first order of approximation, the Pesciara–Monte Postale (Bellwood et al. 2014b). Although commonly compared with Indo- fauna appears modern and there is much truth to the quip of Pacific assemblages on the basis of groups that are endemic to this Patterson (1993a, p. 53) that subsequent evolution among marine modern biodiversity hotspot, the Pesciara–Monte Postale fish fauna fishes ‘was mere tinkering’ (Box 2). However, there are peculiar is not strictly comparable with those of either the Atlantic or Indo- extinct phenotypes among otherwise familiar bodyplans. These Pacific (Bellwood 1997; Fig. 7b). Taken together with other include: early relatives of flatfishes indicating gradual, rather than localities, the Bolca sites provide a picture of a widespread saltational, evolution of asymmetry (Friedman 2008, 2012), although Paleogene marine fish fauna. At higher taxonomic levels (i.e. that stepwise change might have occurred over a geologically short family), it is apparent that the Indo-Pacific region has maintained interval (Harrington et al. 2016); early relatives of gymnodont much of this diversity, whereas Atlantic reef assemblages have been tetraodontiforms (Tyler & Santini 2002) that provide clues to the winnowed by regional extinction (Bellwood 1997). evolutionary origin of the beak-like dentition further elaborated by Fossils from the Bolca Lagerstätten also deliver important living members of the group (Fraser et al. 2012); the peculiar evidence relating to individual fish clades, especially in terms of †Bajaichthys, a zeiform (John Dory) that shows an unprecedented constraints on times of evolutionary divergence and detailed ribbon-like morphology in a group otherwise characterized by deep character data bearing on patterns of phenotypic evolution. The bodies (Davesne et al. 2017); the extinct syngnathiform group oldest occurrences of many teleost families are from Pesciara– †Aulorhamphidae, which combines the elongated snouts so charac- Monte Postale (Patterson 1993a,b; Fig. 6), and fishes from these teristic of the order with generalized postcrania (Tyler 2004). localities serve as important temporal constraints for estimating evolutionary timescales under a variety of approaches (e.g. Near Summary et al. 2012, 2013; Chen et al. 2014; Arcila et al. 2015; Close et al. 2016; Bannikov et al. 2017). The impact of Pesciara–Monte Postale The Bolca Lagerstätten provide a unique window into a series of on raw counts of teleost familial diversity through the Cenozoic is fully marine to terrestrial environments in the early Eocene striking, and suggestive of an extreme Lagerstätten effect (Patterson of Tethys. Their remarkable diversity reflects a fortuitous 1994). Such obvious bias aside, the Bolca Lagerstätten and other combination of taphonomic factors combined with a reef setting fossil deposits of similar age all record a major shift in marine fish in a region interpreted as an ancient biodiversity hotspot. The most assemblages between the Late Cretaceous and Paleogene, defined celebrated sites of the Bolca Lagerstätten are Pesciara and Monte most conspicuously by the increased taxonomic dominance of Postale, both of which yield exquisitely preserved fish fossils acanthomorphs (spiny-rayed fishes) in general and percomorphs totalling well over 200 species. The fossil fishes from these sites are (perch-like fishes) in particular (Box 2). particularly significant in documenting the rise of acanthomorphs, Downloaded from http://jgs.lyellcollection.org/ by guest on September 30, 2021

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Box 3. Outstanding questions The past few years have seen substantial improvements in our understanding of the geological and environmental context of the Pesciara and Monte Postale sites (e.g. Marramà et al. 2016a), coupled with increasingly sophisticated quantitative analysis of their fish faunas (e.g. Bellwood et al. 2014a; Marramà et al. 2016b). However, a series of outstanding challenges must still be addressed. First, clear stratigraphic correlation between freshwater to brackish Vegroni and Purga di Bolca localities and classic marine sites of Bolca remain elusive, partly owing to the complex post-depositional geological history of the region. Clarity on the age of these nearshore to terrestrial deposits will provide insight into the degree to which the Bolca sites collectively represent a geological snapshot, or are instead diachronous. Second, many components of the extended Bolca assemblage are in dire need of taxonomic revision. Nowhere is this more conspicuous than among plants, known fromeach of the Bolca localities but subject to remarkably little targeted investigation over the past century. Third, although the fishes are without question the best known taxonomic component of the Bolca assemblage, it could be argued that they remain understudied relative to the amount of available material. This issue is more acute for some groups (e.g. chondrichthyans), but it is clear that more information is preserved in material studied in the past, from patterns of pigmentation, soft-tissue preservation, and fine osteological details accessible through transfer preparation. New anatomical data for old fossils might help better constrain their phylogenetic positions, a prerequisite for higher-level analyses addressing macroecological and macroevolutionary questions surrounding the origins of modern reef-fish assemblages and specific clades (Box 2).

the dominant group of marine teleosts, as well as providing critical Bellwood, D.R. & Hoey, A.S. 2004. Feeding in Mesozoic fishes: a functional – clues to the early assembly of modern tropical reef ecosystems. perspective. In:Arratia,G.&Tintori,A.(eds)Mesozoic Fishes 3 Systematics, Paleoenvironments and Biodiversity. Pfeil, Munich, Although they are often overshadowed by the fishes, a wide range of 639–649. marine invertebrates, aquatic plants and algae, terrestrial plants and Bellwood, D.R. & Schultz, O. 1988. A review of the fossil record of the insects are also present at Pesciara and Monte Postale. The marginal parrotfishes (Labroidei: Scaridae) with a description of a new Calotomus species from the Middle Miocene (Badenian) of Austria. Annalen des to terrestrial sites near Bolca remain little examined, and their Naturhistorischen Museums in Wien, Serie A, 92,55–71. relationship to the ‘classic’ localities remains unclear (Box 3). Bellwood, D.R. & Wainwright, P.C. 2002. The history and biogeography of fishes on coral reefs. In: Sale, P.F. (ed.) Coral Reef Fishes. Elsevier, Amsterdam, 5–32. Acknowledgements We thank P. Donoghue (University of Bristol) for Bellwood, D.R., Goatley, C.H.R., Brandl, S.J. & Bellwood, O. 2014a. Fifty his invitation to write this review, and our many colleagues studying the fossils million years of herbivory on coral reefs: fossils, fish and functional and geology of the Bolca sites for their helpful input over the years. We especially innovations. Proceedings of the Royal Society of London, Series B, 281, thank the Museo Civico di Storia Naturale, Verona, the Museo di Geologia 20133046. Bellwood, D.R., Hoey, A.S., Bellwood, O. & Goatley, C.H. 2014b. Evolution of e Paleontologia, Università degli Studi di Padova, Padua, Muséum national – d’Histoire naturelle, Paris, the Natural History Museum, London and long-toothed fishes and the changing nature of fish benthos interactions on Naturhistorisches Museum, Vienna for allowing us to photograph fossil fishes coral reefs. Nature Communications, 5, 3144. in their collections. C. Abraczinskas (University of Michigan Museum of Bellwood, D.R., Goatley, C.H., Bellwood, O., Delbarre, D.J. & Friedman, M. 2015. The rise of jaw protrusion in spiny-rayed fishes closes the gap on elusive Paleontology) produced or improved the figures. A. Capobianco (University of – Michigan), D. Harper (University of Durham) and an anonymous referee prey. Current Biology, 25, 2696 2700. provided helpful comments on an earlier version of this paper. Bellwood, D.R., Goatley, C.H. & Bellwood, O. 2017. The evolution of fishes and corals on reefs: form, function and interdependence. Biological Reviews, 92, Scientific editing by Philip Donoghue 878–901. Blot, J. 1969. Les poissons fossiles du Monte Bolca classés jusqu’ici dans les familles des Carangidae, Menidae, Ephippidae, Scatophagidae. Studi e Ricerche sui Giacimenti Terziari di Bolca, 1,1–525. References Blot, J. 1978. Les Apodes fossils du Monte Bolca. Studi e Ricerche sui Adolfssen, J.S., Milan, J. & Friedman, M. 2017. Review of the Danian vertebrate Giacimenti Terziari di Bolca, 3,1–260. fauna of southern Scandinavia. Bulletin of the Geological Society of Denmark, Blot, J. 1980. La faune ichthyologique des gisements du Monte Bolca (Province 65,1–23. de Vérone, Italie). Bulletin du Muséum National d’Histoire Naturelle, Paris, Agassiz, L. 1833–1844. Recherches sur les Poissons fossiles. Petitpierre, 4e Serie,̀ 2, Section C, 4, 339–396. Neuchâtel. Blot, J. 1987. L’ordre des Pycnodontiformes. Studi e Ricerche sui Giacimenti Agassiz, L. 1835. Revue critique des Poissons fossiles figurés dans l’Ittiolitologia Terziari di Bolca, 5,1–211. Veronese. Petitpierre et Prince, Neuchâtel. Bonde, N. 2008. Osteoglossomorphs of the marine Lower Eocene of Denmark – Agnini, C., Fornaciari, E., Raffi, I., Catanzariti, R., Pälike, H., Backman, J. & Rio, with remarks on other Eocene taxa and their importance for palaeobiogeo- D. 2014. Biozonation and biochronology of Paleogene calcareous nanno- graphy. In: Cavin, L., Longbottom, A. & Richter, M. (eds) Fishes and the fossils from low and middle latitudes. Newsletters on Stratigraphy, 47, Break-up of Pangaea. Geological Society, London, Special Publications, 295, 131–181. 253–310, https://doi.org/10.1144/SP295.14 Alvarado-Ortega, J., Cuevas-García, M., del Pilar Melgarejo-Damián, M., Bosellini, A. 1989. Dynamics of Tethyan carbonate platforms. In: Crevello, P.D., Cantalice, K.M., Alaniz-Galvan, A., Solano-Templos, G. & Than-Marchese, Wilson, J.L. & Read, J.F. (eds) Controls on Carbonate Platform and Basin B.A. 2015. Paleocene fishes from Palenque, Chiapas, southeastern Mexico. Platform. SEPM Special Publications, 44,3–13. Palaeontologia Electronica, 18, 39A. Carminati, E., Lustrino, M. & Doglioni, C. 2012. Geodynamic evolution of the Arcila, D., Pyron, R.A., Tyler, J.C., Ortí, G. & Betancur-R, R. 2015. An central and western Mediterranean: tectonic vs. igneous petrology constraints. evaluation of fossil tip-dating versus node-age calibrations in tetraodontiform Tectonophysics, 579, 173–192. fishes (Teleostei: Percomorphaceae). Molecular Phylogenetics and Evolution, Carnevale, G. 2006. Morphology and biology of the Miocene butterflyfish 82, 131–145. Chaetodon ficheuri (Teleostei: Chaetodontidae). Zoological Journal of the Arratia, G. & Tischlinger, H. 2010. The first record of Late Jurassic Linnean Society, 146, 251–267. crossognathiform fishes from Europe and their phylogenetic importance for Carnevale, G. & Johnson, G.D. 2015. A Cretaceous cusk-eel (Teleostei, teleostean phylogeny. Fossil Record, 13, 317–341. Ophidiiformes) from Italy and the Mesozoic diversification of percomorph Bannikov, A.F. 2014. The systematic composition of the Eocene actinopterygian fishes. Copeia, 103, 771–791. fish fauna from Monte Bolca, northern Italy, as known to date. Studi e Carnevale, G., Bannikov, A.F., Marramà, G., Tyler, J.C. & Zorzin, R. 2014. The Ricerche sui Giacimenti Terziari di Bolca, 15,23–34. Pesciara–Monte Postale Fossil-Lagerstätte: fishes and other vertebrates. In: Bannikov, A.F., Tyler, J.C., Arcila, D. & Carnevale, G. 2017. A new family of Papazzoni, C.A., Giusberti, L., Carnevale, G., Roghi, G., Bassi, D. & Zorzin, gymnodont fish (Tetraodontiformes) from the earliest Eocene of the Peri- R. (eds) The Bolca Fossil-Lagerstätten: A Window into the Eocene World. Tethys (Kabardino–Balkaria, northern Caucasus, Russia). Journal of Rendiconti della Società Paleontologica Italiana, 4,37–63. Systematic Palaeontology, 15, 129–146. Ceruti, B. & Chiocco, A. 1622. Musaeum Francesci Calceolari Iunioris Bellwood, D.R. 1996. The Eocene fishes of Monte Bolca: the earliest coral reef Veronensis. Apud Angelum Tatum, Verona. fish assemblage. Coral Reefs, 15,11–19. Chen, W.-J., Santini, F., Carnevale, G., Chen, J.-N., Liu, S.H., Lavoué, S. & Bellwood, D.R. 1997. Reef fish biogeography: habitat associations, fossils and Mayden, R.L. 2014. New insights on early evolution of spiny-rayed fishes phylogenies. In: Lessios, H.A. & Macintyre, I.G. (eds) Proceedings of the 8th (Teleostei: Acanthomorpha). Frontiers in Marine Science, 1, 53. International Coral Reef Symposium, Smithsonian Tropical Research Close, R.A., Johanson, Z., Tyler, J.C., Harrington, R.C. & Friedman, M. 2016. Institute, Balboa, Panama 1, 379–384. Mosaicism in a new Eocene pufferfish highlights rapid morphological Bellwood, D.R. 2003. Origins and escalation of herbivory in fishes: a functional innovation near the origin of crown tetraodontiforms. Palaeontology, 59, perspective. Paleobiology, 29,71–83. 499–514. Downloaded from http://jgs.lyellcollection.org/ by guest on September 30, 2021

M. Friedman & G. Carnevale

Davesne, D., Friedman, M., Barriel, V., Lecointre, G., Janvier, P., Gallut, C. & Marramà, G. & Carnevale, G. 2016. An Eocene anchovy from Monte Bolca, Otero, O. 2014. Early fossils illuminate character evolution and interrelation- Italy: The earliest known record for the family Engraulidae. Geological ships of Lampridiformes (Teleostei, Acanthomorpha). Zoological Journal of Magazine, 153,84–94. the Linnean Society, 172, 475–498. Marramà, G. & Carnevale, G. 2017. Morphology, relationships and palaeobiol- Davesne, D., Gallut, C., Barriel, V., Janvier, P., Lecointre, G. & Otero, O. ogy of the Eocene barracudina †Holosteus esocinus (Aulopiformes: 2016. The phylogenetic intrarelationships of spiny-rayed fishes Paralepididae) from Monte Bolca, Italy. Zoological Journal of the Linnean (Acanthomorpha, Teleostei, Actinopterygii): fossil taxa increase the Society, 181, 209–228. congruence of morphology with molecular data. Frontiers in Ecology and Marramà, G., Bannikov, A.F., Tyler, J.C., Marramà, G. & Carnevale, G. 2016a. Evolution, 4, article 129. Controlled excavations in the Pesciara and Monte Postale sites provide new Davesne, D., Carnevale, G. & Friedman, M. 2017. Bajaichthys elegans insights about the palaeoecology and taphonomy of the fish assemblage of the from the Eocene of Bolca (Italy) and the overlooked morphological Eocene Bolca Konservat-Lagerstätte, Italy. Palaeogeography, diversity of Zeiformes (Teleostei, Acanthomorpha). Palaeontology, 60, Palaeoclimatology, Palaeoecology, 454, 228–245. 255–268. Marramà, G., Garbelli, C. & Carnevale, G. 2016b. A clade-level morphospace for de Blainville, H.D. 1818. Poissons fossiles. In: Nouveau Dictionnaire d’Histoire the Eocene fishes of Bolca: Patterns and relationships with modern tropical naturelle appliquée aux arts, à l’agriculture, à l’économie rurale et shallow marine assemblages. Bollettino della Società Paleontologica Italiana, domestique, à la medicine, etc., XXVII. Deterville, Paris, 310–395. 55, 139–156. Doglioni, C. & Bosellini, A. 1987. Eoalpine and mesoalpine tectonics in the Marramà, G., Carnevale, G., Engelbrecht, A., Claeson, K.M., Zorzin, R., Southern Alps. Geologische Rundschau, 77, 734–754. Fornasiero, M. & Kriwet, J. 2017a. A synoptic review of the Eocene Erwin, D.H. 2001. Lessons from the past: biotic recoveries from mass (Ypresian) cartilaginous fishes (Chondrichthyes: Holocephali, extinctions. Proceedings of the National Academy of Sciences of the USA, Elasmobranchii) of the Bolca Konservat-Lagerstätte, Italy. Paläontologische 98, 5399–5403. Zeitschrift, first published online December 30, 2017, https://doi.org/10.1007/ Fanti, F., Minelli, D., Conte, G.L. & Miyashita, T. 2016. An exceptionally s12542-017-0387-z preserved Eocene shark and the rise of modern predator–prey interactions in Marramà, G., Engelbrecht, A., Carnevale, G. & Kriwet, J. 2017b. Eocene sand the coral reef food web. Zoological Letters, 2,9. tiger sharks (Lamniformes, Odontaspididae) from the Bolca Konservat- Fraser, G.J., Britz, R., Hall, A., Johanson, Z. & Smith, M.M. 2012. Replacing the Lagerstätte, Italy: palaeobiology, palaeobiogeography and evolutionary first-generation dentition in pufferfish with a unique beak. Proceedings of the significance. Historical Biology,1–15, https://doi.org/10.1080/08912963. National Academy of Sciences of the USA, 109, 8179–8184. 2017.1341503 Friedman, M. 2008. The evolutionary origin of flatfish asymmetry. Nature, 454, Massalongo, A.B. 1850. Schizzo geognostico sulla valle del Progno o torrente 209–212. d’Illasi: con un saggio sopra la flora primordiale del M. Bolca. G. Antonelli, Friedman, M. 2009. Ecomorphological selectivity among marine teleost fishes Verona. during the end-Cretaceous extinction. Proceedings of the National Academy of Massalongo, A.B. 1851. Sopra le piante fossili dei terreni terziari del vicentino. Sciences of the USA, 106, 5218–5223. A. Bianchi, Padova. Friedman, M. 2010. Explosive morphological diversification of spiny-finned Massalongo, A. 1859. Specimen photographicum animalium quorumdam teleost fishes in the aftermath of the end-Cretaceous extinction. Proceedings of plantarumque fossilium Agri Veronensis. Vicentini-Franchini, Verona. the Royal Society of London, Series B, 277, 1675–1683. Mattioli, P.A. 1550. Petri Andreae Matthioli Medici Senensis Commentarii, in Friedman, M. 2012. Osteology of †Heteronectes chaneti (Acanthomorpha, Libros sex Pedacii Dioscoridis Anazarbei, de Materia Medica, Adjectis quàm Pleuronectiformes), an Eocene stem flatfish, with a discussion of plurimis plantarum & animalium imaginibus, eodem authore, detti flatfish sister-group relationships. Journal of Vertebrate Paleontology, 32, Commentarii. Valgrisi, Venezia. 735–756. Meschinelli, L. & Squinabol, S. 1892. Flora Terziaria Italica. Tipografia del Friedman, M., Beckett, H.T., Close, R.A. & Johanson, Z. 2016. The English Seminario, Padova. chalk and London clay: Two remarkable British bony fish Lagerstätten. In: Near, T.J., Eytan, R.I. et al. 2012. Resolution of ray-finned fish phylogeny and Johanson, Z., Barrett, P.M., Richer, M. & Smith, M. (eds) Arthur Smith timing of diversification. Proceedings of the National Academy of Sciences of Woodward: his Life and Influence on Modern Vertebrate Palaeontology. the USA, 109, 13698–13703. Geological Society, London, Special Publications, 430, 165–200, https://doi. Near, T.J., Dornburg, A. et al. 2013. Phylogeny and tempo of diversification in org/10.1144/SP430.18 the superradiation of spiny-rayed fishes. Proceedings of the National Academy Giusberti, L., Del Favero, L. & Roghi, G. 2014a. Purga di Bolca–Vegroni of Sciences of the USA, 110, 12738–12743. sites. In: Papazzoni, C.A., Giusberti, L., Carnevale, G., Roghi, G., Bassi, Papazzoni, C.A. & Trevisani, E. 2006. Facies analyes, palaeoenvironmental D. & Zorzin, R. (eds) The Bolca Fossil-Lagerstätten: A Window into the reconstruction, and biostratigraphy of the ‘Pesciara di Bolca’ (Verona, Eocene World. Rendiconti della Società Paleontologica Italiana, 4, northern Italy): An early Eocene Fossil-Lagerstätte. Palaeogeography, 95–103. Palaeoclimatology, Palaeoecology, 242,21–35. Giusberti, L., Fornasiero, M. & Zorzin, R. 2014b. The Pesciara–Monte Postale Papazzoni, C.A., Giusberti, L., Carnevale, G., Roghi, G., Bassi, D. & Zorzin, R. Fossil-Lagerstätte: 4. The ‘minor fauna’ of the laminites. In: Papazzoni, C.A., (eds) 2014. The Bolca Fossil-Lagerstätten: A Window into the Eocene World. Giusberti, L., Carnevale, G., Roghi, G., Bassi, D. & Zorzin, R. (eds) The Bolca Rendiconti della Società Paleontologica Italiana, 4. Fossil-Lagerstätten: A Window into the Eocene World. Rendiconti della Papazzoni, C.A., Fornaciari, E., Giusberti, L., Vescogni, A. & Fornaciari, B. Società Paleontologica Italiana, 4,37–63. 2017. Integrating shallow benthic and calcareous nannofossil zones: the Lower Goatley, C.H., Bellwood, D.R. & Bellwood, O. 2010. Fishes on coral Eocene of the Monte Postale section (Northern Italy). Palaios, 32,1. –12 reefs: changing roles over the past 240 million years. Paleobiology, 36, Patterson, C. 1984. Chanoides, a marine Eocene otophysan fish (Teleostei: 415–427. Ostariophysi). Journal of Vertebrate Paleontology, 4, 430–456. Harrington, R.C., Faircloth, B.C., Eytan, R.I., Smith, W.L., Near, T.J., Alfaro, Patterson, C. 1993a. An overview of the early fossil record of acanthomorphs. M.E. & Friedman, M. 2016. Phylogenomic analysis of carangimorph fishes Bulletin of Marine Science, 52,29–59. reveals flatfish asymmetry arose in a blink of the evolutionary eye. BMC Patterson, C. 1993b. Osteichthyes: Teleostei. In: Benton, M.J. (ed.) The Fossil Evolutionary Biology, 16, 224. Record 2. Chapman & Hall, London, 621–656. Kedves, M. & Zsivin, Z. 1970. Spore–pollen data from the marl layers of Mte. Patterson, C. 1994. Bony fishes. In: Prothero, D.R. & Schoch, R.M. (eds) Major Bolca. Acta Biologica Szeged, 16,55–68. Features of Vertebrate Evolution. Paleontological Society, Short Courses in Kiessling, W. 2009. Geologic and biologic controls on the evolution of reefs. Paleontology, 7,57–84. Annual Review of Ecology, Evolution, and Systematics, 40, 173–192. Price, S.A., Schmitz, L. et al. 2014. Two waves of colonization straddling the K– Landini, W. & Sorbini, L. 1996. Ecological and trophic relationships of Eocene Pg boundary formed the modern reef fish fauna. Proceedings of the Royal Monte Bolca (Pesciara) fish fauna. In: Cherchi, A. (ed) Autoecology of Society of London, Series B, 281, 20140321. Selected Fossil Organisms: Achievements and Problems. Bollettino della Renema, W., Bellwood, D.R. et al. 2008. Hopping hotspots: global shifts in Società Paleontologica Italiana, Volume Speciale, 3, 105–112. marine biodiversity. Science, 321, 654–657. Luciani, V. 1989. Stratigrafia sequenziale del Terziario nella Catena del Monte Sallan, L.C. & Friedman, M. 2012. Heads or tails: staged diversification in Baldo (provincie di Verona e Trento). Memorie di Scienze Geologiche, 41, vertebrate evolutionary radiations. Proceedings of the Royal Society of 263–351. London, Series B, 279, 2025–2032. Luciani, V., Dickens, G.R., Backman, J., Fornaciari, E., Giusberti, L., Agnini, C. Schwark, L., Ferretti, A., Papazzoni, C.A. & Trevisani, E. 2009. Organic &D’Onofrio, R. 2016. Major perturbations in the global carbon cycle and geochemistry and paleoenvironment of the Early Eocene ‘Pesciara di Bolca’ photosymbiont-bearing planktic foraminifera during the early Eocene. Konservat-Lagerstätte, Italy. Palaeogeography, Palaeoclimatology, Climates of the Past, 12, 981–1007. Palaeoecology, 273, 272–285. Macera, P., Gasperini, D., Ranalli, G. & Mahatsente, R. 2008. Slab detachment Sferco, E., López-Arbarello, A. & Báez, A.M. 2015. Phylogenetic relationships and mantle plume upwelling in subduction zones: an example from the Italian of †Luisiella feruglioi (Bordas) and the recognition of a new clade of South-Eastern Alps. Journal of Geodynamics, 45,32–48. freshwater teleosts from the Jurassic of Gondwana. BMC Evolutionary Marramà, G. & Carnevale, G. 2015a. The Eocene sardine †Bolcaichthys Biology, 15, 268. catopygopterus (Woodward, 1901) from Bolca, Italy: osteology, taxonomy, Tang, C.M. 2002. Monte Bolca: An Eocene fishbowl. In: Bottjer, D.J., Etter, W., and paleobiology. Journal of Vertebrate Paleontology, 35, e1014490. Hagadorn, J.W. & Tang, C.M. (eds) Exceptional Fossil Preservation: A Marramà, G. & Carnevale, G. 2015b. Eocene round herring from Monte Bolca, Unique View on the Evolution of Marine Life. Columbia University Press, Italy. Acta Palaeontologica Polonica, 60, 701–710. New York, 365–377. Downloaded from http://jgs.lyellcollection.org/ by guest on September 30, 2021

The Eocene Bolca Lagerstätten

Trevisani, E. 2015. Upper Cretaceous–lower Eocene succession of the Monte Vescogni, A., Bosellini, F.R. et al. 2016. Coralgal buildups associated with the Postale and its relationship with the ‘Pesciara di Bolca’ (Lessini Mountains, Bolca Fossil-Lagerstätten: new evidence from the Ypresian of Monte Postale northern Italy): deposition of a fossil-fish lagerstätte. Facies, 61,7. (NE Italy). Facies, 62, 21. Trevisani, E., Papazzoni, C.A., Ragazzi, E. & Roghi, G. 2005. Early Volta, G.S. 1789. Degl’impietrimenti del territorio veronese ed in particolare dei Eocene amber from the ‘Pesciara di Bolca’ (Lessini Mountains, Pesci fossili del celebre Monte Bolca per servire di continuazione Northern Italy). Palaeogeography, Palaeoclimatology, Palaeoecology, 223, all’argomento delle rivoluzioni terracquee. Letter to Vincenzo Bozza, 260–274. Mantua. Tyler, J.C. 2004. Review of the species of the Eocene of Monte Bolca, Italy, fish Volta, G.S. 1796–1809. Ittiolitologia Veronese del Museo Bozziano ora annesso family Aulorhamphidae, new, related to Gasterosteiformes. Studi e Ricerche a quello del Conte Giovambattista Gazola e di altri gabinetti di fossili sui Giacimenti Terziari di Bolca, 8, 257–268. veronesi. Stamperia Giuliari, Verona. Tyler, J.C. & Bannikov, A.F. 2005. Massalongius gen. & fam. nov., a new clade Wilby, P.R. & Briggs, D.E.G. 1997. Taxonomic trends in the resolution of of acanthuroid fishes (Perciformes, Acanthuroidea) from the early Eocene of detail preserved in fossil phosphatized soft tissues. Geobios, M.S., 20, Monte Bolca, Italy, related to the Zanclidae. Studi e Ricerche sui Giacimenti 493–502. Terziari di Bolca, 11,75–95. Wilde, V., Roghi, G. & Martineto, E. 2014. The Pesciara–Monte Postale Fossil- Tyler, J.C. & Santini, F. 2002. Review and reconstructions of the tetraodontiform Lagerstätte: 3. Flora. In: Papazzoni, C.A., Giusberti, L., Carnevale, G., fishes from the Eocene of Monte Bolca, Italy, with comments on Roghi, G., Bassi, D. & Zorzin, R. (eds) The Bolca Fossil-Lagerstätten: A related Tertiary taxa. Studi e Ricerche sui Giacimenti Terziari di Bolca, 9, Window into the Eocene World. Rendiconti della Società Paleontologica 47–119. Italiana, 4,37–63.