The Bolca Lagerstätten: shallow marine life in the Eocene

Matt Friedman1* & Giorgio Carnevale21 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, ItalyM.F., 0000-0002-0114-7384

*Correspondence: mfriedm@umich.edu

Abstract: The Eocene limestones around the Italian village of Bolca occur in a series of distinct localities providing a uniquesnapshot of marine life in the early Cenozoic. Famous for its fishes, the localities of Bolca also yield diverse invertebrate faunasand a rich, but relatively understudied flora. Most fossils from Bolca derive from the Pesciara and Monte Postale sites, whichbear similar fossils but are characterized by slightly different taphonomic and environmental profiles. Although not preciselycontemporaneous, 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 reefcommunities 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 awarm, shallow marine setting during the early Eocene, roughly50 myr ago. Deposited within an archipelago near the western endof the Tethys Ocean, the major localities of Bolca collectively haveyielded over 500 species of terrestrial vertebrates, fishes, insects,marine invertebrates and plants. The outstanding significance of theBolca Lagerstätten derives from a unique combination of age (nearthe dawn of modern reef ecosystems), location (within an ancientbiodiversity hotspot) and taphonomy (exceptional preservation).Here we provide an overview of these sites, discussing history,geology, fossils and significance.

Geological context

Localities

The village of Bolca lies on the eastern part of Monti Lessini not farfrom Verona, northern Italy. Monti Lessini represents a southernprolongation of the Southern Alps (Carminati et al. 2012). Severalproductive sites characterized by contrasting fossils are known fromthe Bolca region (Papazzoni et al. 2014; Fig. 1), and are collectivelyknown as ‘Monte Bolca’ in older literature although no such placeexists. We refer to this geographically compact collection ofenvironmentally and stratigraphically distinctive localities as theBolca Lagerstätten, drawing distinctions between the various sites.The most famous representative is Pesciara, which has beenexploited since the mid-16th century (Box 1) and yields exquisitelypreserved marine fishes, plants and soft-bodied invertebrates. It isjoined byMonte Postale, located nearby and also famous for marinefishes and plants. These two localities are the source of most fossilsfrom the Bolca area in museums, and have yielded over 100 000exceptionally preserved fossils (e.g. Blot 1969; Box 1). This reviewfocuses on these two localities.

There are two additional nearby localities included among theBolca Lagerstätten: Purga di Bolca and Vegroni. These freshwaterand brackish deposits are classically considered younger thanPesciara and Monte Postale, but their stratigraphic correlation withthe more famous horizons is problematic (Papazzoni et al. 2014).Purga di Bolca consists of lignites around a volcanic neck, and

contains remains of crocodiles, turtles, snakes and plants. Thelignites of Vegroni yield a variety of plants.

Stratigraphy and age

The Pesciara and Monte Postale successions are among the fewshallow-water Eocene sequences deposited on the Lessini Shelf(sensu Bosellini 1989), a palaeogeographical feature of theSouthern Alps that was uplifted during the Alpine orogeny. Uponreaching the photic zone during the early Eocene, the Lessini Shelfacted as a centre of deposition of shallow-water carbonates (Doglioni& Bosellini 1987; Bosellini 1989; Luciani 1989). Eruptive productsof extensive magmatic activity accumulated between the latePaleocene and the middle Eocene (e.g. Macera et al. 2008).Beginning in the early Eocene, these volcanic and volcanoclasticdeposits became intercalated with marls and limestones.

Widespread regional faulting and cross-cutting volcanic unitshinder stratigraphic studies of the Eocene succession of the Bolcaarea. Consequently, the Eocene carbonates of the Lessini Shelf havebeen collectively assigned to the ‘Calcari Nummulitici’, an informalunit poorly constrained in terms of age and depositional setting.

Pesciara consists of a limestone block surrounded by volcanicdeposits (Fig. 1b). The outcrop is less than 20 m thick, covering anarea of a few hundred square metres, and consists of a rhythmicalternation of finely laminated micritic limestone with fishes andplants and grainstone bearing benthic fossils (Papazzoni &Trevisani 2006). Nearly all the fishes, soft-bodied invertebratesand plants collected from Pesciara are from five bands of grey,laminated micritic limestone. The succession of Monte Postaleconsists of more than 130 m of grainstone that alternates withmassive coralgal limestone and laminated wackestone with fishesand plants similar to those of Pesciara (e.g. Vescogni et al. 2016;Papazzoni et al. 2017). The laminated limestone varies in thicknessdepending on position in the succession. However, most layers areabout 1 m thick, very similar to those of Pesciara.

Both the Pesciara and Monte Postale successions were depositedin the early late Ypresian. Calcareous nannofossils and largerbenthic Foraminifera indicate that the Pesciara succession corre-sponds to the upper part of that of Monte Postale. Monte Postale

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spans the entire NP 13 and CNE 5 calcareous nannoplankton zones(Papazzoni et al. 2017), corresponding to a large part of the ShallowBenthic Zone (SBZ) 11 in the time interval between c. 50.5 and48.96 Ma (see Agnini et al. 2014). This corresponds to the earlyEocene climatic optimum (EECO in the sense of Luciani et al.2016). Pesciara has been assigned to the uppermost part of SBZ 11,corresponding to the basal portion of NP 14 and CNE 6, between48.96 and c. 48.5 Ma.

Floral and faunal composition

Study of different components of the Bolca fossil assemblages isuneven. The fishes of Pesciara and Monte Postale have been thesubject of nearly continuous investigation for centuries. The so-called ‘minor fauna’, comprising non-fishes, of Pesciara and MontePostale are poorly known by comparison (Carnevale et al. 2014;Giusberti et al. 2014b). Similarly, relatively little work has builtupon foundational palaeobotanical studies from the 19th century(Wilde et al. 2014).

Plants

Marine plants and macroalgae

Floating or fully marine monocots such as seagrasses are the mostcommon elements of the Pesciara–Monte Postale flora (Wilde et al.2014; Fig. 2a). Brown and red algae are represented by macrofossilsand biomarkers (Schwark et al. 2009).

Terrestrial plants

Ferns are absent, and gymnosperms are limited to long, needle-likeleaves. The terrestrial flora of Pesciara–Monte Postale is dominatedby angiosperms, specifically dicots (Fig. 2b). Terrestrial monocots

are rare, with palms represented only by fruits (complete palms arefound at Vegroni; Giusberti et al. 2014a). Leaves and leaflets,especially of legumes, are the most common remains of dicots, buttwigs, fruits and flowers are also known. Specimens of whole plantsare known, but some of these are regarded as restorations orcomposites (Wilde et al. 2014). In addition to these remains,Pesciara also yields amber (Trevisani et al. 2005). As in themacroflora, angiosperms dominate the microflora, with raregymnosperm pollen and fern spores (Kedves & Zsivin 1970).

In drawing comparisons with approximately coeval fossil floras(e.g. lacustrine deposits of Messel), Wilde et al. (2014) noted lowerdiversity in the Pesciara–Monte Postale macroflora combined with adistinctive composition in terms of both taxa and organs. Theyattributed these features to a taphonomic filter arising from fluvialtransport to the ocean and subsequent shallow marine wave action,and also acknowledged the potentially important role of storms intransporting some plant remains.

Invertebrates

Jellyfishes and corals

Medusae from Pesciara comprise complete specimens preservingdelicate features (Giusberti et al. 2014b; Fig. 2d). Corals are acommon component of the benthic fauna, represented by brokenmaterial in the coarse-grained carbonates intercalated between thelaminites and in the fossiliferous laminated wackestone of MontePostale (Tang 2002; Marramà et al. 2016a; Fig. 1b and c).

Annelids

Annelids from Bolca include four species of polychaete placed intwo genera, and a single species of leech (Giusberti et al. 2014b).

Fig. 1. Location and geology of Pesciaria and Monte Postale, the principal Lagerstätten of Bolca. (a) Location of Bolca in Italy. (b) Topographic map ofregion immediately NW of the village of Bolca. Colours indicate different geological units: yellow, Spilecco Limestone; green, laminated and beddedlimestone; blue, massive limestone; orange, volcanic rocks. Intensity of shading indicates either rock exposed in outcrop (dark) or inferred (light). Adaptedfrom Trevisani (2015).

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Arthropods

Pesciara andMonte Postale yield a diversity of terrestrial andmarinearthropods (Fig. 3c and e). Insects include thysanuruans, odonatans,trichopterans, coleopterans, orthopterans, heteropterans, hymenop-terans and dipterans, with the last group being the most common(Giusberti et al. 2014b). Other terrestrial arthropods include ascorpion and possible pseudoscorpion. Marine crustaceans domin-ate the minor fauna, and include three isopod genera, twostomatopod genera and 12 decapod genera (Giusberti et al. 2014b).

Molluscs

Bivalves and gastropods are abundant in the coarse limestonesbetween laminites, but are uncommon within the laminitesthemselves. However, six bivalve genera and some undescribedforms, plus two gastropod genera, are reported from the laminites.Rare cephalopods include decapodiform coleoids and a nautiloid(Giusberti et al. 2014b).

Lophophorates

Lophophorates are limited to six terebratulid specimens and a singlebryozoan from Pesciara (Giusberti et al. 2014b).

Fishes

Beginning with the first major accounts by Volta (1789, 1796–1809), the fish fauna of Pesciara and Monte Postale has been thesubject of numerous broad overviews (Blot 1980; Bannikov 2014;Carnevale et al. 2014).

Sharks and rays

Chondrichthyans are rare and little studied relative to the morefamous ray-finned fishes, comprising fewer than 20 species(Carnevale et al. 2014; Marramà et al. 2017a,b; Fig. 4a).Nevertheless, the Pesciara–Monte Postale fauna is the mostdiverse assemblage of articulated chondrichthyans known fromthe Cenozoic. Batoids are represented by rhinobatids, narcinids,platyrhinids, dasyatids, myliobatids and urolophids. Sharks includecarchariniforms and a lamniform known only from teeth.Chimaeroids are represented by a single isolated fin-spinebelonging to the genus Ischyodus (Marramà et al. 2017a).Extensive soft-tissue preservation in sharks visualized usingultraviolet light (Fanti et al. 2016) indicates potential forsubstantially more anatomical detail than available in historicalaccounts (Fig. 5).

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 RomanEmpire 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 aVeronese 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 tomodern 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 inNouveau Dictionnaire d’Histoire naturelle, and later by Louis Agassiz, who reviewedVolta’s identifications (Agassiz 1835) and provided further descriptions in his monumental Recherches sur les Poissons fossiles (Agassiz 1833–1844). The firstdetailed 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 anassassination attempt in 1853; material at the Natural HistoryMuseum, London, derives largely from the purchased collections ofWilliamWilloughby Cole, 3rd Earlof Enniskillen, and Sir Philip de Malpas Grey Egerton in the late 1800s; Bolca specimens at the Carnegie Museum of Natural History, Pittsburgh, were acquired in1903 from the Belgian Baron de Bayet, executive secretary to King Leopold II. Fossils from Pesciara–Monte Postale are otherwise found in numerous smallercollections 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 Berybolcensisleptacanthus, MCSNV T.177 (top), with historical illustration from Ceruti & Chiocco (1622) (bottom). (b) One of two galleries dedicated to thedisplay of fossil fishes from Bolca in the museum of Giovanni Battista Gazola.

The Eocene Bolca Lagerstätten

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Non-acanthomorph ray-finned fishes

Roughly 30 species constitute the non-acanthomorph ray-finnedfishes of Pesciara–Monte Postale. These include late-survivingpycnodonts, deep-bodied neopterygians abundant during theMesozoic (Blot 1987; Fig. 4b). Other Mesozoic elements includePlatinx, the last known member of Crossognathiformes, an earlydiverging teleost clade (Arratia & Tischlinger 2010; Sferco et al.2015). No fewer than nine families of eels represent Elopomorpha(Blot 1978), and are joined by three osteoglossomorph species.The latter are noteworthy as extant examples are freshwater,although several taxa are known from marine deposits in thePaleogene (e.g. Bonde 2008). The most common fish specimensfound in the Bolca Lagerstätten (Landini & Sorbini 1996, table 1),clupeomorphs have only recently been studied in detail (e.g.Marramà & Carnevale 2015a,b, 2016; Fig. 4c). Ostariophysans, adominant group of primarily freshwater fishes, include theanatomically primitive Chanoides (Patterson 1984). No ‘prota-canthopterygians’, stomiiforms (dragonfishes) or myctophiforms(lanternfishes) are known, and aulopiforms (lizardfishes and kin)are represented by a single species (Marramà & Carnevale 2017;Fig. 4d).

Acanthomorphs

Taxonomically, the ichthyofauna is dominated by spiny-rayedteleosts, or acanthomorphs (Fig. 4e–l). Non-percomorphs fromBolca include lampridiforms, a zeiform and holocentroids(Carnevale et al. 2014; Davesne et al. 2017). Percomorphsmake up the vast majority of fish species from the BolcaLagerstätten, and include familiar inhabitants of modern reefs:apogonids (cardinalfishes), acanthurids (surgeonfishes), caran-gids ( jacks), syngnathiforms (pipefishes and allies), labrids(wrasses), tetraodontiforms (pufferfishes and allies), ephippids(spadefishes), sphyraenids (barracudas), lophiiforms (anglerfishes),

pleuronectiforms (flatfishes), siganids (rabbitfishes), scatophagids(scatties), priacanthids (bigeyes), sparids (porgies), lutjanids(snappers) and pomacentrids (damselfishes). Joining these taxaare groups associated with more open-water habitats, includingbeloniforms (halfbeaks and flying fishes), scombrids (tunas andmackerels), xiphioids (billfishes) and palaeorhynchids (an extinctbillfish group), as well as several groups of uncertain relationshipsto modern lineages (e.g. exelliids).

Terrestrial vertebrates

Reptiles

A turtle and two genera of boid snakes are known from Pesciara(Carnevale et al. 2014). Reptiles are more common at Purga diBolca, and include crocodiles in need of taxonomic revision, asnake and two genera of freshwater turtles (Giusberti et al. 2014a).

Birds

Birds are limited to isolated feathers from Pesciara. Whereabouts ofskeletal remains reported in historical accounts are unknown(Carnevale et al. 2014).

Taphonomy

Fossils from Pesciara–Monte Postale, particularly the fishes, areusually found as part and counterpart with complete squamation,traces of pigmentation and phosphatized soft tissues (e.g. Wilby &Briggs 1997; Fig. 5). Controlled excavations carried out in Pesciaraand Monte Postale show that preservation and abundance of fossilsdiffer between the two sites as a consequence of contrastingdepositional environments (Marramà et al. 2016a).

Exceptionally preserved fossils are abundant in the finelylaminated micritic limestone of Pesciara, where they constitute the

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, MCSNVi.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 diGeoscienze e Georisorse, CNR, Padova); invertebrates, R. Zorzin (MCSNV).

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vast majority of the collected specimens. The current taphonomicmodel for fishes invokes rapid accumulation of corpses on an anoxicbottom, where a well-developed microbial biofilm delayed theirdecomposition, protected them from scavengers and bottomcurrents, and promoted rapid mineralization. Tetany exhibited bynumerous fish specimens (e.g. Fig. 4c) suggests that toxic algal

blooms might represent one of the main causes of death of marineorganisms from Pesciara (Marramà et al. 2016a).

Most fossils from Monte Postale are incomplete or stronglydisarticulated (c. 90% of fish specimens) to the degree that theycannot be identified at genus or species level. This incompletenessand disarticulation, as well as the disruption of fins, S-shaped

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 OR37227; (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 unclearaffinities Ceratoichthys pinnatiformis, MCSNV T.950; (h) the cornetfish Urosphen dubia, NHMUK PV P 15638; (i) the batfish Eoplatax papilio, MCSNVI.G. 24573; ( j) the mackerel Godsilia lanceolata, MCSNV T.89; (k) the monkfish Caruso brachysomus, MNHN BOL 42; (l) the triggerfish relativeProtobalistum imperiale, MCSNV T.21. Scale bars represent 50 mm.

The Eocene Bolca Lagerstätten

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curving of the vertebral column and the unidirectional dispersion ofscales around the body are indicative of episodic disturbance andmixing of the bottom. These occasional events resulted in thedevelopment of normal aerobic conditions on the bottom thateventually allowed the settling of a moderately diverse benthicfauna, revealed by relatively abundant bioturbation tracks andcrustacean and mollusc remains (Marramà et al. 2016a).

Palaeoenvironment

The differences in taphonomy and of the fish assemblagesthemselves suggest different palaeoenvironmental settings for thetwo principal Bolca localities. Landini & Sorbini (1996) hypothe-sized that deposition of the laminated limestone of Pesciara occurred

in a silled depression with restricted bottom circulation, a shortdistance from the coast at a depth of many tens of metres. Accordingto those researchers, coral reefs and seagrass beds were present inclose proximity. Based on an integrative approach using faciesanalysis and foraminiferal palaeoecology, Papazzoni & Trevisani(2006) proposed deposition in a subtropical lagoon close to anemerged area and characterized by seasonal changes of watercirculation that modulated oxygen concentrations near the seafloor.What is agreed upon by all the recent studies is that sediments ofPesciara reflect a peri-reefal system subject to the ecologicalinfluence of both coastal environments and the open sea, and thatthe deposition of the fossiliferous micritic limestone took place in alow-energy basin characterized by permanent bottom dysoxia oranoxia (Marramà et al. 2016a). Sometimes conspicuous primaryproduction was dominated by diatoms (Schwark et al. 2009), whichconstituted the base of the trophic chain of the Pesciara assemblageand sustained large shoals of the sardine Bolcaichthys catopygop-terus (Marramà & Carnevale 2015a).

Roughly half of fossil specimens from the laminated wackestoneof Monte Postale are remains of algae and plants, followed by fishes(about 30%) showing different degrees of completeness, andabundant invertebrates (corals, molluscs and crustaceans). Fishesprimarily consist of small epibenthic species and rarer large taxa(Marramà et al. 2016a). The laminated wackestone of Monte Postaleoriginated in a lagoon surrounded by coralgal buildups made ofcorals, calcareous algae and encrusting foraminifera (Vescogni et al.2016). The peri-reefal areas were densely vegetated by seagrass bedsand 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-associatedmarine ecosystems and adjacent terrestrial areas in the earlyCenozoic. As such, they are a unique line of evidence bearing onthe origin and early history of modern reefs, which represent majorhotspots of marine biodiversity. As a result of previous research, theimportance of the Bolca localities is clearest for fishes and derivesfrom three main features apart from excellent preservation: earlyEocene age, unique environmental setting and palaeogeographicallocation. With respect to age, the principal Bolca sites postdate theCretaceous–Paleogene (K–Pg) mass extinction by roughly 15 myr,providing a glimpse into a mature ecosystem following an intervalof evolutionary recovery (see Erwin 2001; Box 2, Fig. 6). Withrespect to environmental setting, Pesciara–Monte Postale showsubstantially higher species richness of fishes than, and contrastingtaxonomic composition to, other Ypresian deposits that can beconsidered Lagerstätten in their own right (Danata Formation,Turkmenistan; Fur Formation, Denmark; London Clay Formation,UK; Friedman et al. 2016); it is possible that this is due to closeassociation with reefs. With respect to palaeobiogeography, theBolca sites are ideally positioned for capturing a high-diversitymarine assemblage of Paleogene age. High species richness ofbenthic foraminifera, corals and molluscs in the late Eocene of thewestern Tethys, the area including Bolca, suggests that this regionwas an ancient biodiversity hotspot, comparable with today’s Indo-Pacific (Renema et al. 2008; Fig. 7a).

Modern coralgal reef ecosystems trace their origins to the earlyPaleogene (Kiessling 2009; Bellwood et al. 2017). Temporally, theBolca Lagerstätten fall near the end of a second wave of reefinvasions by modern teleosts as inferred on the basis of comparativephylogenetic data (Price et al. 2014), and their fauna is often hailedas the earliest modern reef-fish assemblage (Bellwood 1996;Bellwood & Wainwright 2002). Such comparisons are not withoutmerit, but there are differences from living reef faunas (Fig. 7b–d).Some major groups of reef-associated fishes such as butterflyfishes

Fig. 5. Examples of exceptional preservation of fossils from the BolcaLagerstätten. (a) Preservation of pigmentation (p), soft tissues and gutcontents in the triakid shark Galeorhinus cuvieri, Museo GeologicoGiovanni Capellini, Bologna (MGGC) 1976; specimen shown in rightlateral view and illuminated in ultraviolet light. Dashed-line rectangleindicates area shown in (b). (b) Close-up view of abdominal cavity ofspecimen in (a), including spiral valve of intestine (sv) and skeleton of thebarracuda Sphyraena bolcensis representing gut contents (gc). Imagescourtesy of T. Miyashita (University of Alberta). (c) Pigmentation patternsin the eel Paranguilla tigrina, Museo di Geologia e Paleontologia,Università degli Studi di Padova (MGP-PD) 26288; specimen shown inleft lateral view. Image courtesy of S. Castelli and L. Giusberti (MGP-PD). Scale bars: (a) 75 mm; (b) 25 mm; (c) 20 mm.

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and parrotfishes are not found at Pesciara–Monte Postale, and onlyappear later in the Cenozoic (Bellwood & Schultz 1988; Carnevale2006). Associated with the lack of some modern groups areremarkable examples of evolutionary convergence between Eoceneand extant reef fishes (Tyler&Bannikov 2005). Contrasts in terms ofdiversity of genus-level lineages within families, as well as relativeabundance of individuals within families, are also apparent

(Bellwood 1996; Bellwood et al. 2017; Fig. 7c). There arevarying degrees of overlap between fossils of the BolcaLagerstätten and their modern reef-dwelling relatives, as gaugedby geometric morphometric quantification of body shape (Bellwoodet al. 2014a; Marramà et al. 2016b), as well as differences inecomorphologically relevant traits such as eye size (Goatley et al.2010), mandibular mechanics (Bellwood 2003; Bellwood & Hoey

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 iscommensurate with their diversity in kind, with modern acanthomorphs assuming morphologies as divergent as those of flounders, seahorses, anglerfishes, tunas andmudskippers. The majority of acanthomorphs in turn belong to a group known as percomorphs, a species-rich radiation that has long vexed systematists as theunresolved ‘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 theirdebut tens of millions of years later, near the end of the Late Cretaceous, and belong to early diverging groups such as syngnathiforms, ophidiiforms and possiblybatrachoidiformes (Carnevale & Johnson 2015). Although some basal phylogenetic splits had clearly taken place by the Late Cretaceous, acanthomorphs remainedcomparatively 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 amongmarine fishes occurred at the end of the Cretaceous (Friedman 2009). Faunas of the earliest Cenozoic remainpoorly known, but largely include acanthomorph groups already known from the Late Cretaceous (Alvarado-Ortega et al. 2015; Adolfssen et al. 2017). A series ofdeposits from near or shortly after the Paleocene–Eocene Thermal Maximum in Europe and western Asia provide the first evidence of acanthomorph-dominatedfaunas 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 Postalepostdate the earliest of these assemblages by roughly 6 myr, and further mark the shift to percomorph-dominated marine fish faunas. Significantly, the Bolcalocalities capture the first (and in a few cases, only) body fossil occurrences of many reef-fish clades (Fig. 6). Increased taxonomic dominance of acanthomorphs inthe early Paleogene is associated with a substantial increase in morphological diversity as measured by overall body shape (Friedman 2010), although there is someevidence for an earlier onset of cranial diversification (Sallan & Friedman 2012). Pesciara and Monte Postale are unquestionably exceptional, but the pattern ofincreased anatomical diversity among acanthomorphs in the early Paleogene appears robust to the exclusion of these sites from quantitative analyses (Friedman2010).

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

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2004), jaw protrusion (Bellwood et al. 2015) and dentalmorphology(Bellwood et al. 2014b). Although commonly compared with Indo-Pacific assemblages on the basis of groups that are endemic to thismodern biodiversity hotspot, the Pesciara–Monte Postale fish faunais not strictly comparable with those of either the Atlantic or Indo-Pacific (Bellwood 1997; Fig. 7b). Taken together with otherlocalities, the Bolca sites provide a picture of a widespreadPaleogene marine fish fauna. At higher taxonomic levels (i.e.family), it is apparent that the Indo-Pacific region has maintainedmuch of this diversity, whereas Atlantic reef assemblages have beenwinnowed by regional extinction (Bellwood 1997).

Fossils from the Bolca Lagerstätten also deliver importantevidence relating to individual fish clades, especially in terms ofconstraints on times of evolutionary divergence and detailedcharacter data bearing on patterns of phenotypic evolution. Theoldest occurrences of many teleost families are from Pesciara–Monte Postale (Patterson 1993a,b; Fig. 6), and fishes from theselocalities serve as important temporal constraints for estimatingevolutionary timescales under a variety of approaches (e.g. Nearet al. 2012, 2013; Chen et al. 2014; Arcila et al. 2015; Close et al.2016; Bannikov et al. 2017). The impact of Pesciara–Monte Postaleon raw counts of teleost familial diversity through the Cenozoic isstriking, and suggestive of an extreme Lagerstätten effect (Patterson1994). Such obvious bias aside, the Bolca Lagerstätten and otherfossil deposits of similar age all record a major shift in marine fishassemblages between the Late Cretaceous and Paleogene, definedmost conspicuously by the increased taxonomic dominance ofacanthomorphs (spiny-rayed fishes) in general and percomorphs(perch-like fishes) in particular (Box 2).

To a first order of approximation, the Pesciara–Monte Postalefauna appears modern and there is much truth to the quip ofPatterson (1993a, p. 53) that subsequent evolution among marinefishes ‘was mere tinkering’ (Box 2). However, there are peculiarextinct phenotypes among otherwise familiar bodyplans. Theseinclude: early relatives of flatfishes indicating gradual, rather thansaltational, evolution of asymmetry (Friedman 2008, 2012), althoughthat stepwise change might have occurred over a geologically shortinterval (Harrington et al. 2016); early relatives of gymnodonttetraodontiforms (Tyler & Santini 2002) that provide clues to theevolutionary origin of the beak-like dentition further elaborated byliving members of the group (Fraser et al. 2012); the peculiar†Bajaichthys, a zeiform (John Dory) that shows an unprecedentedribbon-like morphology in a group otherwise characterized by deepbodies (Davesne et al. 2017); the extinct syngnathiform group†Aulorhamphidae, which combines the elongated snouts so charac-teristic of the order with generalized postcrania (Tyler 2004).

Summary

The Bolca Lagerstätten provide a unique window into a series offully marine to terrestrial environments in the early Eoceneof Tethys. Their remarkable diversity reflects a fortuitouscombination of taphonomic factors combined with a reef settingin a region interpreted as an ancient biodiversity hotspot. The mostcelebrated sites of the Bolca Lagerstätten are Pesciara and MontePostale, both of which yield exquisitely preserved fish fossilstotalling well over 200 species. The fossil fishes from these sites areparticularly significant in documenting the rise of acanthomorphs,

Fig. 7. The fossil fishes of the Bolca Lagerstätten represent an early coral reef assemblage. In panels comparing multiple localities, Bolca is represented bya 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–MontePostale ichthyofauna, based on taxonomic composition. Adapted from Bellwood (1997). (c) Differences between genus-level diversity within major extantreef-fish families in a modern rocky reef in the eastern Pacific (top) and Pesciara–Monte Postale (bottom). Other modern reef ecosystems show similarcontrasts to these Eocene sites. Adapted from Bellwood et al. (2017). (d) Morphological disparity (multivariate variance) of modern reef-fish faunas andthat of Pesciara–Monte Postale, assessed from a geometric morphometric analysis of body shape and fin position. Adapted from Marramà et al. (2016b).

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the dominant group of marine teleosts, as well as providing criticalclues to the early assembly of modern tropical reef ecosystems.Although they are often overshadowed by the fishes, a wide range ofmarine invertebrates, aquatic plants and algae, terrestrial plants andinsects are also present at Pesciara and Monte Postale. The marginalto terrestrial sites near Bolca remain little examined, and theirrelationship to the ‘classic’ localities remains unclear (Box 3).

Acknowledgements We thank P. Donoghue (University of Bristol) forhis invitation to write this review, and our many colleagues studying the fossilsand geology of the Bolca sites for their helpful input over the years. We especiallythank the Museo Civico di Storia Naturale, Verona, the Museo di Geologiae Paleontologia, Università degli Studi di Padova, Padua, Muséum nationald’Histoire naturelle, Paris, the Natural History Museum, London andNaturhistorisches Museum, Vienna for allowing us to photograph fossil fishesin their collections. C. Abraczinskas (University of Michigan Museum ofPaleontology) produced or improved the figures. A. Capobianco (University ofMichigan), D. Harper (University of Durham) and an anonymous refereeprovided helpful comments on an earlier version of this paper.

Scientific editing by Philip Donoghue

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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 andMonte 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 localitiesand 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 nearshoreto 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 from eachof the Bolca localities but subject to remarkably little targeted investigation over the past century. Third, although the fishes are without question the best knowntaxonomic component of the Bolca assemblage, it could be argued that they remain understudied relative to the amount of available material. This issue is more acutefor 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-tissuepreservation, and fine osteological details accessible through transfer preparation. New anatomical data for old fossils might help better constrain their phylogeneticpositions, a prerequisite for higher-level analyses addressing macroecological and macroevolutionary questions surrounding the origins of modern reef-fishassemblages and specific clades (Box 2).

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The Eocene Bolca Lagerstätten

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