Ghosts of the Holobiont: Borings on a Miocene Turtle Carapace from the Pisco Formation (Peru) as Witnesses of Ancient Symbiosis

In spite of the widespread occurrence of epibiotic turtle barnacles (Coronuloidea: Chelonibiidae and Platylepadidae) on extant marine turtles (Chelonioidea: Cheloniidae and Dermochelyidae), and although the association between these cirripedes and their chelonian hosts has existed for more than 30 million years, only a few studies have investigated the deep past of this iconic symbiotic relationship on palaeontological grounds. We describe probable platylepadid attachment scars in the form of hemispherical/hemiellipsoidal borings on an Upper Miocene (Tortonian) fragmentary turtle carapace, identified herein as belonging to Cheloniidae, from the Pisco Lagerstätte (East Pisco Basin, southern Peru). When coupled with the available molecular data, this and other similar ichnofossils allow for hypothesising that platylepadid symbionts were hosted by sea turtles as early as in early Oligocene times and became relatively widespread during the subsequent Miocene epoch. Chelonian fossils that preserve evidence of colonisation by platylepadid epibionts in the form of pits on the turtle shell should be regarded as fossil holobionts, i.e., palaeontological witnesses of discrete communal ecological units formed by a basibiont and the associated symbionts (including the epibiota). A greater attention to the bone modifications that may be detected on fossil turtle bones is expected to contribute significantly to the emerging field of palaeosymbiology

The extinct nautiloid Aturia in the Middle Miocene of Pacific South America: new data from the Pisco Lagerstätte of Peru

We report on an aturiid (Cephalopoda: Nautiloidea) shell from the Pisco Formation, a Neogene marine sedimentary unit of the East Pisco Basin (southern Peru) that is widely known for its rich and exquisitely preserved marine vertebrate fossil content, including an outstanding cetacean assemblage. The studied specimen was collected from Middle Miocene strata exposed in the vicinity of Cerro Submarino. It consists of an internal mould of a phragmocone and is tentatively identified herein as belonging to the widespread, long-ranging species Aturia cubaensis. This fossil represents the first occurrence of Aturia in the Middle Miocene of the Pacific margin of South America; as such, it fills a gap in the chronostratigraphic distribution of the Southeastern Pacific finds of this genus, helping to bridge the Lower and Upper Miocene segments of its regional fossil record. The rarity of Aturia in the shelfal Cenozoic deposits of the East Pisco Basin may reflect the palaeoenvironmental habits of this extinct cephalopod genus, which may have lived in the upper bathyal zone, at about 250–350 m water depth. Despite recent suggestions that some extinct and extant marine mammal ecomorphotypes (including some odontocetes) were likely predators of nautiloids, there is no indication that any member of the diverse and abundant toothed whale faunas of the Pisco Formation exploited these shelled cephalopods as a relevant food source

THE EXTINCT NAUTILOID ATURIA FROM THE MIDDLE MIOCENE OF PACIFIC SOUTH AMERICA

We report on an aturiid (Cephalopoda: Nautiloidea) shell from the Pisco Formation, a Neogene marine sedimentary unit of the East Pisco Basin (southern Peru) that is broadly renowned for its rich and exquisitely preserved marine vertebrate fossil content, including an outstanding cetacean assemblage. This specimen was collected from Middle Miocene strata exposed in the vicinity of Cerro Submarino. It consists of an internal mould of a phragmocone and is tentatively identified herein as belonging to the widespread, long-ranging species Aturia cubaensis. This fossil represents the first occurrence of Aturia in the Middle Miocene of the Pacific margin of South America, and as such, it fills a gap in the chronostratigraphic distribution of the Southeastern Pacific finds of this genus, helping to bridge the Lower and Upper Miocene segments of its regional fossil record. The rarity of Aturia in the shelfal Cenozoic deposits of the East Pisco Basin may reflect the palaeoenvironmental habits of this extinct cephalopod genus, which may have lived in the upper bathyal zone, at about 250–350 m water depth. Despite some recent suggestions that some extinct and extant marine mammal ecomorphotypes (including some odontocetes) were likely predators of nautiloids, there is no indication that any member of the diverse and abundant toothed whale faunas of the Pisco Formation exploited these shelled cephalopods as a relevant food source

A puzzling occurrence of the bite mark ichnogenus Linichnus from the Lower Miocene Chilcatay Formation of Peru

An upper anterior tooth of Cosmopolitodus hastalis (Elasmobranchii: Lamnidae) from Burdigalian strata of the shallow-marine Chilcatay Formation exposed at Zamaca (East Pisco Basin, Peru) exhibits the remarkable occurrence of a serrated bite mark consistent with Linichnus serratus (Praedichnia: Machichnidae). In marine successions of Cenozoic age, traces belonging to the ich- nogenus Linichnus are typically found occurring on the bones of marine mammals and interpreted as due to predation or scavenging by sharks provided with smooth-edged (Linichnus bromleyi) or denticulated (L. serratus) teeth. Only a few fossil shark teeth exist preserving serrated bite marks, all of which have been interpreted as due to self-biting, which may occur when a shark loses a tooth while feeding and accidentally bites into it. Since C. hastalis is a smooth-toothed species, self-biting cannot explain our unusual find of L. serratus, which in turn may either reflect some kind of trophic interaction between large carnivorous sharks (with a late juvenile or young adult C. hastalis being fed upon by another elasmobranch, possibly a large-sized carcharhinid) or testify to accidental biting during multispecies shark scavenging on the carcass of a third organism that did not get preserved alongside the bitten tooth

Did the giant fossil shark Carcharocles megalodon eat small prey? Insights from bitten mammalian bones from the late Miocene of Peru.

Unlike bony fish, sharks are K-selected animals whose life history strategies generally include the use of protected nursery areas by young of the year and juveniles. Nursery areas can be primary (i.e., grounds where the sharks are born and spend the very first part of their lives) or secondary (i.e., grounds inhabited by slightly older but not yet adolescent or mature individuals). Criteria utilized to recognize and define these strategic habitats include: high concentration of young sharks, continuous or repeated use on various temporal scales, high food availability, and low predation risk. Since the fossil record of sharks is mainly composed of isolated teeth, identification of paleo-nurseries involves a series of problems due to difficult application of the above reported criteria. In fact, only four putative shark paleo-nurseries have been individuated to date: three of them regard lamniform sharks and were proposed on the basis of a few isolated small-sized teeth, whereas the fourth one comprises hybodontid and xenacanthid taxa and is testified by both selachian eggs and juvenile teeth. In the upper Miocene (Tortonian) deposits of the Pisco Formation exposed at Cerro Colorado (South Peru), a very rich shark tooth bearing level has recently been discovered. About 80% of the teeth collected from this level belong to the extant copper shark Carcharhinus brachyurus (Chondrichthyes: Carcharhinidae). These teeth are small-sized and compatible with extant individuals ranging from 80 cm to 210 cm in total length (i.e., immature and subadult copper sharks ranging in age between 4 and 16 years); adult teeth of C. brachyurus are in turn completely absent (although they are known from other Neogene deposits of Southeast Pacific, including a single site of the Pisco Formation). By analyzing the paleoenvironment of the Cerro Colorado shark tooth bearing level, we found that it meets the ecological criteria for individuating extant shark nurseries. The absence of very small-sized teeth (i.e., teeth referable to neonates and young of the year) allows us to hypothesize a secondary nursery ground inhabited by preadolescent copper sharks. The teeth size distribution of other chondrichthyan taxa (Lamniformes, Carcharhiniformes, and Myliobatiformes) that occur along with C. brachyurus put in evidence a significantly juvenile composition of the fossil shark assemblage, thus supporting the hypothesis of a communal use of the Cerro Colorado paleo-nursery by various mesopredator shark species. This study resulted in the identification of the first paleo-nursery for a carcharhiniform taxon, as well as in the first fossil shark nursery investigated with an ecology-based, actualistic approach

On the ecotrophic role of the giant Neogene shark Carcharocles megalodon: some notes from the Pisco Formation of Peru

The extinct otodontid shark species Carcharocles megalodon is known by giant serrated teeth and large vertebrae from Mio-Pliocene marine deposits worldwide. Reaching a total body length greater than 16 m, C. megalodon is regarded as an apex predator which likely occupied the top of the trophic chains of the Neogene global ocean. Despite C. megalodon being interpreted as a whale-eating predator, and its fossil remains being common in Neogene deposits worldwide, little direct evidence for the trophic ecology of this mega-toothed shark arose from the fossil record to date. We report on long and serrated shark bite marks attributed to C. megalodon affecting fossil mammalian bones collected from late Miocene shallow-marine deposits of the Pisco Formation exposed at Aguada de Lomas (South Peru). These occurrences, the first in their kind from the Southern Hemisphere, significantly expand the record of bite marks of C. megalodon; moreover, for the first time a prey of C. megalodon is identified at the specific level (as Piscobalaena nana, a diminutive member of the extinct mysticete family Cetotheriidae). Due to the fragmentary nature of the studied material, it was not possible to ascertain if the observed bite marks were due to scavenging or to active predation. Nevertheless, based on actualistic observations and size-based considerations, we propose that small-sized mysticetes (e.g., P. nana) could have been one of the target prey of adult C. megalodon. A predatory behavior somewhat similar to that of the great white shark attacking seals may be hypothesized for C. megalodon preying upon small mysticetes. We suggest that C. megalodon was a generalist apex predator whose trophic spectrum was still focussed on small-sized baleen whales. It is therefore interesting to observe that the extinction of C. megalodon (occurring at the end of Pliocene) roughly coincides with the the decline and fall of various lineages of small-sized baleen whales (including most Cetotheriidae). The disappearance of the last mega-toothed shark could thus have been triggered by the collapse of the archaic diminutive mysticetes (mostly inhabiting coastal upwelling-influenced waters of warm to temperate oceans) in favor of modern gigantic baleen whales (seasonally migrating to high latitude cold waters), the latter event being possibly driven by long-term planetary oceanographic and climatic changes

HOW OLD IS THE HUMBOLDT CURRENT SYSTEM?

Nowadays, about 20% of the world’s marine fish catch comes from the Peru-Chile area in the southeastern Pacific Ocean. The high productivity and biomass abundance of these waters reflect coastal upwelling in the framework of the Humboldt Current System (HCS). The latter includes surface and subsurface currents that bring deep, cold, nutrient-rich waters from Antarctica to Peru. Despite its ecological significance, the age and origin of the HCS remain poorly constrained. Here, we present a comprehensive review of previous works on the deep past of the HCS and coastal upwelling off Peru, with a special focus on the Cenozoic succession of the southern Peruvian Pisco Basin. The Paleogene biogenic portion of the basin fill indicates warm-water conditions for the middle Eocene and an incipit of coastal upwelling before the latest Eocene, hinting at the existence of a “proto-Humboldt current”. A late Eocene age is also attributed to the establishment of the Antarctic Circumpolar Current following the opening of the Drake Passage and Tasmanian Gateway. Although diatomaceous sediments have occurred since the late Eocene, the main diatom genera indicate seasonal rather than year-round upwelling. Warm/temperate taxa in the LowerMiddle Miocene, and paleotemperature estimates as well as diatom assemblages in the Upper Miocene point to a moderate upwelling during the Early-Middle Miocene that strengthened in Late Miocene times. Likewise, neodymium isotope ratios of fossil shark teeth show an overall Miocene-Pleistocene trend similar to that of the deep equatorial Pacific, with increasing contribution of Antarctic waters since ca. 6 Ma

A new barnacle (Cirripedia: Neobalanoformes) from the early Miocene of Peru: Palaeoecological and palaeobiogeographical implications

A new megabalanine barnacle, Austromegabalanus carrioli sp. nov., is described from lower Miocene strata of the Chilcatay Formation (East Pisco Basin, southern Peru). An assessment of the value of interlaminate figures in distinguishing species within the tribe Austromegabalanini from thin sections is provided– a useful identificationtool with fossil taxa such as the austromegabalanines, which are commonly found only as fragmented shells. The paper concludes with a reassessment of the palaeobiogeography and distribution patterns of the austromegabalanines, proposing a circumequatorial origin for this tribe

A new barnacle (Cirripedia: Neobalanoformes) from the early miocene of Peru: Palaeoecological and palaeobiogeographical implications

A new megabalanine barnacle, Austromegabalanus carrioli sp. nov., is described from lower Miocene strata of the Chilcatay Formation (East Pisco Basin, southern Peru). An assessment of the value of interlaminate f gures in distinguishing species within the tribe Austromegabalanini from thin sections is provided a useful identif cation tool with fossil taxa such as the austromegabalanines, which are commonly found only as fragmented shells. The paper concludes with a reassessment of the palaeobiogeography and distribution patterns of the austromegabalanines, proposing a circum-equatorial origin for this tribe

TOWARDS A PALAEOECOLOGICAL RECONSTRUCTION OF THE MIOCENE VERTEBRATE FAUNAS OF THE PISCO FORMATION (PERU): GLIMPSES INTO THE PAST OF THE HUMBOLDT CURRENT ECOSYSTEM

Flowing northwards along the western coast of South America, the Humboldt Current hosts extremely high levels of biological productivity all-year-round. With the aim of developing a deep-time investigation of this unique ecological setting, we provide the first synoptic overview of the palaeoecological habits of the fossil marine vertebrates of the Pisco Formation, a shallow-marine sedimentary unit of southern Peru that is renowned worldwide for its abundant and well-preserved Miocene fossil content. By building upon palaeontological data gathered on hundreds of fossils (including cetaceans, pinnipeds, seabirds, turtles, crocodiles, and bony and cartilaginous fishes), palaeoenvironmental conditions and palaeoecological relationships are thus reconstructed for the three sequences that comprise the Pisco Formation and their marine vertebrate assemblages. Some aspects of the Pisco palaeoecosystems are then investigated in detail, and similarities and differences are highlighted with respect to the present-day Humboldt Current Ecosystem and other extant Eastern Boundary upwelling systems. Like today, the southern Peruvian shelfal ecosystems witnessed by the Miocene Pisco strata were based on sardines, which are locally known from several fossils (including stomach contents). At the same time, they notably differed from their modern equivalent in being dominated by extremely large-bodied apex predators such as Livyatan melvillei and Carcharocles megalodon