Drill holes in Australian Cainozoic brachiopods

The fossil record of drill holes in marine invertebrates has received a considerable amount of interest from paleontologists, primarily due to its importance for reconstructing the history of interactions between drilling predators and their prey. Such drill holes have been described in numerous studies of Paleozoic brachiopods but rarely in those focusing on brachiopods of the post-Paleozoic, a striking pattern given that in the late Mesozoic and Cainozoic drilling gastropods diversified and frequencies of drilled molluscs increased dramatically. During the past several years, however, drilled brachiopods were reported in several studies of the Mesozoic and Cainozoic, suggesting that this phenomenon may be more common than has been previously assumed. Here we report on 10 genera of brachiopods from four Cainozoic basins in Australia of which 7 shows evidence of having been drilled by predators. Of 298 specimens examined, 38 contain a single complete hole. Drilled specimens were identified in all 4 basins and in all stratigraphic units. When considered in the context of recent reports of drilled Cainozoic brachiopods, these Australian brachiopods further imply that drilling predation on these invertebrates was geographically, taxonomically and temporally widespread.     

High frequency of drill holes in brachiopods from the Pliocene of Algeria and its ecological implications

The fossil record holds a wealth of ecological data, including data on biotic interactions. For example, holes in the skeletons of invertebrates produced by drilling activities of their enemies are widely used for exploring the intensity of such interactions through time because they are common and easily distinguished from non-biotic holes or holes produced by other types of interactions. Such drill holes have been described in numerous studies of Palaeozoic brachiopods but rarely in those focusing on brachiopods of the post-Palaeozoic, a striking pattern given that in the late Mesozoic and Cenozoic drilling gastropods diversified and frequencies of drilled molluscs increased dramatically. During the past several years, however, drilled brachiopods were reported in several studies of the Mesozoic and Cenozoic, suggesting that this phenomenon may be more common than has been previously assumed. Here we report on drilled brachiopods from a Pliocene locality in Algeria where 90 of 261 (34.5%) specimens of Megerlia truncata show evidence of predatory drilling. These data confirm that Cenozoic drilling frequencies of brachiopods may be locally high and, when taken together with other published data, that drilling frequencies are highly heterogeneous in space and time.     

Stereotypic and size-selective predation in Polinices pulchellus (Gastropoda: Naticidae) Risso 1826

Polinices pulchellus were size-selective in their choice of Cerastoderma edule. Large predators (12-15.9 mm shell length) selected both larger and a wider size range of cockles than smaller individuals (4-11.9 mm shell length). Considerable overlap occurred in the sizes of cockles frequently drilled by different size classes of snails, indicating that certain sizes of cockles may be most profitable to a wide range of predator sizes. Consumption rates were highest during July and August and were closely related to seawater temperature. Inner and outer drill hole diameters were both correlated with predator size, and the morphology of the drill hole was geometrically similar across a range of predator sizes. Polinices pulchellus showed no preference for either the left or right valve and drilled most cockles in the centre of the shell valve. The relationship between the distance of the drill hole from the umbo and prey size was unaffected by predator size, such that predators of different sizes were not found to drill cockles in different positions. When disturbed during drilling, incomplete drill holes were abandoned and, when drilling resumed, it occurred in new locations on the surface of the shell valve. The findings of this study highlight the stereotyped nature of drilling behaviour seen in the family Naticidae.     

Drilling under threat: An experimental assessment of the drilling behavior of Nucella lamellosa in the presence of a predator

Using the drilling muricid, Nucella lamellosa (Gmelin 1791) and its prey, the mussel Mytilus trossulus (Gould 1850), the impact of a secondary predator, the crab Cancer gracilis, on drilling was investigated experimentally. The frequency of incomplete holes was compared under two conditions: (1) when the gastropod's natural predator, C. gracilis, was present and (2) when it was absent. The results indicate that the presence of a secondary predator can affect drilling activity, leading to a significant increase in the frequency of incomplete drill holes. The introduction of a secondary predator can also decrease the overall drilling frequency. The size distributions of completely and incompletely drilled mussels suggest that in the presence of the secondary predator the decision by the gastropod to either abandon or continue drilling its prey might be influenced by how much time it has already invested into drilling or the size of the prey item. These results are important for the ecological and evolutionary implications of incomplete drill holes frequencies, especially with regard for their use as proxies for evolutionary prey improvement.     

Brachiopod morphology,life mode,and crushing predation in the Ordovician Arnheim Formation,Kentucky, USA

Predation on ancient shelled prey is an often-studied topic in paleoecology, but the early Paleozoic and the brachiopods that dominated the seafloor at that time are relatively underrepresented in the predation literature. We assessed predatory repair scar frequencies among the brachiopod genera from the Early Richmondian (Late Ordovician) Oregonia Member (Arnheim Formation) near Flemingsburg, Kentucky. We found higher repair frequencies on the concavo-convex Rafinesquina and Leptaena relative to the bi-convex genera. There were no trends in repair frequency through the stratigraphic section and no relationships between repair frequency and community diversity metrics. It is possible that concavo-convex brachiopods’ flat shape, thin shell profile, and free-lying (no pedicle attachment) lifestyle made them more likely or appealing targets of Ordovician crushing predators. It is also possible that concavo-convex brachiopods were better suited to survive crushing attacks than biconvex taxa. We also found differences in shell ornament that may influence the visibility of repair scars.     

Effect of durophagy on drilling predation: a case study of Cenozoic molluscs from North America

Drilling predation represents one of the most widely studied biotic interactions preserved in the fossil record, and complete and incomplete drill holes have been commonly used to explore spatial and temporal patterns of this phenomenon. While such patterns are generally viewed solely in terms of the interactions between predator and prey, they might also be affected by extrinsic ecological factors. Recent experiments have demonstrated that in the presence of a secondary predator (crab), the incomplete drilling frequency increases indicating increasing abandonment of the prey, and drilling frequency decreases implying a decrease in successful attacks. Here, we tested whether the effect of secondary predators on drilling frequencies can be detected in the fossil record. Using fossil molluscs from six Plio-Pleistocene localities, we found that repair scar frequencies, a proxy for activity of durophagous predators, correlate directly with incomplete drill hole frequencies and inversely with complete drill hole frequencies. These results suggest that the activity and success of drilling predators is influenced not just by the prey, but also by secondary predators.     

Traces of predation/parasitism recorded in Eocene brachiopods from the Castle Hayne Limestone,North Carolina,USA

Schimmel, M., Kowalewski, M. & Coffey, BP. 2011: Traces of predation/parasitism recorded in Eocene brachiopods from the Castle Hayne Limestone, North Carolina, USA. Lethaia, Vol. 45, pp. 274–289. The Castle Hayne Limestone (Middle Eocene, North Carolina), noted for its diverse macro‐invertebrate fossils, was sampled to assess if Early Cenozoic brachiopods from eastern North America record any traces of biotic interactions. Systematic surveys of two North Carolina quarries yielded 494 brachiopods dominated by one species: Plicatoria wilmingtonensis (Lyell and Sowerby, 1845). Despite subtle variations in taphonomy, taxonomy and drilling patterns, the two sampled quarries are remarkably similar in terms of quantitative and qualitative palaeoecological and taphonomic patterns. In both quarries, brachiopods contain frequent drillholes (24.5% specimens drilled). The majority of drillholes were singular, perpendicular to shell surface and drilled from the outside. Ventral valves were drilled slightly more frequently than dorsal ones, but site‐selectivity in drilhole location was not evident. Larger brachiopods were drilled significantly more frequently than smaller ones. However, drillhole diameter did not correlate with brachiopod size. The drillholes are interpreted as records of ‘live‐live’ biotic interactions, representing either predatory attacks or parasitic infestations or a combination of those two types of interactions. A notable fraction of specimens bear multiple drillholes, which is consistent with either parasitic nature of interactions or frequent failed predatory events. The high drilling frequency reported here reinforces other reports (from other continents and other epochs of the Cenozoic), which suggest that brachiopods may be an important prey or host of drilling organisms in some settings. The number of case studies reporting high frequencies of drilling in brachiopods is still limited and thus insufficient to draw reliable generalizations regarding the causes and consequences of these occasionally intense ecological interactions. □Brachiopods, drilling parasitism, drilling predation, Eocene, North Carolina, taphonomy.     

The post‐Palaeozoic fossil record of drilling predation on lingulide brachiopods

Research on drilling predation, one of the most studied biological interactions in the fossil record, has been concentrated on prey with calcareous skeletons (e.g. molluscs, echinoids, rhynchonelliform brachiopods). Based on a compilation of literature sources and surveys of paleontological collections of the Florida Museum of Natural History and the National Museum of Natural History, we provide a tentative evaluation of the post‐Palaeozoic history of drilling predation on the organophosphatic brachiopods of the family Lingulidae. Despite temporal, geographical and methodological limitations of the data assembled here, the results indicate that lingulide brachiopods have been subject to drilling predation since at least the Eocene. Variation in drilling frequencies at the locality level suggests that lingulides may occasionally experience somewhat elevated predation pressures from drilling organisms. Overall, however, drilling predation on lingulide brachiopods has been infrequent in the Cenozoic and may have been absent in the Mesozoic. The Mesozoic‐to‐Cenozoic increase in drilling frequencies on lingulides is similar to the trends observed in other marine benthic invertebrates and consistent with the hypothesis that predation pressures increased through time in marine ecosystems.     

Survival and repair of surgical and natural shell damage in the articulate brachiopod Terebratulina retusa (Linnaeus)

Living specimens of Terebratulina retusa from the Firth of Lorn, Scotland, were surgically damaged by drilling 2 mm diameter holes or narrow slits one cm long in the anterior portion of one valve, by bevelling the anterior margin of both valves, or by amputation of the anterior third of one valve. These injuries to the shell and mantle simulated the type of repaired shell damage seen in Paleozoic species, i.e., scalloped, divoted, cleft, and embayed valves. Less than ten percent of the 200 damaged specimens survived until the 25th week after surgery. Specimens of T. retusa showed the ability to repair drill holes, slits, and bevelled anterior shell regions, but not the most severe damage, i.e., amputations of the anterior third of one valve. Shell‐repair was initiated in the fourth week after surgery by the development of a membrane across the wound. The development of caeca in the new shell layer secreted to plug the drill holes became apparent by the eighth week. The punctate pattern was complete in the new, translucent shell material of bevelled and drilled specimens by the 25th week following surgery. Failure of any specimens to survive amputation of the anterior portion of a valve for more than seven weeks after surgery, and the absence of initiation of the repair process, suggests that terebratulids do not have the tolerance for, nor the ability to repair, the severe injuries (embayed valves) which were sustained and mended by extinct strophomenids.     

Pulling or drilling, does size or species matter? An experimental study of prey handling in Octopus dierythraeus ()

The influence of both predator and prey size on the shift from a pulling to a drilling predatory response was examined in the intertidal octopus Octopus dierythraeus, using an experimental program. Additionally, selective drilling, where particular regions of the prey are targeted, was examined for a variety of bivalve and gastropod prey. O. dierythraeus always initially attempted to pull bivalves apart. Shells that were eventually drilled were always subjected to significantly more pulling attempts than those that could be pulled apart, indicating that octopus are willing to expend more energy to access the flesh quickly. There was no defined threshold where bivalve size caused an octopus to switch from a pulling to a drilling response. Instead, there was a broad size range where the octopus could adopt either handling method and it varied for each individual. Octopus may only able to pull open bivalves before the molecular ratchet or ‘catch’ mechanism that many bivalves possess is engaged. This might explain the lack of a relationship between either octopus or bivalve size and the success of pulling, as it is likely that when the bivalves were presented to individual octopus they were either setting the ‘catch’ mechanism, or had already engaged it. O. dierythraeus demonstrated selective drilling on a variety of molluscan prey, with penetration sites differing between prey species. O. dierythraeus targeted the valve periphery, which was the thinnest part of the shell, therefore minimizing handling time. O. dierythraeus always drilled gastropods, but did not target the thinnest regions of the shells, with drill site varying according to the morphology of the prey. Elongate species with pronounced aperture lips were drilled in the apical region, close to the columella on the side of the opercula whereas nonelongate species were drilled immediately above the aperture. The location of drilling sites may represent a trade-off between targeting the most effective places to inject paralyzing secretions and the mechanically simplest places to drill.     

Predatory shell drilling by two species of Austroginella (Gastropoda: Marginellidae)

Predatory shell drilling of bivalve mollusc shells is reported for the gastropods Austroginella johnstoni and A. muscaria from south-eastern Australia. This is the first record of this feeding behaviour in the family Marginellidae. The drill holes are circular and paraboloid, with a small inner penetration hole. The corroded nature of the aragonite crystals within the drill holes suggests a chemical dissolution drilling mechanism. No obvious accessory boring organ was located. The gastropods have subepithelial gland cells in the proboscis, a pair of small salivary glands and a large foregut gland. The latter has a duct bypassing the valve of Leiblein and joining the anterior oesophagus.     

Reappraising the early evidence of durophagy and drilling predation in the fossil record: implications for escalation and the Cambrian Explosion

The Cambrian Explosion is arguably the most extreme example of a biological radiation preserved in the fossil record, and studies of Cambrian Lagerstätten have facilitated the exploration of many facets of this key evolutionary event. As predation was a major ecological driver behind the Explosion – particularly the radiation of biomineralising metazoans – the evidence for shell crushing (durophagy), drilling and puncturing predation in the Cambrian (and possibly the Ediacaran) is considered. Examples of durophagous predation on biomineralised taxa other than trilobites are apparently rare, reflecting predator preference, taphonomic and sampling biases, or simply lack of documentation. The oldest known example of durophagy is shell damage on the problematic taxon Mobergella holsti from the early Cambrian (possibly Terreneuvian) of Sweden. Using functional morphology to identify (or perhaps misidentify) durophagous predators is discussed, with emphasis on the toolkit used by Cambrian arthropods, specifically the radiodontan oral cone and the frontal and gnathobasic appendages of various taxa. Records of drill holes and possible puncture holes in Cambrian shells are mostly on brachiopods, but the lack of prey diversity may represent either a true biological signal or a result of various biases. The oldest drilled Cambrian shells occur in a variety of Terreneuvian‐aged taxa, but specimens of the ubiquitous Ediacaran shelly fossil Cloudina also show putative drilling traces. Knowledge on Cambrian shell drillers is sorely lacking and there is little evidence or consensus concerning the taxonomic groups that made the holes, which often leads to the suggestion of an unknown ‘soft bodied driller’. Useful methodologies for deciphering the identities and capabilities of shell drillers are outlined. Evidence for puncture holes in Cambrian shelly taxa is rare. Such holes are more jagged than drill holes and possibly made by a Cambrian ‘puncher’. The Cambrian arthropod Yohoia may have used its frontal appendages in a jack‐knifing manner, similar to Recent stomatopod crustaceans, to strike and puncture shells rapidly. Finally, Cambrian durophagous and shell‐drilling predation is considered in the context of escalation – an evolutionary process that, amongst other scenarios, involves predators (and other ‘enemies’) as the predominant agents of natural selection. The rapid increase in diversity and abundance of biomineralised shells during the early Cambrian is often attributed to escalation: enemies placed selective pressure on prey, forcing phenotypic responses in prey and, by extension, in predator groups over time. Unfortunately, few case studies illustrate long‐term patterns in shelly fossil morphologies that may reflect the influence of predation throughout the Cambrian. More studies on phenotypic change in hard‐shelled lineages are needed to convincingly illustrate escalation and the responses of prey during the Cambrian.     

Traces of Naticid Predation on the Gryphaeid Oyster Pycnodonte dissimilaris: Epifaunal Drilling of Prey in the Paleocene

Traces of drilling predation by naticid gastropods were observed on 51 valves of the free-lying, semi-infaunal oyster Pycnodonte dissimilaris (Gryphaeidae) from the Paleocene Hornerstown Formation, in New Jersey. Stereotypic behavior of the predator is indicated by the highly constrained placement of drill holes, 94% of which are centrally located on the oyster shells. Predator—prey mismatches in size, involving small predators that drilled through the upper valves of relatively large oysters, are documented by comparison of outer borehole diameter, as an index of predator size, with the sizes of the oyster shells. Results of this analysis suggest that at least some prey were drilled epifaunally, as they were too large to be manipulated and buried by the predator. This indicates, together with reports of epifaunal drilling by living naticids, that such behavior is geographically and stratigraphically more widespread in the Naticidae than has previously been acknowledged. This in turn suggests that epifaunal drilling of prey is a plesiomorphic, opportunistic mode of behavior, conserved in the evolution of the Naticidae, that has permitted subsequent escalation or expansion in range of naticid foraging from a more narrowly defined infaunal paradigm into exposed intertidal refugia.     

Ecologic stability of the dysaerobic biofacies during the Late Paleozoic

Late Paleozoic faunas found in sediments of dysaerobic origin represent a unique community type that remained essentially unchanged from the Middle Devonian to the Early Permian. This dysaerobic community had the following unique characteristics: (1) dominance by vagile molluscs, with suspension-feeding brachiopods, bryozoans, corals and echinoderms usually subordinate; (2) a trophic structure dominated by deposit feeders and carnivorous or scavenging cephalopods; (3) small body size as the result of high juvenile mortality and possibly stunting; and (4) preservation of most individuals as pyritic stein-kerns. All these characteristics are directly linked to the low oxygen levels of the dysaerobic environment. The relative stability of the deeper water, dysaerobic environment is consistent with Sanders' Stability-Time Hypothesis. The dysaerobic environment apparently offered a refuge for more archaic biotas that evolved in nearshore environments of the early Paleozoic.     

Substrate specific associations of epebionts on Middle Devonian brachiopods: Implications for paleoecology

A detailed study of over 2500 host brachiopods, from the Middle Devonian Hamilton Group of New York State, revealed distinct patterns of epibiont encrustation, that provide insight into taphonomy and paleoautecology of the host brachiopod shells and depositional environments. The concavo‐convex orthid, Tropidoleptus carinatus (Conrad), as well as strophomenid, and smooth athyrid brachiopods are among the most heavily encrusted. However, terebratulids of nearly identical size and shape are relatively clean of epibionts. This selective distribution strongly suggests that epibionts were discouraged from settling on punctate brachiopods. Brachiopods with small spines and frills were also nearly clean of epibionts, possibly because of entrapment of a mud layer, which made the outer layer of the host inhospitable for larval settling. Concavo‐convex taxa reveal high percent coverage and diversity of epibionts on the convex valve, which probably rested on the substrate during the life of brachiopod. This pattern is observed even on brachiopods that were buried with the convex valve downward. This implies complex post‐mortem histories involving multiple episodes of reorientation and colonization.     

Drill Holes and Predation Traces versus Abrasion-Induced Artifacts Revealed by Tumbling Experiments

Drill holes made by predators in prey shells are widely considered to be the most unambiguous bodies of evidence of predator-prey interactions in the fossil record. However, recognition of traces of predatory origin from those formed by abiotic factors still waits for a rigorous evaluation as a prerequisite to ascertain predation intensity through geologic time and to test macroevolutionary patterns. New experimental data from tumbling various extant shells demonstrate that abrasion may leave holes strongly resembling the traces produced by drilling predators. They typically represent singular, circular to oval penetrations perpendicular to the shell surface. These data provide an alternative explanation to the drilling predation hypothesis for the origin of holes recorded in fossil shells. Although various non-morphological criteria (evaluation of holes for non-random distribution) and morphometric studies (quantification of the drill hole shape) have been employed to separate biological from abiotic traces, these are probably insufficient to exclude abrasion artifacts, consequently leading to overestimate predation intensity. As a result, from now on, we must adopt more rigorous criteria to appropriately distinguish abrasion artifacts from drill holes, such as microstructural identification of micro-rasping traces.     

Stereotypic boring behaviour inferred from the earliest known octopod feeding traces: Early Eocene,southern England

Todd, JA. & Harper, EM. 2011: Stereotypic boring behaviour inferred from the earliest known octopod feeding traces: Early Eocene, southern England. Lethaia, Vol. 44, pp. 214–222. A bulk sample of 267 disarticulated valves of the bivalve Venericor clarendonensis (Wood) collected from the Lower Eocene London Clay (southern UK) yielded 38 individuals that had been perforated by small drill holes (0.70–2.14 mm in outer diameter). These drill holes had more or less circular plan views, with slightly irregular openings, and taper as they pass through the valve, conforming to the ichnotaxon Oichnus simplex Bromley. They show stereotypic positioning, being concentrated in the posterior region on the prey, moreover there is remarkable preference for perforating the sites of muscle attachment (principally the posterior adductor). We consider the most likely culprits to be octopods. As such these are the oldest octopod drill holes yet recorded. They provide the only evidence of these important top predators in this shallow marine community and also demonstrate that the sophisticated predatory behaviour shown by modern octopods had been evolved by at least the Early Eocene. □Eocene, octopod behaviour, Oichnus, stereotypic boring.     

Predation of late Marjuman (Cambrian) linguliformean brachiopods from the Deadwood Formation of South Dakota, USA

One hundred and twenty-five linguliformean brachiopods of late Marjuman (Cambrian) age with shell perforations, presumably caused by predation, were recovered from shallow-water limestones at two localities of the Deadwood Formation in the Black Hills of South Dakota, USA. Three-quarters of the perforated valves belonged to taxa in the order Acrotretida, while one-quarter of the specimens belonged to those of the order Lingulida. This is the first report of predation of fossil lingulids. In both orders there was a marked selection for valve type. Ninety-five per cent of all perforations of acrotretids were in the ventral valve, while 87% of all perforations of lingulids were in the dorsal valve. The highest rate of predation of collected acrotretids, at any stratigraphic horizon, was 22%, while the rate of predation of collected lingulids, at any given stratigraphic horizon, was as high as 9%. Half of the perforated valves had round holes with a sharp, non-beveled exterior edge, and half had irregularly shaped holes with chipped interior edges. The former type is attributed to either boring or a swift, piercing percussive strike, while the latter is attributed to a smashing percussive strike with a blunt appendage. A third type of perforation consisting of minute, roughly circular holes is thought to be too small to be the work of predators, and is assumed to be the result of an encrusting organism or parasite. The different types of perforation seen in the brachiopod valves indicate that there was more than one type of predator attacking them, including possibly one of the earliest durophages. Various hypothetical predators are suggested as potential candidates for causing the shell perforations. The criteria for their selection as possible linguliformean predators include possessing the ability to produce one of the two types of shell perforation, and being small enough to warrant preying on small (< 2 mm) brachiopods.     

Changes in the communities of Paleozoic brachiopods due to their development of their filtering system

Onward changes in the communities of Paleozoic articulated brachiopods were mainly connected with the improvement of the function of their filter feeding system, which is responsible for the feeding of animals. Three major routes of improvement are known: (1) feeding using a primitive lophophore and specialized mantle (orders Strophomenida, Chonetida, and Productida); (2) increased complexity and enlargement of the spirolophe and the appearance of the spiral brachidium (orders Atrypida, Spiriferida, and Athyridida); (3) development of the protective structures preventing ingestible particles into the inner cavity of the shell (order Rhynchonellida). The most effective was the third variant that allowed rhynchonellids, which appeared in the Ordovician, to live up to recently and survive after two largest extinctions in the history of the group development: in the Late Devonian and at the Permian-Triassic boundary.