Intense drilling in the Carboniferous brachiopod Cardiarina cordata Cooper, 1956

The brachiopod Cardiarina cordata, collected from a Late Pennsylvanian (Virgilian) limestone unit in Grapevine Canyon (Sacramento Mts., New Mexico), reveals frequent drillings: 32.7% (n = 400) of these small, invariably articulated specimens (<2 mm size) display small (<0.2 mm), round often beveled holes that are typically single and penetrate one valve of an articulated shell. The observed drilling frequency is comparable with frequencies observed in the Late Mesozoic and Cenozoic. The drilling organism displayed high valve and site selectivity, although the exact nature of the biotic interaction recorded by drill holes (parasitism vs. predation) cannot be established. In addition, prey/host size may have been an important factor in the selection of prey/host taxa by the predator/parasite. These results suggest that drilling interactions occasionally occurred at high (Cenozoic-like) frequencies in the Paleozoic. However, such anomalously high frequencies may have been restricted to small prey/host with small drill holes. Small drillings in C. cordata, and other Paleozoic brachiopods, may record a different guild of predators/parasites than the larger, but less common, drill holes previously documented for Paleozoic brachiopods, echinoderms, and mollusks.     

Predation on freshwater snails in Miocene Lake Steinheim: a trigger for intralacustrine evolution?

Shells of the freshwater gastropods Gyraulus trochiformis (Planorbidae or ramshorn snails) and Bania pseudoglobula (formerly Pseudamnicola, Hydrobiidae) from Miocene Steinheim Basin in SW Germany contain small holes with a mean diameter of 0.8 mm. Analyses of comparable holes are so far unknown from fossil or extant assemblages of freshwater shells. This analysis of the perforated shells suggests that the holes were not formed by post‐depositional or pure taphonomic processes. Instead, they were most likely produced by predators. This analysis widens the means for identification of predation on freshwater snail shells that can be used in other palaeolimnological studies. The co‐occurrence of fish teeth and perforated shells in the studied samples as well as the perforation features suggest that the predator was either barbel or tench fish. The correlation between shell sizes and hole diameters suggests a size relationship between predator and prey that may generally be related to gape‐limited fish predators. The co‐occurrence of perforated shells in these lake sediments with a dominance of large and armoured shells suggest that these larger shells with protuberances and knobs could not be crushed by the gape‐limited fish predators. This analysis is the basis for a hypothesis that the endemic evolution of Gyraulus in Lake Steinheim, with some varied forms of shell thickness and morphology, was triggered by a predator–prey relationship based on adaptations to avoid shell‐breaking predators.     

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.     

Morpho-anatomical differences of the Early Cambrian Chengjiang and Recent lingulids and their implications

Since the publication of Darwin's theory of evolution in 1859, lingulids have probably been the most widely quoted examples of arrested evolution. This, to some degree, may be because few anatomical features are impressed either on or inside valves so these may not adequately reflect the extent of change incurred during lingulid evolution. Two lingulid brachiopods, Lingulella chengjiangensis and Lingulellotreta malongensis, from the Early Cambrian Chengjiang Lagerstätte (Yunnan, South China) show preservation of a series of soft parts, notably the lophophores, setae mantle canals and perfectly impressed visceral region, which are vital to understanding the evolution and lifestyle of brachiopods. Analysis of the valve interiors favours the claim that an epifaunal mode of life could be a plesiomorphic state in contrast to the infaunal one of modern lingulids. Based on these fossils, the three‐pseudosiphon formation of setae found in Recent lingulids is proposed to be an apomorphy derived as an adaptation to an infaunal lifestyle. Comparison between the interior of the fossils with that of modern lingulids does little to support the widespread notion that the morphology of this lineage has remained remarkably constant since at least the early Palaeozoic.     

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.     

Latitudinal and depth gradients in marine predation pressure

Aim There is a general paradigm that marine predation pressure increases towards the tropics and decreases with depth. However, data demonstrating global trends are generally lacking. Rhynchonelliform brachiopods inhabit all the oceans and often survive shell‐crushing predator attacks. We investigate shell repair in brachiopods across a range of Southern Hemisphere and tropical Northern Hemisphere latitudes and depths. Location The Southern Hemisphere and tropical Northern Hemisphere. Methods We analysed the frequency of shell repair in 112 bulk samples, over 70% of which showed traces of shell damage and repair. Results The pattern of shell repair frequency (RF) was more complicated than the anticipated increase with decreasing latitude, with low levels at both polar and tropical sites but high levels at temperate latitudes. This pattern is only evident, however, in shallow water assemblages; and there is no latitudinal trend in water depths greater than 200 m, where shell RF is systematically low. There was a significant logarithmic relationship between RF and depth. Low polar repair rates reflect reduced predation pressure, directly supporting the global paradigm. Low rates in the tropics appears counter to the paradigm. However, tropical brachiopods are generally very small (micromorphic) in shallow water and below the minimum size at which damage is recorded anywhere. Main conclusions Predation pressure decreased logarithmically with depth. At shallow depths (< 200 m) RF showed its highest levels in the mid temperate latitudes with decreasing frequency towards both the tropics and the poles. Low levels of shell repair at high latitudes are likely to be due to a lack of crushing predators, but in the tropics it is suggested that the low frequency is a result of the small size of tropical brachiopods. We hypothesize that micromorphy in this region may be an outcome of high predation pressure.     

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.     

Epizoans on late Ordovician brachiopods from Southeastern Indiana

The frequency of epizoans (cornulitids, inarticulate brachiopods, bryozoans, solitary and colonial rugosan corals) on over 8000 specimens of articulate brachiopods (four strophomenids, five orthids, one rhynchonellid) was calculated for four stratigraphic horizons in the Dillsboro Formation of southeastern Indiana. Frequency of shells encrusted correlates significantly with the surface area of the valves. Punctae in brachiopod shells (Onniella meeki) may have deterred larval settlement of epizoans. Coarse ribbing on articulates deterred encrustation by the inarticulate brachiopod. The horn coral shows a preference for attachment to the anterior of Hiscobeccus capax. Bryozoans show a preference for the incurrent lateral margins of inferred living hosts, suggesting rheotropic behavior by settling larvae. Inarticulate brachiopods are concentrated around the sloping commissure of the brachial valve of strophomenids, suggesting geotropic behavior and/or selective survival of settling larvae. Inarticulates deterred overgrowth by bryozoans. High frequencies of encrustations of the medial region of pedicle valves of orthids and strophomenids probably reflect post‐mortem encrustations. Alternating intervals of slow sediment accumulation punctuated by tropical storms and rapid shell burial may account for the high frequency of shells with either their entire surface veneered or only a very small area encrusted by bryozoans.     

Evidence of predation damage in Pliocene Apletosia maxima (Brachiopoda)

Abstract:  Little is known about predation of Mesozoic and Cenozoic articulated brachiopods, but it is far from clear whether this is because they suffered very little predation pressure or because there have been few attempts to search for evidence of it. A study of 248 museum specimens of the large Pliocene terebratulid Apletosia maxima from the Coralline Crag (UK) has revealed that more than 16 per cent of them show evidence of having been attacked by predators. The styles of damage can be attributed to drilling muricid gastropods (most of which were successful) and failed crushing attacks probably by decapods. Brachiopods are usually thought to offer a poor tissue yield to potential predators, but in this instance it appears that A. maxima was attractive to predators even though they were living with a rich molluscan fauna. It is suggested that the mass of adductor and diductor muscles (likely to be spicule-free) of these particularly large brachiopods may have made them profitable. Further studies of post-Palaeozoic brachiopod faunas are required, particularly those from mixed shallow-water communities, before it can be established whether articulated brachiopods have or have not been driven into refugia by increasing predation pressure.     

Koskinoid perforations in brachiopod shells: function and mode of formation

Clusters of tiny perforations called 'koskinoid' have been interpreted as having accommodated byssus-like fibrils for attachment in Devonian Uncites and the Orthotetacea, which range from the Silurian through the Permian. The mode of formation of the tiny holes has inspired three hypotheses: (1) The fibrils protruded at the commissure and then were surrounded by growing shell. (2) The fibrils protruded from a juvenile foramen at the beak, which then was covered by shell that caused them to separate and migrate. (3) The fibrils penetrated their own shells like pedicles of living brachiopods are known to penetrate calcite. The first two hypotheses assume that the fibrils were produced by a rudimentary pedicle within the shell; the third postulates that the fibrils are diverticula from the outer epithelium of the mantle. The facts that the clusters are not confined to the beak region, but occur scattered over the ventral valve, and that they also penetrate the interara, favor the third theory. All Orthotetacea except Thecospira have the koskinoid perforations; all Davidsoniacea except Morinorhynchus lack them. This suggests that the two genera should trade places in the classification.     

Predation on artificial avian nests is higher in forests bordering small anthropogenic openings

Habitat edges alter the diversity of avian communities and are often associated with higher rates of nest predation. However, most previous studies on habitat edges have been conducted along long linear corridors or at the transition between large field and forest patches in agricultural systems. Less is known about predation rates when the habitat edge is the result of a small interior forest opening. We assessed predation rates on artificial nests mimicking ground and shrub nesters in Northern Michigan forests perforated by small clearings used previously for oil and gas extraction. Nests were placed at varying distances from the edges of these clearings, and in similar spatial arrangements within unfragmented interior forest plots. Predation rates increased in forests near edges, but significant impacts were limited to shrub nests. Markings on predated clay eggs indicated that the type of predation also differed. Scratch marks were the most prevalent egg indentation, but eggs with poked holes were twice as common near the forest edge. The increase in the number of poked eggs suggests that a higher density of avian predators occurred in forests near an edge. Predation rates at forest edges did not vary by distance from the forest edge. Surveys of the avian community revealed differences between edge and interior forests: American Crows Corvus brachyrhynchos and Blue Jays Cyanocitta cristata, two species known to predate bird nests, were more common near edges. Our results suggest that small forest openings alter the avian community and may adversely impact reproductive output in some species. If the alteration of these processes results in population‐level impacts, small forest perforations should be avoided when possible and reforestation of abandoned well‐pads should be encouraged.     

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.     

Predatory asteroids and the decline of the articulate brachiopods

Various causes, such as increased predation pressure, the lack of planktotrophic larvae, a 'resetting' of diversity, increased competition from benthic molluscs and the decline of the Palaeozoic fauna, have been suggested to explain the failure of the brachiopods to reradiate following the Permo-Triassic mass extinction. Increased predation pressure has hitherto appeared improbable, because typical predators of brachiopods, such as teleostean fish, brachyuran crabs and predatory gastropods, did not undergo major radiation until the late Mesozoic and early Cenozoic. However, new evidence strongly suggests that one important group of predators of shelly benthic organisms, the asteroids, underwent a major radiation at the beginning of the Mesozoic. Although asteroids appeared in the early Ordovician, they remained a minor element of the marine benthos during the Palaeozoic acme of the brachiopods. However, these early asteroids lacked four important requirements for active predation on a bivalved epifauna: muscular arms (evolved in the early Carboniferous); suckered tube feet, a flexible mouth frame and an eversible stomach (all evolved in the early Triassic). Thus radiation of the Subclass Neoasteroidea coincided with both their improved feeding capability and the decline of the articulates. The asteroids were the only group of predators of brachiopods that underwent a major adaptive radiation in the earliest Mesozoic. The asteroids may therefore have contributed to inhibiting a Mesozoic reradiation of the brachiopods. Epifaunal species lacking a muscular pedicle may have been particularly vulnerable. Unlike bivalve molluscs, modern brachiopods show only a limited range of adaptations to discourage asteroid predation. □ Asteroidea, Brachiopoda, evolution, predation, functional morphology.     

Patterns of shell penetration by Chorus giganteus juveniles (Gastropoda: Muricidae) on the mussel Semimytilus algosus

Patterns are described for shell penetration by the sublittoral muricid snail Chorus giganteus during predatory attacks on the mussel Semimytilus algosus. Location, form and size of shell penetrations were observed in relation to the size of the predator. The results suggested that positions of the perforations on the mussel shells were related to size of the attacking snail. Smaller snails perforated areas near the shell ligament and in the central zone of the shell, while larger snails more frequently attacked shell borders, principally on the ventral side. These observations may be related to: (a) changes in the process of manipulation of the prey during development of the foot and the shell tooth of the predator, (b) changes in internal structure of the snails related to the shell perforation mechanism, or (c) learned behavior acquired experientially by the snails during early growth. Although in other studies of muricid penetration patterns larger boreholes made in shells of the prey were positively correlated with increasing predator size, this relation did not appear to hold with C. giganteus, as larger specimens often made relatively small shell perforations. Areas of boreholes made in the mussel shells by this snail varied from 0.01 to 1.1 mm(2), and were unusually variable in size and shape, especially when compared with literature results on bores characteristic of other muricid species.     

Boring Late Cambrian organisms

Specimens of inarticulate brachiopods (family Acrotrctidae) with boreholes were found in Upper Cambrian carbonates in the southern Great Basin of the United States. Some morphologic features and preferred orientation of the borings are similar to those made by predators and previously reported in the fossil and Holocene record. Such predatory activity on brachiopods is previously unknown in Cambrian rocks. Taxa associated with these specimens are not known to have been predators and identity of the predatory organism is unknown. Cambrian brachiopods, predation, paleoecology.     

Traces of predation in the Cambrian

Series two marks a revolution in Cambrian predation when new predators and new predation methods appeared, which led to general increase in predation intensities and in the diversity of prey groups. The number of bored taxa and taxa with the predation scars is similar in the Cambrian. Most of the borings are associated with brachiopods and most of the scars with trilobites. Brachiopods, arthropods, molluscs, cnidarians and echinoderms were the most common prey in the Cambrian. The Cambrian record of predation is dominated by damage inflicted on brachiopods and trilobites. The fossils with predation signs are known from a majority of paleocontinents and all the Cambrian series.     

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.     

Predation by odonates depresses mosquito abundance in water-filled tree holes in Panama

In the lowland moist forest of Barro Colorado Island (BCI), Panama, larvae of four common species of odonates, a mosquito, and a tadpole are the major predators in water-filled tree holes. Mosquito larvae are their most common prey. Holes colonized naturally by predators and prey had lower densities of mosquitoes if odonates were present than if they were absent. Using artificial tree holes placed in the field, we tested the effects of odonates on their mosquito prey while controlling for the quantity and species of predator, hole volume, and nutrient input. In large and small holes with low nutrient input, odonates depressed the number of mosquitoes present and the number that survived to pupation. Increasing nutrient input (and consequently, mosquito abundance) to abnormally high levels dampened the effect of predation when odonates were relatively small. However, the predators grew faster with higher nutrients, and large larvae in all three genera reduced the number of mosquitoes surviving to pupation, even though the abundance of mosquito larvae remained high. Size-selective predation by the odonates is a likely explanation for this result; large mosquito larvae were less abundant in the predator treatment than in the controls. Because species assemblages were similar between natural and artificial tree holes, our results suggest that odonates are keystone species in tree holes on BCI, where they are the most common large predators. Received: 4 November 1996 / Accepted: 11 April 1997     

Chemico-structure of the organophosphatic shells of siphonotretide brachiopods

The organophosphatic shell of siphonotretide brachiopods is stratiform with orthodoxly secreted primary and secondary layers. The dominant apatitic constituents of the secondary layer are prismatic laths and rods arranged in monolayers (occasionally in cross-bladed successions), normally recrystallized as platy laminae. Sporadically distributed, interlaminar, lenticular chambers, containing apatitic meshes of laths and aggregates of plates and spherulites, probably represent degraded, localized exudations of glycosaminoglycans (GAGs) with dispersed apatite.
The shells of Helmersenia and Gorchakovia are perforated by canals with external depressions (antechambers) that possibly contained chitinous tubercles in vivo . The immature shell of Siphonotreta and most other siphonotretids is similarly perforated and pitted; but the mature part bears recumbent, rheomorphic, hollow spines that grew forward out of pits. Internally, spines pierce the shell as independent structures to terminate as pillars in GAGs chambers. Spines and pillars were probably secreted by collectives of specialized cells (acanthoblasts) within the mantle.
The shell of the oldest siphonotretide, Schizambon , is imperforate but the ventral valve has a pedicle foramen that lies forward of the posterior margin of the juvenile valve. This relationship characterizes all siphonotretides, suggesting that the pedicle, in vivo , originated within the ventral outer epithelium and not from the posterior body wall as in lingulides.     

Protegulum and brephic shell of the earliest organophosphatic brachiopods

Early development stages imprinted on the shells of Cambrian brachiopods from the class Linguliformea (orders Paterinida, Lingulida, Acrotretida) were studied with scanning electron microscope based on a large collection from the Siberian Platform. Some specimens of all three orders preserved protegulum (embryonic shell); their brephic (juvenile) shells, also were studied. Many of them might lack larval development stage as it is known for the recent representatives of the family Lingulidae. But unlike recent lingulids, the surface of the juvenile dorsal valves of all studied linguliformeans bore two (rarely three) pairs of gentle elevations accommodating bundles of setae, which sometime preserve as groups of fine imprints along their margins. Recent Lingula and Glottidia lack setae in this stage. On the other hand, recent classes Craniformea and Rhynchonelliformea have setae, but they develop in the larval stage. Most of brachiopod groups have the setae in the adult stage but these setae have different origin, are short, located on the lateral and anterior ends of the shell, and grow from the marginal cells of the mantle.