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.     

Drilling predation on scaphopods and other molluscs from the Upper Cretaceous of Manitoba, Canada

Abundant information on drilling predation upon fossil bivalves, gastropods, and brachiopods has been accumulated during the past several decades, but very little is known about the predation on marine, infaunal carnivorous scaphopods. A survey of over 440 specimens of the scaphopod Dentalium gracile collected from the Upper Cretaceous Millwood Member (Campanian) of the Pierre Shale at a site near Russell, Manitoba displays a drilling percentage of approximately 35%. This figure is higher than previously reported for the scaphopods of similar age elsewhere, but is comparable to or lower than that of the sub-Holocene (34–61%). The difference in drilling percentage among different collections may be taxon-related or affected by the composition and structure of the fossil community. Morphologically, the drill-holes, produced by predatory drilling, are beveled with a countersunk profile of clean sharp edges. The drill-hole inner margin is ovate whereas the outer margin is nearly circular. Among the Manitoba specimens, drill-holes seem to be more common on the lateral side. Presumably due to the lack of effective defense strategy, the prey effectiveness is low (∼3.2%). There is no correlation between drill-hole dimension and scaphopod prey size, indicating that predator size does not correlate with the prey size. Nearly 480 specimens of cephalopods, pelecypods, and gastropods were also collected from the same community. There were only a total of 16 drill-holes on this additional material. Over 400 specimens of the only naticid Euspira obliquata were recovered from the same site and are believed to be the predators of the scaphopods and other molluscs. The low percentage (∼2.5%) of drilling on the abundant gastropod E. obliquata may indicate mistaken or opportunistic attacks by the predator, or that the cannibalism is not common in this community.     

Record of Naticid Predation on Scaphopods (Mollusca) from the Latest Maastrichtian of Rajahmundry,India

Drilling predation provides a rare opportunity to study and quantify prey-predator interactions in the fossil record. Records of drilling predation on scaphopod mollusc are rare. Here, we report naticid drilling predation on scaphopods from a “Turritelline-dominated assemblage” (TDA) stratigraphically just below the K-Pg boundary sections in Rajahmundry, India, which was situated in the Southern Hemisphere during that time. Low drilling frequency was found in the present assemblage based on 248 specimens, which was similar to most of the Cretaceous values previously reported. Majority of the specimens of previous studies were reported from higher latitudes in the Northern Hemisphere. Our report extended the palaeobiogeography of naticid predation on scaphopods into the Southern Hemisphere. Size and site stereotypy of drillholes on the scaphopod shell suggested that predatory behavior of naticids was already highly evolved, but evidence of escalation was less clear in scaphopod prey.     

Repair of gastropod drillholes in a platidiid brachiopod from Fiordland,New Zealand

Two morphologies of drillhole, probably attributable to gastropods, have been recognized in specimens of the small extant New Zealand platidiid brachiopod Neoaemula vector, collected from Fiordland, New Zealand. Some of these drillholes have been repaired, and these repairs occur in two different ways. The thin replacement shell has both primary and secondary layers and in some cases is punctate. Drillhole repair is virtually unknown among living brachiopods, but this may due to successfully repaired drillholes being classified as abandoned or incomplete.     

Microscopic evidence of serpulid affinities of the problematic fossil tube ‘Serpula’ etalensis from the Lower Jurassic of Germany

Tube structure, ultrastructure and mineralogy support serpulid affinities of the problematic worm fossil ‘Serpula’etalensis from the Lower Jurassic of Germany. The original tube mineralogy of ‘Serpula’etalensis is purely aragonitic and is preserved in Upper Pliensbachian specimens from eastern Germany. ‘Serpula’etalensis represent the earliest record of aragonitic mineralogy for serpulids. The tube is formed of irregularly oriented prismatic crystals that are 3–6 µm in length and 0.5–1.0 µm in diameter. Calcitic specimens of ‘Serpula’etalensis from Upper Sinemurian of southwestern Germany were recrystallized during the diagenesis and lack the original tube ultrastructure.     

Invasion of a naticid predator and associated changes in death assemblages of bivalve prey in northern Japan: implications for palaeoecological studies

The recent invasion of a naticid predator (Laguncula pulchella) and associated changes in the death assemblages of bivalve prey (Ruditapes philippinarum) provide a baseline for interpreting predator–prey interactions in the fossil record. This article presents quantitative data on size‐frequency distributions (SFDs) of living and death assemblages, prey size selectivity and drillhole site selectivity from the Tona Coast, northern Japan. Before the appearance of the predator, the SFD of the death assemblage exhibited a right‐skewed platykurtic distribution, and there were very few predatory drillholes. Once the predator appeared, frequencies of predatory drillholes increased, particularly in the smallest size class (2–10 mm shell length). Furthermore, juvenile peaks in the SFDs of death assemblages sharpened, and thus, SFDs exhibited strongly right‐skewed leptokurtic distributions. These changes suggest that intense naticid predation precluded juvenile clams from growing to adulthood, and thus, many dead shells of juvenile clams were introduced into the sediment. The changes in SFDs may also indicate intensification of predation pressure in the fossil record. No temporal shifts in prey size selectivity and drillhole site selectivity were noted, despite substantial changes in the demographics of Ruditapes philippinarum. This suggests that lack of specific size classes of preferred prey species is unlikely to be a primary factor accounting for size mismatches between predator and prey, because, in such situations, naticid predators probably attack other prey species. Therefore, such a factor is unlikely to primarily explain the less stereotypical predatory behaviour (i.e. low prey size selectivity and low drillhole site selectivity), which has been frequently recognized in fossil assemblages. Such less stereotypical predatory behaviour in fossil assemblages is likely to be explained by other factors, such as the existence of multiple predator taxa and lack of specific size classes of all available prey.     

Ultrastructure and mineral composition of serpulid tubes (Polychaeta,Annelida)

We have studied the tube ultrastructure of 44 recent species from 36 serpulid genera. Twelve distinct ultrastructures are identified. Serpulids possess very diverse tube ultrastructures, in contrast with the traditional point of view. Most species show single‐layered tubes, but 34% of these species have between two and four ultrastructurally different layers. Tubes are mostly bimineralic, and are composed of aragonite and calcite; however, one of the polymorphs is always dominant. All the studied single‐layered tubes with a lamello fibrillar tube ultrastructure are exclusively calcitic; prismatic structures, both in regular or irregular orientation, are either calcitic or aragonitic in composition. There is no correlation between tube mineralogy, and ultrastructure, and marine, brackish, and freshwater environments. We find that 47% of the serpulid species studied possess a unique combination of tube structure characters. © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154 , 633–650.     

Retreat site selection and social organization in captive electric fish, Apteronotus leptorhynchus

Gymnotiform fish use their electric organ discharge for electrolocation and communication. They are active nocturnally and seek retreat sites during the day. We examined retreat site selection in Apteronotus leptorhynchus by assessing their preference for retreat tubes that differed in opacity and dimension. Isolated fish preferred opaque to clear tubes, long and narrow diameter tubes to short, wide diameter tubes, and open-ended to closed tubes. We also assessed how groups of fish distributed themselves in tubes according to sex and electric organ discharge frequency under four conditions: (1) unlimited tube availability, (2) limited tube availability, (3) variation in tube opacity, and (4) variation in tube dimension. When tube availability was unlimited, fish generally preferred to occupy tubes alone. However, females, but not males, often cohabited tubes with consexuals. When tube availability was limited, females were more often than males found outside of tubes. When tubes varied by opacity and dimension, fish clustered most commonly in preferred tube types (opaque and long tubes). Males with the highest electric organ discharge frequencies usually occupied the most preferred tube type. Thus, fish have clear preferences in selecting retreat sites and groups of fish reveal their dominance relationships when presented with variation in retreat sites.     

Contribution to the revision of some late Callovian serpulids (Annelida, Polychaeta) of Central Russia: Part 2

This paper deals with the revision of the species of the genera Mucroserpula, Propomatoceros, and Spiraserpula (family Serpulidae) from the Upper Callovian of the locality Peski (Moscow Region). All taxa are described in accordance with the current classification of fossil serpulid tubes. Two new species are described: Propomatoceros barskovi sp. nov. and Spiraserpula oligospiralis sp. nov.     

Serpulids and other calcareous tube-dwelling encrusting polychaetes from the Early Cretaceous Agrio Formation (Neuquén Basin,Argentina)

Serpulids and other related tube-dwelling polychaetes are often ignored when found as fossil remains. They are, however, a widespread and important group today, and abundant literature has been published on them. Knowledge of fossil serpulids is centered on European material, and little has already been done on South American fossil calcareous tubes. In this paper, seven serpulid and sabellid morphotypes are described from the Early Cretaceous marine Agrio Formation of Argentina, revealing a diversity of worms recorded as encrusters on bivalves, ammonites and corals. Sabellids are represented by Glomerula cf. serpentina. Serpulids are represented by two subfamilies: “Serpulinae” includes Mucroserpula mucroserpula, Parsimonia antiquata, Placostegus cf. conchophilus, Propomatoceros semicostatus and P. sulcicarinatus; Spirorbinae is represented by heavily worn tiny coiled tubes assigned to ?Neomicrorbis. Serpulids and sabellids are one of the main components of the mollusk-encrusting fauna recorded in the Agrio Formation, along with small oysters but much more diverse. They are most commonly found as post-mortem encrusters, but some cases of unquestionable living interaction are also found, such as serpulid tubes embedded on coral branches. They are often overgrown by bryozoans, and sometimes by oysters; they frequently occur aggregated.     

Can Naticid Gastropod Predators Be Identified by the Holes They Drill?

We tested the hypothesis that drillholes made by different species of predatory naticid gastropods can be differentiated by variability in the inner (IBD) and outer borehole diameters (OBD) of the holes they drill. We compared two samples of Mya arenaria that were drilled by different predators, Euspira heros and Neverita duplicata, under experimental conditions. Mean IBD:OBD ratio was significantly greater for holes drilled by Euspira compared to Neverita, indicating that Euspira drills a steeper drillhole than Neverita. We also found consistent differences between the two naticids for slopes of regression lines of IBD on OBD after standardization for predator size and prey size and thickness, with slopes for Euspira being steeper, but results were not statistically significant. However, the range of IBD:OBD ratios was wide and overlapped considerably for each species, which decreases confidence in assignment of individual drillholes to a particular predator species. At least in the case of these two naticid species, interspecific differences in variation of the inner and outer diameters of the holes they drill have limited utility in identifying the maker of individual boring traces in the fossil record.     

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.     

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.     

Occurrence,Formation and Function of Organic Sheets in the Mineral Tube Structures of Serpulidae (Polychaeta,Annelida)

A scanning electron microscopy study of organic sheets in serpulid tube mineral structures was carried out to discern their function, formation and evolution. The organic sheets may have some taxonomic value in distinguishing the two major clades of serpulids previously identified. The organic sheets in the mineral tube structure occur only in certain taxa belonging to clade A, but not all species in clade A have them. Organic sheets are best developed in genus Spirobranchus. One could speculate that organic sheets have evolved as an adaption to further strengthen the mechanical properties of the tubes in clade A, which contains serpulids with the most advanced mineral tube microstructures. The organic sheets are presumably secreted with at least some mineral phase.     

Clumping behavior as a strategy against drilling predation: Implications for the fossil record

Drilling gastropod predators are of particular interest to paleontologists, because predatory drill-holes in marine invertebrates serve as one of the rare sources of data for the study of ancient predator-prey interactions. Modern laboratory studies are an important part of predation research providing valuable ecological insight and constraining fossil evidence and interpretations. Previous studies have shown that mussels use clumping behavior against durophagous predation [Okamura, B., 1986. Group living and the effects of spatial position in aggregations of Mylitus edulis. Oecologia 69, 341-347.; Lin, J., 1991. Predator-prey interactions between blue crabs and ribbed mussels living in clumps. Estuar. Coast. Shelf Sci. 32, 61-69.], but its role against drilling predation had not been explored. In this study, we explore the effect of clumping on predator success (drill-hole frequency) and prey handling (drill-hole position) using the mussel, Mytilus trossulus, as prey and the gastropod, Nucella lamellosa, as drilling predator. We assigned mussels to two groups: in one, mussels were allowed to clump together with their byssal threads, and in the other, they were kept separate. We observed a significant decrease in the drilling frequency within the group containing clumped mussels, confirming that clumping acts as a successful anti-predatory strategy against drilling predators. The use of clumping as an effective strategy against multiple types of predators may relax the trade-offs associated with aggregated lifestyles [Bertness, M.D., Grosholz, E., 1985. Population dynamics of the ribbed mussel, Geukensia demissa: the costs and benefits of an aggregated distribution. Oecologia 67, 192-204.]. The increased benefit and unchanged metabolic cost of clumped living alters estimates of individual fitness with evolutionarily significant implications (e.g., eliminating the need to invoke group or species selection to explain the adaptive benefit of an aggregated lifestyle). In spite of potential differences in prey handling and grappling due to clumping, mean drill-hole placement and variation in drill-hole placement showed no significant differences between the two groups. These observations suggest that comparison of predation intensities across clumping and non-clumping taxa must consider the anti-predatory effect of this behavior.     

Tempestitic shell beds formed by a new serpulid polychaete from the Bajocian (Middle Jurassic) of the Central High Atlas (Morocco)

Serpulid-dominated shell beds from the Lower Bajocian (Middle Jurassic) of the Central High Atlas (Morocco) are primarily formed by quadrangular tubes of the serpulid polychaete Nogrobs moroccensis sp. nov. The transverse tube ornament consisting predominately of wrinkles, the lack of narrow spirals and the shortness or absence of attached posterior tube portion represent the diagnostic features of this new species. Tubes of Nogrobs moroccensis co-occur with gastropods and oyster–crinoidal debris. We suggest that these serpulids were free-lying in their adult stage and formed benthic meadows on soft-bottom habitats. They frequently show parallel alignment in plane views in both graded and non-graded, few-cm-thick shell beds, corresponding to distal tempestites deposited close to and below storm wave base in an outer-ramp environment. The excellent preservation of serpulids implies short residence time on the seafloor, and the lack of compositional mixing with other communities and their restriction to outer-ramp habitats indicate that they represent parautochthonous assemblages. Analyses of serpulid orientation on the bottom bedding planes of shell beds revealed weak unidirectional arrangement of tubes, whereas orientation on the top bedding planes revealed strong unidirectional arrangement of tubes, with significantly different orientation relative to the bottom planes. This change could suggest a shift from predominantly a current component of the combined storm flow (with uneven seafloor surface and adhesion of skeletal grains to muddy substrate) to significant oscillatory component of the waning storm, as also suggested by bidirectional orientation of gastropods.     

Late Carboniferous hydrocarbon-seep carbonates from the glaciomarine Dwyka Group,southern Namibia

Limestone deposits with columnar to lenticular geometry (max. 3.2 m in height and 1.5 m in diameter) occur within the uppermost part of the Ganigobis Shale Member, a marine mudstone unit capping the second deglaciation sequence of the glaciomarine Dwyka Group in southern Namibia. The limestones mainly consist of four authigenic carbonate phases (microspar, banded/botryoidal cement, yellow calcite, spheroidal calcite). Extremely negative δ¹³C values (as low as ? 51‰ VPDB) indicate a hydrocarbon-derived origin of the carbonates with biogenic methane being the most likely carbon source. The limestones contain a low-diversity but high-abundance faunal assemblage of tubular fossils. These fossils closely resemble the tubes of modern and fossil seep-dwelling vestimentiferan tube worms in terms of size, shape, arrangement, and taphonomical patterns.     

Remarkably preserved annelid worms from the La Meseta Formation (Eocene), Seymour Island, Antarctica

Abstract: Worm tubes, which exhibit the replaced tube-lining membrane, have been collected from the lowermost Lower Eocene Acantilados Allomember of the La Meseta Formation, Seymour Island, Antarctica. The discovery represents the oldest examples of preservation of the tube-lining membrane of tube-dwelling Polychaeta in the fossil record. A new genus and species, Caprascolex antarcticus , are described. The specimens are preserved as thin coatings of amorphous iron oxide on the inner surface of the moulds interpreted to be the replaced tube-lining membrane. Examination of the rarely described tube-lining mucosoid membrane in extant polychaetes shows that the fossils are nearly identical in morphology and scale to extant forms. These fossils record in remarkable detail the morphology of the tube-lining membrane, which appears to be composed of growth bands formed as the worm constructed the tube. The tube-lining is believed to have been originally preserved as pyrite, with subsequent oxidation to iron oxide. The tube-lining membrane of worm tubes possibly is known from only one other fossil occurrence.     

Radiocarbon dating and metal analyses of `fossil' and living tubes of Protula (Annelida: Polychaeta)

Since the initiation of benthic and trawling studies in southern California over 50 years ago, empty calcareous tubes, measuring up to 36 cm in length and 2.1 cm in diameter, have been collected and presumed to belong to the serpulid genus Protula. ¹⁴C dating of these `fossil' tubes, ranged from 631 ±34 to 3987 ±42 yrs. In connection with monitoring programs, living specimens of Protula superba Moore, 1909 were collected from the benthos off southern California. A comparison of the elemental profile of the ancient and extant tubes was conducted to ascertain the effects of time and the recent increase in various anthropogenically mobilized metals on the incorporation of Al, As, Ba, Cd, Ce, Co, Cr, Fe, Mo, Ni, Pb, U, V and Zn in the calcareous tube. Surprisingly, inductively coupled plasma mass spectroscopy (ICP-MS) analysis of the digested tubes showed the concentrations of the elements were generally higher in `fossil' tubes than those obtained from living animals. However, the concentration of elements was higher in `fossil' tubes collected from the vicinity of municipal outfall discharges compared to `fossil' tubes collected from near an offshore island. Laser ablation ICP-MS analyses across transverse sections of `fossil' and living tubes showed spatial heterogeneity of elements in the structure. Elevated signals for Pb, Gd, Ce, La, Pr, Sm, Eu and Nd were observed on both internal and external surfaces on all tubes. Elevated responses for Fe, Zn, Sr, Mn, Tb, Dy, Ho, Er and Bi were primarily noted on the outer surfaces. It is hypothesized that the higher concentrations of metals in the `fossil' tubes may be the result of surface contamination facilitating elemental adsorption or substitution over the years. It is concluded that the use of biomineralized structures as biomonitors of water quality should involve rigorous chelating procedures to remove contaminating metals from lattice bound elements locked in the mineral matrix.