Elizabeth M. Harper

The Mesozoic Marine Revolution

The modern oceans teem with animals which kill others to live, from killer whales that form pods of several individuals in co-ordinated attacks on their quarry (Pitman et al., 2001) to the drilling activities of tiny predatory foraminifers (Hallock et al., 1998). Most authors believe that predator-prey interactions, in tandem with competition, are key factorsS in controlling structure in modern communities. Classic work by Connell (1970) and Paine (1974) showed how predation in rocky shore communities prevented domination by major space occupiers and thus promoted overall diversity. In such situations taxa with antipredatory adaptations will be at an advantage and, if predation has been similarly important over geological time, we should anticipate that it has been an important agent of natural selection. Indeed, it is often suggested that the first appearance of shelled organisms in the “Cambrian explosion” might be due, in part, to the rise of predators (Conway Morris, 2001).

Investigating the Bivalve Tree of Life – an exemplar-based approach combining molecular and novel morphological characters

Abstract. To re-evaluate the relationships of the major bivalve lineages, we amassed detailed morpho-anatomical, ultrastructural and molecular sequence data for a targeted selection of exemplar bivalves spanning the phylogenetic diversity of the class. We included molecular data for 103 bivalve species (up to five markers) and also analysed a subset of taxa with four additional nuclear protein-encoding genes. Novel as well as historically employed morphological characters were explored, and we systematically disassembled widely used descriptors such as gill and stomach ‘types’. Phylogenetic analyses, conducted using parsimony direct optimisation and probabilistic methods on static alignments (maximum likelihood and Bayesian inference) of the molecular data, both alone and in combination with morphological characters, offer a robust test of bivalve relationships. A calibrated phylogeny also provided insights into the tempo of bivalve evolution. Finally, an analysis of the informativeness of morphological characters showed that sperm ultrastructure characters are among the best morphological features to diagnose bivalve clades, followed by characters of the shell, including its microstructure. Our study found support for monophyly of most broadly recognised higher bivalve taxa, although support was not uniform for Protobranchia. However, monophyly of the bivalves with protobranchiate gills was the best-supported hypothesis with incremental morphological and/or molecular sequence data. Autobranchia, Pteriomorphia, Heteroconchia, Palaeoheterodonta, Archiheterodonta, Euheterodonta, Anomalodesmata and Imparidentia new clade ( = Euheterodonta excluding Anomalodesmata) were recovered across analyses, irrespective of data treatment or analytical framework. Another clade supported by our analyses but not formally recognised in the literature includes Palaeoheterodonta and Archiheterodonta, which emerged under multiple analytical conditions. The origin and diversification of each of these major clades is Cambrian or Ordovician, except for Archiheterodonta, which diverged from Palaeoheterodonta during the Cambrian, but diversified during the Mesozoic. Although the radiation of some lineages was shifted towards the Palaeozoic (Pteriomorphia, Anomalodesmata), or presented a gap between origin and diversification (Archiheterodonta, Unionida), Imparidentia showed steady diversification through the Palaeozoic and Mesozoic. Finally, a classification system with six major monophyletic lineages is proposed to comprise modern Bivalvia: Protobranchia, Pteriomorphia, Palaeoheterodonta, Archiheterodonta, Anomalodesmata and Imparidentia.

Taphonomy and the Mesozoic marine revolution; preservation state masks the importance of boring predators

Exceptionally neomorphosed bivalves from a range of Jurassic sediments from England and North Ireland have been discovered to bear neat, circular, straight-sided boreholes over a millimeter in diameter. These boreholes appear to have been predatory in origin and are highly reminiscent of those produced by muricid gastropods. Although none of the known gastropod borers have stratigraphic ranges that extend into the Jurassic, it seems likely that other taxa, perhaps other gastropods, also possessed the ability to feed in this manner, thus extending the record of this type of predation by at least 90 million years. The frequency of boreholes recorded in Liassic bivalves from Blockley is as great as has been recorded in Tertiary and Recent malacofaunas that are assailed by predatory gastropods, thus indicating that these unknown predators were capable of exerting a substantial selection pressure on their prey. Recognition of Mesozoic predatory boreholes occurs only where shell preservation is particularly good. More usual moldic and castic preservation is incapable of recording borehole morphology and, thus, the presence of boreholes is overlooked in most faunas of this age. Consequently, the timing of the onset of this type of predation may be underestimated. The boreholes described in this paper probably do not represent the actions of the very earliest large, gastropod-like predators but they do have implications for further studies that seek to document the appearance of adaptations in prey taxa in response to this threat, and also indicate that taphonomy may affect evolutionary interpretations.

Assessing the importance of drilling predation over the Palaeozoic and Mesozoic

Abstract Plausible predatory Palaeozoic and Mesozoic drillholes have been reported in the literature from 62 localities, mainly from North America and Western Europe, most of which were discovered in the last 20 years. Twenty-nine of these reports include sufficient data to be statistically valid. Analyses of these data suggest that there was a highly significant increase in drillhole, and hence predator, size in the Early Devonian which may reflect a change in predatory taxa as part of the Mid-Palaeozoic marine revolution. In this study frequency of drillholes in particular species has been examined. Examination of drilling frequency suffered by individual taxa from a range of Palaeozoic and Mesozoic sites showing that these are highly variable, just as they are between different Holocene localities. Nevertheless, levels of up to 50% in the Palaeozoic and 40% in the Mesozoic suggest that, at least locally, drillers did exert an important selection pressure. Analysis of the currently available data set reveals no significant change in drilling frequency over the Palaeozoic and Mesozoic. There are fewer records of drilling predation from the Palaeozoic and Mesozoic than from the Cenozoic. At present, however, it is difficult to assess whether drilling was truly less widespread than in the Cenozoic or whether at least part of the problem is taphonomic loss of information, in particular in the Late Palaeozoic and Mesozoic. It is striking that relatively few reports involve molluscan prey, despite their attractiveness as profitable prey with high flesh yield when compared with the apparently more frequently drilled brachiopods. However, study of the style of preservation of drilled molluscs, that were mostly originally aragonitic, suggests that drillholes are only preserved in faunas which are exceptionally preserved such that the original microstructure is still observable. By contrast, brachiopods, which were either originally phosphatic or calcitic, have much better preservation potentials and therefore may be more likely to show drillholes. An understanding of the preservation biases involved in the recognition of drillholes may suggest suitable localities for further research. More data, from a suite of localities world-wide, are required for a more detailed analysis of patterns of drilling predation in the Palaeozoic and Mesozoic.

Pliocene climate and seasonality in North Atlantic shelf seas

This paper reviews North Atlantic shelf seas palaeoclimate during the interval 4–3 Ma, prior to and incorporating the ‘Mid-Pliocene warm period’ (ca 3.29–2.97 Ma). Fossil assemblages and stable isotope data demonstrate northwards extension of subtropical faunas along the coast of the Carolinas–Virginia (Yorktown and Duplin Formations) relative to the present day, suggesting a more vigorous Florida Current, with reduced seasonality and warm water extending north of Cape Hatteras (reconstructed annual range for Virginia 12–30°C). This interpretation supports conceptual models of increased meridional heat transport for the Pliocene. Sea temperatures for Florida (Lower Pinecrest Beds) were similar to or slightly cooler than (summers 25–27°C) today, and were probably influenced by seasonal upwelling of cold deep water. Reduced seasonality is also apparent in the Coralline Crag Formation of the southern North Sea, with ostracods suggesting winter sea temperatures of 10°C (modern 4°C). However, estimates from Pliocene bivalves (3.6–16.6°C) are similar to or cooler than the present day. This ‘mixed’ signal is problematic given warmer seas in the Carolinas–Virginia, and climate model and oceanographic data that show warmer seas in the ‘Mid-Pliocene’ eastern North Atlantic. This may be because the Coralline Crag Formation was deposited prior to peak Mid-Pliocene warmth.

Adult acclimation to combined temperature and pH stressors significantly enhances reproductive outcomes compared to short‐term exposures

This study examined the effects of long-term culture under altered conditions on the Antarctic sea urchin, Sterechinus neumayeri. Sterechinus neumayeri was cultured under the combined environmental stressors of lowered pH (-0.3 and -0.5 pH units) and increased temperature (+2 °C) for 2 years. This time-scale covered two full reproductive cycles in this species and analyses included studies on both adult metabolism and larval development. Adults took at least 6-8 months to acclimate to the altered conditions, but beyond this, there was no detectable effect of temperature or pH. Animals were spawned after 6 and 17 months exposure to altered conditions, with markedly different outcomes. At 6 months, the percentage hatching and larval survival rates were greatest in the animals kept at 0 °C under current pH conditions, whilst those under lowered pH and +2 °C performed significantly less well. After 17 months, performance was not significantly different across treatments, including controls. However, under the altered conditions urchins produced larger eggs compared with control animals. These data show that under long-term culture adult S. neumayeri appear to acclimate their metabolic and reproductive physiology to the combined stressors of altered pH and increased temperature, with relatively little measureable effect. They also emphasize the importance of long-term studies in evaluating effects of altered pH, particularly in slow developing marine species with long gonad maturation times, as the effects of altered conditions cannot be accurately evaluated unless gonads have fully matured under the new conditions.

Phylogenetic analysis of four nuclear protein-encoding genes largely corroborates the traditional classification of Bivalvia (Mollusca)

Revived interest in molluscan phylogeny has resulted in a torrent of molecular sequence data from phylogenetic, mitogenomic, and phylogenomic studies. Despite recent progress, basal relationships of the class Bivalvia remain contentious, owing to conflicting morphological and molecular hypotheses. Marked incongruity of phylogenetic signal in datasets heavily represented by nuclear ribosomal genes versus mitochondrial genes has also impeded consensus on the type of molecular data best suited for investigating bivalve relationships. To arbitrate conflicting phylogenetic hypotheses, we evaluated the utility of four nuclear protein-encoding genes-ATP synthase β, elongation factor-1α, myosin heavy chain type II, and RNA polymerase II-for resolving the basal relationships of Bivalvia. We sampled all five major lineages of bivalves (Archiheterodonta, Euheterodonta [including Anomalodesmata], Palaeoheterodonta, Protobranchia, and Pteriomorphia) and inferred relationships using maximum likelihood and Bayesian approaches. To investigate the robustness of the phylogenetic signal embedded in the data, we implemented additional datasets wherein length variability and/or third codon positions were eliminated. Results obtained include (a) the clade (Nuculanida+Opponobranchia), i.e., the traditionally defined Protobranchia; (b) the monophyly of Pteriomorphia; (c) the clade (Archiheterodonta+Palaeoheterodonta); (d) the monophyly of the traditionally defined Euheterodonta (including Anomalodesmata); and (e) the monophyly of Heteroconchia, i.e., (Palaeoheterodonta+Archiheterodonta+Euheterodonta). The stability of the basal tree topology to dataset manipulation is indicative of signal robustness in these four genes. The inferred tree topology corresponds closely to those obtained by datasets dominated by nuclear ribosomal genes (18S rRNA and 28S rRNA), controverting recent taxonomic actions based solely upon mitochondrial gene phylogenies.

The unusual mineral vaterite in shells of the freshwater bivalve Corbicula fluminea from the UK

Asian clams (Corbicula fluminea) with abnormally thickened shell valves were found in four rivers in the UK (Rivers Yare, Waveney, Thames and New Bedford River). The material making up these malformations was the rare calcium carbonate polymorph vaterite. Vaterite is seldom found in the natural environment because it is less stable than the other calcium carbonate polymorphs (aragonite and calcite). In the few reported cases of vaterite formation in molluscs, it is usually related to unusual biomineralisation events such as shell regeneration, pearls and initial stages of shell formation. We compared two populations from the Rivers Yare and Waveney in the Norfolk Broads, UK, one (River Waveney) displaying dominantly the normal Corbicula shell form with aragonitic shells. In the River Yare population, all individuals sampled had shell deformations to different extents. These deformations were apparent as bulges on the inside of the ventral shell margin. X-ray diffraction confirmed that the shell material in the bulges of recently collected clams was vaterite. Other parts of the deformed shells were aragonitic. The shell deformations alter the shell morphology, leading to higher and wider shells. The shell microstructure is fibrous in the vateritic parts and crossed-lamellar in the aragonitic parts of deformed or non-deformed shells. The cause for the malformations is probably a disrupted biomineralisation process in the bivalves. Fossil Corbicula specimens from the late Pleistocene had similar deformations, suggesting that this is not a response to anthropogenic causes, such as pollution.

Iceberg Scour and Shell Damage in the Antarctic Bivalve Laternula elliptica

We document differences in shell damage and shell thickness in a bivalve mollusc (Laternula elliptica) from seven sites around Antarctica with differing exposures to ice movement. These range from 60% of the sea bed impacted by ice per year (Hangar Cove, Antarctic Peninsula) to those protected by virtually permanent sea ice cover (McMurdo Sound). Patterns of shell damage consistent with blunt force trauma were observed in populations where ice scour frequently occurs; damage repair frequencies and the thickness of shells correlated positively with the frequency of iceberg scour at the different sites with the highest repair rates and thicker shells at Hangar Cove (74.2% of animals damaged) compared to the other less impacted sites (less than 10% at McMurdo Sound). Genetic analysis of population structure using Amplified Fragment Length Polymorphisms (AFLPs) revealed no genetic differences between the two sites showing the greatest difference in shell morphology and repair rates. Taken together, our results suggest that L. elliptica exhibits considerable phenotypic plasticity in response to geographic variation in physical disturbance.

Drilling and chipping patterns of bivalve prey shell penetration by Hexaplex trunculus (Mollusca: Gastropoda: Muricidae)

The predatory caenogastropod Hexaplex trunculus employed different methods to access different species of bivalve prey characterized by different shell thicknesses. Hexaplex trunculus drilled Callista chione and Venus verrucosa at their shell margins but the latter species also laterally. It also attempted to drill two species of Tapes but successfully penetrated these only after chipping the shell margin. Chipping, whereby a labral spine is forcibly pushed between the preys valves, especially posteriorly, to break them followed by proboscis insertion, was typically applied to access the thinner shelled prey Cerastoderma glaucum whereas Modiolus barbatus and Mytilus galloprovincialis were either chipped or drilled. The pattern of M. galloprovincialis shell penetration appears related to predator and prey size. Small (40 mm shell height) H. trunculus tended to drill rather than marginally chip M. galloprovincialis. Medium sized (55 mm shell height) H. trunculus either chipped or drilled M. galloprovincialis in approximately equal proportions but also at the valve margin. Larger (70 mm shell height) H. trunculus tended to laterally drill average sized (35 mm shell length) and the biggest (65 mm shell length) M. galloprovincialis. When larger M. galloprovincialis are attacked it thus becomes increasingly more difficult for H. trunculus to chip and drill the shell margin, possibly because the periostracum is thicker here in such individuals, and the predator resorts to lateral drilling. This is possible because as the mytilid ages its surface periostracum becomes progressively eroded and thus thinner and easier to access. Scanning electron microscopy (SEM) identified shell microstructure damage which shows that the chipping and drilling behaviours of H. trunculus result from labral spine damage and dissolutional etching, respectively, rather than mechanical radula rasping. These observations have implications for the use of such predation marks to identify the predator taxon implicated from holes in either empty Recent shells or fossil material.