Bivalve and Gastropod shells in the Red Crag - further discussion

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BIVALVE AND GASTROPOD SHELLS IN THE RED CRAG – FURTHER DISCUSSION HOWARD MOTTRAM Opening remarks In last year’s journal I reviewed the types of calcium carbonate that occur in commonly found Red Crag bivalve and gastropod shells (Mottram, 2018). It may have seemed that the types of calcium carbonate varied somewhat randomly between and within taxonomic groups. However, when grouped by lifestyles, there was a logic as to how these molluscs exploited the different types of calcium carbonate relative to their needs.

Shell fabrication - aragonite or calcite?

We tend to think that aragonite is less resilient than calcite because it is unstable over time and it dissolves more readily, especially in very cold water and under high pressure. These physico-chemical limitations of aragonite were not problematic to the bivalves and gastropods because they had short life spans (usually less than 15 years) and, when the Red Crag sediments were deposited, the bivalves and gastropods were living within temperate latitudes in a shallow North Sea (i.e. not arctic and the water pressures at the sea-bed would have been relatively low).

Aragonite is actually slightly harder than calcite but what was important to the development and maintenance of the shells was how these different types of calcium carbonate behaved in their respective layers in the shell walls. Each layer was composed of either calcite or aragonite, never a heterogeneous mix, and the layers were built up from very thin sheets in which the crystals were laid down in particular styles from a range of possible crystal shapes and orientations. If a crack occurred in a shell then it was most likely to propagate ‘along, but not across, the grain’. In a simple situation, if elongate crystals in a sheet were aligned along the length of the sheet and in the next sheet they were aligned across the length of the sheet, the effects of cracks would have been minimised: this is the principle that makes plywood so effective. The arrangements of the sheets within the layers, helped by the tiny proportion of protein between the crystals, also gave the shell structure a little flexibility, i.e. reduced brittleness. Materials scientists have tested shells and found that the ways in which the shells have been built up makes shells over 1,000 times better at resisting crushing or stretching than single flawless crystals of calcite or aragonite. In practice, the possible shapes and orientations of aragonite crystals would have created even stronger sheets of building material than calcite would have done, e.g. Zhang et al., 2011, p.8683. When I refer to aragonite sheets as having been stronger than calcite sheets, this was in terms of resisting both squeezing (compression) and stretching (tension). Calcite may not have seemed the best option in respect of strength, but deposition of it would have been quicker and less demanding of an individual’s resources (Vermeij, 1993b, p.52). Therefore, calcite was also used, especially when the objective was to thicken the shell walls.

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Burrowing types The vast majority of Red Crag bivalves, and a few gastropods, burrowed into sand or mud to gain security. The pod razor (Ensis siliqua) had a thin shell but the risks posed by this were offset by burrowing deeply. Most burrowers lived below a shallower cover of sand or mud where they were still in some danger from probing predators and from being unearthed by stormy seas. Despite this, the tellins (Macoma obliqua and M. praetenuis) still had thin shells and it is not uncommon to find specimens that had been bored, presumably by predatory gastropods. Most other burrowing bivalves had sturdy shells e.g. the dog cockle (Glycimeris glycimeris), the soft-shell, or Ipswich, clam (Mya arenaria) and the true cockles (Cerastoderma angustatum, C. interuptum and C. parkinsoni). Perhaps, not too surprisingly, burrowers had shells that were constructed from the stronger option, aragonite.

Much less common overall, but they could be locally abundant, were the pholad bivalves that lived within harder substrates. When specific identification has been possible, it has usually been of the oval, or great, piddock (Zirfaea crispata). Young individuals used the spiky ornamentation on their shells to grind a way into the surface of underlying London Clay or Coralline Crag where they then enlarged the living area of their burrows as they grew, retaining only a narrow shaft to the surface through which they could not be pulled out. In these safe burrows, the shells of this specialist could afford to be thin but they still needed to have resilience. According to Bouillon, 1958, p.236, (relying on Stolkowsky, 1951), modern day pholad shells are constructed from aragonite with a trace of calcite, but Taylor et al., 1973, p.281, stated that Zirfaea crispata is entirely aragonitic and de Lahidalga & Elorza, 2010, only found calcite in worm tubes that encrusted some pholad shells. It is therefore believed that the calcium carbonate in the shells of Zirfaea crispata, and any other pholads in the Red Crag, were solely composed of aragonite.

Exposed - but ‘swimming’ types The primary defence mechanism of ‘swimming’ bivalves was to slam their valves shut to eject water as a jet, or jets, and so propel themselves away from predators. It was therefore important that scallops maintained characteristics that were not detrimental to this ‘squirt and spurt’ escape mechanism. Studies on living specimens of the giant scallop, more correctly known as the Atlantic deep-sea scallop (Placopecten magellanicus), have shown that at around 5 years of age, individuals phase out ‘swimming’ (Dadswell & Weihs, 1990, p.783; Hart & Chute, 2004, p.2) and rely on their enlarged size and thickened shells to mitigate predation. There is a distinct weight gain associated with enlargement and thickening, and although they have particularly large adductor muscles, individuals outgrow the ability of these muscles to perform ‘squirt and spurt’. The scallops usually found in the Red Crag were the small, or queen, scallop (Aequipecten opercularis) and the king scallop (Pecten maximus). The soft parts of these fossils have long decayed away but modern-day specimens show that the soft parts would have contributed about 40% of an individual’s total body weight, therefore the shells would have contributed about 60%. As calcite is slightly less dense than aragonite, then there was a small weight

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advantage (a 4 to 5% benefit) for Red Crag scallops to build with calcite in order to ensure that they were able to continue ‘swimming’ throughout their lives. There don’t seem to be any published analyses of the shells of these two scallops, but it has been stated that they are largely composed of calcite (Taylor et al., 1969, p.91; Hickson et al., 1989, p.326).

Exposed – creeping and sedentary types Most gastropods, and some bivalves, lived on top of the substrates and were clearly vulnerable to attack through:boring (mainly by carnivorous gastropods, also sponges and worms) crushing and smashing (particularly by crabs but including birds and wolffish) prising apart the valves or the operculum (usually by starfish, sometimes crabs).

There was therefore a clear need for exposed gastropods and bivalves that didn’t ‘swim’ to possess other protective means.

Red Crag bivalves that lived in this open environment included mussels and oysters; these bivalves managed the risks slightly differently. Blue mussels (Mytilus edulis) created their shells with a thin inner layer of aragonite and a more dominant outer layer of calcite. Thickening has been recorded in some shells, Markham 1966, p.24, but thickening probably wasn’t always worthwhile if the main threat was from carnivorous gastropods as beds of mussels could have ensnared slow-boring gastropods with byssal threads and could have even ‘swayed about en-masse’ to flip over the predators. In contrast, our native oyster (Ostrea edulis), lived in quieter waters where physical damage resulting from rough seas was less of a threat. Instead, to minimise the threat of being crushed or fatally bored by predators they always developed thick shell walls. Apart from retaining a nacreous layer of aragonite to provide a very strong anchorage for their well-developed adductor muscles, oysters had shells that were otherwise entirely composed of the less demanding option, calcite.

Most exposed gastropods opted for the stronger option, aragonite, when developing their shells. Marauding gastropods were themselves exposed to predation, particularly if they were a relatively small species or not fully grown. As a thickening response consumed significant resources (Palmer, 1992), thickening would have only been undertaken where the risk of predation stimulated it, i.e. in environments where individuals strongly detected the chemical characteristics (‘smell’) of killed companions. The most attractive environments to predators were where there was not only a good supply of potential prey but also shelter from waves and currents which could have dislodged the predators and washed them away. As mentioned earlier, calcite was a less demanding option than aragonite and some gastropods thickened with calcite. Further details regarding some of the true whelks, which were among the largest predatory gastropods in the Red Crag, and the smaller sized dog winkles follow.

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Calcium carbonate in some true whelks (buccinids) Buccinum undatum There were 4 layers of calcium carbonate in the shells of this true whelk and it is well known that they were composed entirely of aragonite, yet, there is a surprising lack of published analyses, or even references based on quantitative analyses, to substantiate this fact. The only two reliable sources that I have found so far are Bøggild, 1930, p.314, and Hollyman, 2017, p.92 & 99; both of these authors analysed modern day specimens.

Neptunea spp.

The neptunes were closely related to Buccinum undatum and although aragonite was important, the neptunes had more reliance on calcite. This has been corroborated by indicative analyses carried out for me by x-ray diffraction at the University of East Anglia’s Science Analytical Facility, see Table 1.

TABLE 1. THE CALCIUM CARBONATE COMPOSITION OF SOME NEPTUNEA SHELLS CALCIUM CARBONATE FURTHER DETAILS OF SPECIMENS (ACCURACY ±2%) SPECIES OF % % DATE OF COLLECTED COLLECTED NEPTUNEA CALCITE ARAGONITE DEATH FROM BY

N. antiqua

78.5

21.5

2006

Smith’s Knoll, N. Sea

Phil Hollyman

N. contraria (≡ angulata)

77.5

22.5

c. 2.5Myrs ago

Red Crag Chicken Pit, Sutton, Suffolk

Bob Markham

N. despecta

55.0

45.0

2006

Smith’s Knoll, N. Sea

Phil Hollyman

Note the lower proportion of calcite in the specimen of Neptunea despecta. This was the largest of these 3 specimens, but it was also the lightest and thinnest (least thickened).

Calcium carbonate in some dog winkles (‘nucellids’) Nucella lapillus In respect of the calcium carbonate in Nucella lapillus shells, some authors have stated that the shells were composed of calcite in their entirety, or sufficiently close to entirely. This is a view that I transcribed last year (Mottram, 2018, Table 1.) but, upon looking into the situation more deeply, I have found studies that have suggested that aragonite may have represented up to ⅓ of the calcium carbonate in the shells of Nucella lapillus, see Table 2.

Spinucella tetragona Like many molluscs, Spinucella tetragona has been referred to by several names.

From the late 1800s this gastropod usually appears in accounts of the geology of

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TABLE 2. THE CALCIUM CARBONATE COMPOSITION OF NUCELLA LAPILLUS SHELLS SOURCE OF INFORMATION

DESCRIPTION OR DETAILS PROVIDED

INFERRED COMPOSITIONS OF THE SAMPLED AREAS OF THE SHELLS

Bøggild (1930) p.314

a thick outer calcite layer and a thin inner aragonite layer

Plate XII Fig. 6

calcite layer about 0.673mm thick and aragonite layer about 0.091mm thick

Hall & Kennedy (1967) p.391

composed of calcite

Vermeij (1993b) p.45

the genus Nucella has shells of calcite

100% calcite : 0% aragonite

Kool (1993) p.93-94

the outer layer is calcite and is 5580% of shell thickness with 1 to 2 layers of cross lamellar aragonite below

55% calcite: 45% aragonite to 80% calcite: 20% aragonite

Avery & Etter (2006) p.160

a cross section (under scanning electron microscope) shows an outer homogenous layer that is 0.246mm thick and an inner cross-lamellar 68% calcite: 32% aragonite layer that is 0.114mm thick

(the authors identified their specimen as Nucella incrassata Sowerby and stated equiv. to Purpura lapillis auct)

88% calcite: 12% aragonite

100% calcite: 0% aragonite

(the authors didn’t use the terms calcite or aragonite)

Demarchi et al.

(2014) p.7 & 9 and in appendices

a thick outer homogeneous layer of calcite and a thin inner layer of crossed lamellar material

Rühl et al. (2017) an outer layer of homogenous calcite p.5 and a thin inner layer of crosslamellar aragonite

calcite > aragonite

calcite > aragonite

Suffolk as Purpura tetragona but during the 1950s it started to appear as Nucella tetragona, a name that is still engraved in many of our memories and one that I unwittingly used last year. Strictly speaking, due to the presence of ‘spines’ in part of the shell ‘ornamentation’, see Fig1 the tetragona species should be referred to the genus of ‘spiny Nucella’, viz Spinucella (Vermeij, 1993a).

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Buccinum undatum

50 mm

Neptunea antiqua

Nucella lapillus

Figure 1.

Photographs by courtesy of The Colchester and Ipswich Museum Service. All specimens were from the collections in the Ipswich Museum and all are from the Red Crag except N. antiqua which is a modern day specimen.

Neptunea contraria

Spinucella tetragona ‘spines’

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So far, I have not seen any analyses of the shell composition of Spinucella tetragona, nor of any of the other species of Spinucella. Some indication of the shell composition may be provided by observation of specimens of Spinucella tetragona collected from the Red Crag in Suffolk: these specimens are often friable, R. Markham, pers comm., a condition that is commonly associated with degradation of the aragonitic layer(s) of calcium carbonate in shells.

Spinucella tetragona is extinct and so its lineage cannot be readily checked using DNA analysis, but shell morphology indicates that Spinucella tetragona is very closely related to species of the genus Nucella. Possibly drawn by their heavy ornamentations, Crothers (1985, p.336-338) speculated that Spinucella tetragona was the ancestor of Nucella lamellosa. However, following observations on the evolutions and migrations of molluscs during the last 20 million years, Vermeij (1993a, p.2), suggested that Spinucella sp. was the stock from which the smoother shelled Nucella lapillus evolved.

Following from the foregoing, it is quite likely that the calcium carbonate in Spinucella tetragona shells was largely constructed from calcite but with appreciable amounts of aragonite. Given the divergence between Buccinum undatum and Neptunea spp. mentioned earlier, this presumption must be tinged with some caution.

Summary There was a logic to the types of calcium carbonate deposited in the shells of Red Crag bivalves and gastropods that was related to the lifestyles that the animals led.

The basic associations were:Burrowers → shells composed of aragonite Exposed - sedentary and creeping types → shells usually composed of aragonite; in some species there was also a thicker outer layer(s) of calcite Exposed - but able to ‘swim’ → shells constructed with thin inner layer(s) of aragonite and thicker outer layer(s) of calcite References Avery, R. & Etter, R. J. (2006). Microstructural differences in the reinforcement of a gastropod shell against predation. Marine Ecology Progress Series 323: 159-170. http://www.etterlab.umb.edu/Pubs/AveryEtter06MEPS.pdf Bøggild, B. O. (1930). The shell structure of the mollusks. Det Kongeligr Danske Videnskabernes Selskabs Skrifter Naturvidenskabelig og Mathematisk Afdeling 9de Raekke II: 233–325.

Bouillon, J. (1958). Quelques observations sur la nature de la coquille chez les mollusques. Annales de la Société royale zoologique de Belgique, Bruxelles, t.

LXXXIX, fasc. 9, p. 229-237. www.vliz.be/imisdocs/publications/256240.pdf Crothers, J. H. (1985). Dog-whelks: an introduction to the biology of Nucella lapillus (L.). Field Studies 6: 291-360. https://fsj.field-studies-council.org/media/342851/vol6.2_171_colour.pdf

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Dadswell, D. J. & Weihs, J. (1990). Size related hydrodynamic characteristics of the giant scallop, Placopecten magellanicus (Bivalvia: Pectinidae). Canadian Journal of Zoology 68: 778-785. https://www.researchgate.net/publication/238020430 de Lahidalga, U. M. & Elorza, J. (2010). Activity of recent endolithic bivalves (Pholas) in carbonated boulders from the Biscay abrasion platform. Geogaeta 49: 63-66. https://www.researchgate.net/publication/301290352 Demarchi, B., O’Connor, S., de Lima Ponzoni, A., de Almeida Rocha Ponzoni, R., Sheridan, A., Penkman, K., Hancock, Y. & Wilson, J. (2014). An integrated approach to the taxonomic identification of prehistoric shell ornaments. https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0099839 Hall, A. & Kennedy, W. J. (1967). Aragonite in fossils. Proc. Roy. Soc. (B) 168: 377-412. https://vdocuments.site/aragonite-in-fossils.html Hart, D R. & Chute, A. S. (2004). Technical Memorandum NMFS-NE-189 - Sea Scallop, Placopecten magellanicus, life history and habitat characteristics. NOAA. US Department of Commerce. www.nefsc.noaa.gov/publications/tm/tm189/tm189.pdf Kool, S. P. (1993). The systematic position of the genus Nucella (Prosobranchia; Muricidae: Ocenebrinae). The Nautilus 107: 43-57. https://archive.org/details/cbarchive_38282_thesystematicpositionofthegenu9999 Hickson, J. A., Johnson, I. A., Heaton, T. H. E. & Balson, P. S. (1999) The shell of the Queen Scallop Aequipecten opercularis (L.) as a promising tool for palaeoenvironmental reconstruction: evidence and reasons for equilibrium stableisotope incorporation. Paleogeography, Palaeoclimatology, Palaeoecology 154: 325-337.

Hollyman, P. R. (2017). Age, growth and reproductive assessment of the whelk, Buccinum undatum, in coastal shelf seas. PhD thesis, Bangor University. e.bangor.ac.uk/9872 Markham, R. A. D. (1966). Waldringfield Crag. Ipswich Geological Group Bulletin No. 1. http://geosuffolk.co.uk/images/ipswich-geological-group/IGG-Bulletin-1.pdf Mottram. H. (2018). Can modern day molluscs help us model decalcified Red Crag back to shelly Red Crag? – a discussion. Trans. Suffolk Nat. Soc. 54: 77-86.

Palmer, R. A. (1992). Calcification in marine molluscs how costly is it?. Proceedings of the National Academy of Science, USA. 89: 1379-1382. https://www.pnas.org/content/pnas/89/4/1379.full.pdf Rühl, S., Calosi, P., Faulwetter, S., Keklikoglou, K., Widdecombe, S. & Queriós, A. M. (2017). Long-term exposure to elevated pCO2 more than warming modifies earlylife shell growth in a temperate gastropod. ICES Journal of Marine Science 74: 1113 –1124. https://www.researchgate.net/publication/324794973 Taylor J. D. Kennedy, W. J. & Hall, A., (1969). The shell structure and mineralogy of the bivalvia I - introduction. Nuculacea to Trigonacea. Zoology Series 3, Supplement, 1125. Bulletin of the British Museum (Natural History) Zoology, London. https://archive.org/details/bulletinofbritis3196brit

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Taylor, J. D. Kennedy, W. J. & Hall, A., (1973). The shell structure and mineralogy of the bivalvia II - Lucinacea to Clavagellacea. Zoology volume 22, No.9: 253-294.

Bulletin of the British Museum (Natural History) Zoology, London. https:// archive.org/details/cbarchive_121063_theshellstructureandmineralogy9999 Vermeij, G. J. (1993a). Spinucella, a new genus of Miocene to Pliocene muricid gastropods from the eastern Atlantic. Contributions to Tertiary and Quaternary Geology 30: 19-27. natuurtijdschriften.nl/download?type=document&docid=521600 Vermeij, G. J. (1993b). A natural history of shells. Princetown University Press, New York.

Zhang, J., Tong, J., Caihua, L., Yunhai, M & Yaqin, L. (2011). The microstructure and nanomechanical properties of Chlamys farreri shell. 2011 International Conference on Remote Sensing, Environment and Transportation Engineering. p. 8683-8686.

Nanjing, China. IEEE. https://www.researchgate.net/publication/252020677 H. Mottram

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