Paul D Taylor (UK)
Many fossil collectors will have been disappointed to discover mollusc and brachiopod shells ‘disfigured’ by crust-like coverings of oysters, serpulid worms, barnacles or bryozoans so firmly cemented to the shells that they cannot be removed. However, rather than discarding these encrusted shells, it is worth considering what they can tell us about the ecology of the host animals and the fate of their shells after death. Furthermore, the surfaces of the shells were battlefields for encrusters fighting for living space, allowing a rare opportunity to observe the effects of biological competition millions of years ago.
The key palaeoecological advantage offered by encrusters over most other fossils is that they preserve their original life positions. For example, a fossil barnacle encrusting a fossil bivalve (Fig. 1) is located on the shell exactly where the barnacle larva settled and the adult spent its life. Encrusters are not transported or displaced from where they originally lived, although of course the shells themselves may have been moved.
Encrusters are sclerobionts, a collective term for organisms colonizing all kinds of hard substrates, including shells, bones, wood, rocks and sedimentary hardgrounds (Taylor and Wilson, 2003). Other types of sclerobionts bore into hard substrates, leaving trace fossils as evidence of their former presence, or are anchored to the surfaces of hard substrates before growing upwards into the water column, such as mussels attached by byssal threads or tree-like corals.
Then there are sclerobionts, such as limpets, which graze hard substrates scraping off the algal covering for food. But my focus here is on the low-profile encrusting animals and plants found on fossil shells. For these encrusters, the shells they lived on represent habitat islands. For palaeontologists, the microcommunities they form on these shells are convenient and fascinating subjects for scientific study.
Encrusting sclerobionts affix themselves to shells using a combination of organic glues and mineral cements. The bond between encruster and substrate is usually strong enough to survive long after the death of the encruster, which explains why encrusters are frequently fossilized in-situ. Occasionally, however, during fossil extraction, encrusters separate from shells and adhere to the surrounding sediment.
Because they are attached to a hard surface throughout their life, encrusting animals lack the ability to pursue their prey and must rely on food in the water around them. Nearly all encrusters are suspension feeders, using their own feeding currents to capture small planktonic organisms that come within their range or, in the case of corals, harpooning zooplankton employing the stinging cells on their tentacles.
As the adults of encrusting species are immobile, dispersal is the responsibility of larvae formed during sexual reproduction. Larvae swim – and sometimes feed – until they encounter a suitable hard substrate. Here, they settle and metamorphose into the adult, forever to remain associated with the same substrate. Huge numbers of larvae can be released into the sea, but many do not survive long enough to locate a suitable hard substrate and, of those that do, only a small proportion typically recruit successfully to develop into fully fledged adults.
The cast of encrusters
Before discussing the palaeoecology of shell encrusters, it is worth briefly mentioning the main groups of organisms containing encrusting species. Hard substrates in the sea today are colonized by a wide variety of encrusting organisms. Some of these do not readily fossilize, for example, bacteria, fleshy algae, sea-squirts, and sponges without mineralized skeletons. Others, however, are well represented in the fossil record.
Photosynthetic calcareous algae are common encrusters of shells at the present-day, but are seldom seen on shells before the Late Cretaceous. They tend to form somewhat featureless coatings requiring thin sectioning for identification.
Free-living species of single-celled foraminifera have been used extensively in biostratigraphy, oceanography and palaeoclimatology. Far less well-known are encrusting foraminifera. However, look carefully at the surfaces of shells of the oyster Gryphaea from the Upper Jurassic Oxford Clay and you may notice a covering of fine white threads. These belong to the foraminiferan genus Nubeculinella. Under a microscope, the beaded, chambered structure of their calcareous skeletons becomes evident. Elsewhere, agglutinated foraminifera, with tests consisting of minute grains of sediment cemented together, are not uncommon as encrusters, as in the Early Cretaceous Faringdon Sponge Gravel (Wilson, 1986).
Encrusting sponges may form sheet-like coverings on fossil shells. They owe their preservation to having mineralized skeletons, which can be solid or spicular, with the spicules fused or strongly interlocking. Neuroporids, which are found quite commonly in the Jurassic and Cretaceous but are often mistaken for bryozoans, have solid calcareous skeletons, the surface of which is covered by tiny pores and crossed by ridges radiating from blunt spines.
Some corals are encrusters, notably Aulopora (see Zapalski, 2005), a tabulate coral commonly found on the shells of Silurian and Devonian brachiopods. Colonies of Aulopora have bifurcating branches formed of rows of tubular corallites reclining on their brachiopod and other hosts. Rugose and scleractinian corals, both colonial and solitary, are also occasionally found attached to fossil shells.
A small minority of brachiopods are encrusters, the ventral (pedicle) valve being cemented to the substrate and the dorsal (brachial) valve hinged onto it like a lid (for example, Hoel, 2007). Fossil collectors are most likely to come across one of two groups of encrusting brachiopods:
- craniids like Ancistrocrania found in the Cretaceous Chalk, and
- the cideans which occur quite often on Jurassic–Recent hard substrates, but are easily overlooked because of their minute size (Fig. 2).
Numerous species of bryozoans can be found encrusting shells from the Ordovician to the Recent (Figs. 5 to 7). Most are sheet-like expansions, but some have branching colonies superficially resembling those of the coral Aulopora. Bryozoan colonies comprise modular units – zooids – each typically less than a millimetre in length. A polygonal or round opening at the end of each feeding module marks the place where the retractable tentacle crown was extruded for the purpose of feeding on plankton.
Serpulid worms (Fig. 4) construct external tubes of calcium carbonate, with an opening at the end through which the worm protrudes its ciliated tentacles. These tubes may be straight, sinuous or tightly coiled (as in Spirorbis, Fig. 7D), and vary from rounded to angular with one, two or three ridges running along their lengths. Although older examples are known, serpulids first became common in the Jurassic and can be found in all younger deposits, often in great numbers.
Among molluscs, oysters – family Ostreidae – are the most important group of encrusters, but several other bivalve families also evolved cemented species capable of encrusting shells (Fig. 3), especially in the Mesozoic and Cenozoic. Often, only the cemented valve is preserved on the hard substrate, the upper valve having been lost following disarticulation after death. Vermetids are a group of irregularly coiled gastropods known as ‘worm shells’, sometimes found cemented onto Cenozoic shell substrates (Fig. 3).
Acorn barnacles – balanomorphs – are all too familiar to anyone who has suffered lacerated feet while walking along a rocky shoreline. These aberrant crustaceans did not appear until the Cretaceous and were uncommon before the Oligocene. Fossil examples on shells often occur in dense aggregations, as they do in modern seas.
Other encrusters include edrioasteroids, an unusual group of echinoderms that are occasionally found on Palaeozoic brachiopod shells, and a few rare groups of hemichordates, notably crustoids, that construct ramifying (that is, branching or forming offshoots), carbonaceous colonies on shells.
Finally, there are several kinds of Palaeozoic encrusters, whose biological affinities are unknown or uncertain. These include microconchids and cornulitids, tubeworms resembling Spirorbis and non-coiled serpulids, respectively (for example, Vinn and Mutvei, 2009). Hederelloids are colonial encrusters particularly common on Devonian brachiopods that may be related to modern phoronid worms. More enigmatic is Ascodictyon, a thread-like encrustation radiating from central points to form a network on shells.
Syn-vivo or post-mortem encrustation?
Or, in other words, did the encrusters colonize the shelled animal while it was alive (syn-vivo) or after it had died (post-mortem)? It is crucial to know this if seeking to use encrusters to understand the ecology of the host. Post-mortem encrustation can be inferred when an encruster is present on an interior shell surface (Fig. 3) that would have been covered by soft tissues during the host’s life. Thus, encrusters on the concave, inner surfaces of bivalve, brachiopod and gastropod shells would have grown on these surfaces after the host had died.
In contrast, colonization of outer surfaces can occur both before and after death of the host animal. Some shelled animals have the ability to prevent or discourage encrustation of their outer exposed surfaces, but, for others, encrusters are tolerated and have even been shown in some living species to be beneficial. For example, coverings of sponges can protect pectinid bivalves from being eaten by starfish, because the sponges hamper the adhesion of the tube feet of the predatory starfish trying to pry open the shells.
Evidence pointing to encrustation when the host was alive can be obtained by examining the distributions and orientations of the encrusters over the shell surface. Encrusters may be positioned to take advantage of the stronger feeding currents of their larger hosts, meaning that they often cluster around the openings – commissures – at the edges of the bivalve and brachiopod shells. The growth direction of the encruster may be towards the commissure, as in serpulids encrusting brachiopod shells (Fig. 4).
Very occasionally, the growth of an encruster stops abruptly at a growth line on the host shell. This signifies that the event causing the host to temporarily halt shell growth also led to the demise of the encruster, another good line of evidence for a life association. Likewise, distorted host shell growth where encrusters are present can indicate that the host was alive when encrusted. Specimens of the Early Jurassic ammonite Promicroceras from Dorset have been described encrusted by serpulid worms that grew along the venter of the host while maintaining the tube opening just ahead of the advancing whorls of the host (Andrew et al., 2011). The serpulids became embedded between the whorls of the ammonite shell, disrupting normal shell growth and causing death of the hosts at a smaller size than is usual for these ammonites.
Being encrusted was clearly disadvantageous to the host animal in this example, as may be true for mobile hosts that have an optimal shape and weight for balance. Nevertheless, encrusters were common on some swimming cephalopods, including Ordovician orthoconic nautiloids from the Cincinnati region of the USA (Fig. 5). As described by Wyse Jackson et al. (2014), colonies of the encrusting bryozoan, Spatiopora, were able to flourish on the shells of these animals as they swam, often surviving and continuing to grow following the death of the host cephalopods.
Growth of an encruster from one valve onto the other of a brachiopod or bivalve locking the two valves together, and thereby preventing the host from feeding, indicates a post-mortem association, at least during its final phases. It can be difficult, however, to discount the possibility that the encruster initially grew on a living host, but continued to grow after the host had died.
The positioning of encrusters on shells of extinct species can be useful for interpreting the feeding of the host. For example, a concentration of encrusters at a particular area along the commissure of a host shell may suggest that this is where the incurrents carrying plankton entered, the optimal site for encrusters seeking to steal some of this food.
In the case of semi-infaunal hosts living partly buried in the sediment, the distribution of encruster scan indicate which parts of the shell were above the sediment surface and available for colonization by encrusters. Watson’s (1982) study of the brachiopod Discinisca attached to shells the Early Jurassic bivalve Dacryomya in the Upper Liassic of Yorkshire illustrates both of these patterns. Individuals of Discinisca were found by Watson to be clustered around the posterior margins of the host bivalve, where they were not only above the level of the sediment in this semi-infaunal animal, but could also benefit from its feeding currents.
Collections of fossil shells sometimes reveal no encrusters whatsoever. This might mean that the shelled animals lived infaunally in the sediment and their shells were therefore never available as substrates available for encrustation on the sea-bed. It is also possible that any encrusters present were not fossilized, as is often the case for sponges, sea-squirts and fleshy algae.
In addition, encrusting species tend to be patchily distributed in the sea, which reflects the typically short duration and restricted dispersal of their larvae. Unless there is an adult population nearby, the larvae of encrusters may never reach shells that would be potential substrates. However, once a local community of encrusters has been established, any newly available shell becomes a target.
Pinpointing the exact place on the fossil shell where the larva of an encruster settled is usually quite straightforward, making it possible to map the pattern of recruitment over the shell surface, and also the respective areas occupied by different encrusters on each shell (for example, Barclay et al., 2015). The identities and spatial distributions of encrusters can be compared between:
- the external and internal surfaces of a shell
- the two valves of a shell with two valves (for example, brachiopod or bivalve)
- different individuals of one species, and
- between different host species.
These comparisons can provide useful information about the ecology and taphonomy of hosts and encrusters.
A good example of mapping is the study of Bishop (1988) on the distribution of tiny colonies of the bryozoan Cribrilina puncturata over the concave inner surfaces of bivalve shells from the Red Crag Formation of eastern England. These shells were colonized by this encrusting bryozoan while resting in a stable, convex upwards attitude on the Plio-Pleistocene seafloor.
Bishop found the bryozoans to be concentrated on the deepest parts of the bivalve shells, most distant from the sediment and thus in a location delaying their eventual demise from burial. Encrusters are far less common on the convex outer surfaces of the same bivalve shells. Reasons for this might include:
- exclusion by algae which could flourish on these well-lit, upper surfaces
- abrasion by entrained sand grains in the strong currents, and/or
- destruction by grazing predators.
In one of numerous studies of encrusters on Palaeozoic brachiopods, Zapalski (2005) found clear variations in the frequency of encrustation of different brachiopod genera by auloporid corals in the Devonian Holy Cross Mountains of Poland. The brachiopod Kyratrypa was more often encrusted than Desquamatia, a difference attributed by Zapalski to the stronger ribbing and ornamentation on the shell of the former. It is known that larvae of some modern encrusters settle selectively, and survive better, in protected recesses on shells, which could account for the pattern seen in these Devonian brachiopods. The same study also noted the greater likelihood of finding encrusters on larger rather than smaller brachiopod shells. This is commonly the case and can have several explanations, including the larger surface area for larvae to settle, and the longer time that older shells are available as targets for encrustation.
The fight for living space
Occupying and holding onto living space is of paramount importance to encrusting organisms. Indeed, as the main limiting resource, space can be the focus of vigorous competition; in contrast, planktonic food is superabundant in some habitats and need not be competed for.
As encrusters spread across shells during their growth, and available habitat space diminishes (Fig. 6), they often meet others head-to-head. Usually, one of the competing encrusters on these spatial battlefields is dominant and overgrows the other (Fig. 7A). This can be observed by the overlapping relationship between overgrower and overgrown encrusters in fossils.
Sometimes, however, there is a ‘stand-off’ and the edges of the two encrusters abut with neither being able to overgrow the other (Fig. 7B). Stand-offs are particularly common when two encrusters belonging to the same species meet, which is understandable as they have roughly the same competitive ability. Yet another outcome is occasionally seen: reciprocal overgrowth, in which one encruster overgrows the other along part of their line of contact but this is reversed elsewhere (Fig. 7C).
All of these possibilities can also be observed among encrusters on fossil shells and other hard substrates (Taylor, 2016). An important qualification is that it is seldom possible to know for sure whether the overgrown encruster was alive or dead at the time of overgrowth. However, there can be some lines of evidence pointing to syn-vivo interactions. These include the presence of reciprocal overgrowths, showing that both encrusters were alive at the same time, or of standoffs between encrusters belonging to the same species as overgrowth would be expected if one had been dead.
Overgrowth may result in smothering and death of the overgrown encruster, but this is not always the case. For example, serpulid worms can survive overgrowth if this is confined to the tube exterior and does not block the opening from which the soft parts of the animal are protruded for feeding. And, in the case of colonial animals, overgrowth of some individual zooids can be survived, as long as others in the colony are not smothered.
Some shells reveal layers of encrusters piled one on top of the other. Like a sequence of strata, those on the bottom are the oldest, the encrusters becoming progressively younger towards the top of the pile, recording an ecological succession. Overgrowth during competition or post-mortem can be responsible for this layering, but another process – fouling –also produces layering. Fouling is when a larva successfully settles on the surface of an existing organism, in this case an encruster, and develops into an adult. As organisms tend to have good defences to deter fouling, the existence of fouling can indicate the fouled organism was either dead or moribund.
Exceptionally adept at fouling living hosts, however, are microconchids and spirorbids (Fig. 7D).These small spiral tubeworms are frequently found fouling other encrusters, the organisms they foul sometimes responding in time by overgrowing the fouler.
Here’s an example of the battle for space on fossil shells. Di Martino et al. (2020) studied interactions between encrusters on valves of the Pliocene bivalve, Anomia simplex. A total of 867 upper valves of this cemented bivalve were collected from the Tamiami Formation of Florida. Of these, 96% were encrusted on outer surfaces and 62% on inner surfaces, indicating that at least some of the encrustation occurred after the bivalves had died. Most of the encrusters are bryozoans, although there are also a few barnacles, spirorbid worms, small corals and foraminifera.
Focusing on the bryozoans, which are almost entirely sheet-like colonies, 1,438 competitive interactions were observed. As expected for competition between living encrusters, encounters between colonies of the same species tended to result in stand-offs, whereas those between different species led to overgrowths. Bryozoan species with small zooids were usually overgrown by species with larger zooids, a pattern typical of contests for living space between bryozoans.
Size in this case really does matter.
Think twice before throwing encrusted shells onto the pile of rejects when fossil collecting. You risk discarding fossils replete with palaeoecological interest. Instead, keep them and challenge yourself to work out the relationships between the encrusters and the host shells (for example, whether the shells were encrusted during life or after death), and see how the different encrusters battled it out for living space on their habitat islands.
In Britain, encrusted brachiopod shells can be collected from the Silurian Wenlock Limestone of the West Midlands and the Jurassic Boueti Bed of Dorset, while encrusted bivalve shells are common in the Plio-Pleistocene Crags of East Anglia. In the US, encrusted brachiopods are to be found abundantly in the Late Ordovician of the mid-west and the Devonian of New York State and Michigan, with encrusted molluscs numerous in Cretaceous to Cenozoic deposits of the eastern states from Maryland to Texas.
Andrew, C., Howe, P., Paul, C.R.C. & Donovan, S.K. 2011. Epifaunal worm tubes on Lower Jurassic (Lower Lias) ammonites from Dorset. Proceedings of the Geologists’ Association 122: 34–46.
Barclay, K. M., Schneider, C. L. & Leighton, L. R. 2015. Mapping sclerobiosis: a new method for interpreting the distribution, biological implications, and paleoenvironmental significance of sclerobionts on biotic hosts. Paleobiology 41: 592–609.
Bishop, J.D.D. 1988. Disarticulated bivalve shells as substrates for encrustation by the bryozoan Cribrilinapuncturata in the Plio-Pleistocene Red Crag of Eastern England. Palaeontology 31: 237–253.
Di Martino, E., Liow, L. H., Perkins, T., Portell, R. W. & Taylor, P. D. 2020. Sneaking up on ‘enemies’: alleviating inherent disadvantages in competitive outcomes in a nearly 3‐million‐year‐old palaeocommunity from Florida. Lethaia 53: 553–562.
Hoel, O. A. 2007. Cementing strophomenide brachiopods from the Silurian of Gotland (Sweden): Morphology and life habits. Geobios 40: 589–608.
Taylor, P. D. 2016. Competition between encrusters on marine hard substrates and its fossil record. Palaeontology 59: 481–497.
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Vinn, O. &Mutvei, H. 2009. Calcareous tubeworms of the Phanerozoic. Estonian Journal of Earth Sciences 58: 286–296.
Watson, J.S. 1982. The occurrence of Discinisca on Dacryomya ovum: an example of commensalism from the Upper Lias of Yorkshire. Proceedings of the Yorkshire Geological Society 44: 45–51.
Wilson, M.A. 1986. New adherent foraminiferans from the Lower Cretaceous (Aptian) of south-central England. Journal of Micropaleontology 5: 1–8.
Wyse Jackson, P. N., Key, M. M. Jr & Coakley, S. P. 2014. Epizoozoan trepostome bryozoans on nautiloids from the Upper Ordovician (Katian) of the Cincinnati Arch region, U.S.A.: an assessment of growth, form, and water flow dynamics. Journal of Paleontology 88: 475–487.
Zapalski, M. K. 2005. Paleoecology of Auloporida: an example from the Devonian of the Holy Cross Mts., Poland. Geobios 38: 677–683.