A Prejudiced Review of Ancient Parasites and Their Host Echinoderms

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A Prejudiced Review of Ancient Parasites and Their Host Echinoderms: CSI Fossil Record or Just an Excuse for Speculation? Stephen K. Donovan Department of Geology, Naturalis Biodiversity Center, Leiden, The Netherlands E-mail: [email protected]

Contents 1. Introduction 2. Interpretations and Confidence 2.1 Problems of interpretation 2.2 Limits of confidence 3. Some Examples 3.1 A coralecrinoid association from the Mississippian 3.2 A growth deformity in a Mississippian crinoid 3.3 Epizoobionts infesting a Mississippian crinoid 3.4 Platyceratid gastropods infesting Upper Palaeozoic crinoids 3.5 Site selectivity of pits in echinoid tests, Upper Cretaceous 4. Discussion 5. Conclusions Acknowledgements References

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Abstract Recognizing the presence of a parasite and identifying it is a relatively straightforward task for the twenty-first century parasitologist. Not so the pursuit of ancient parasites in fossil organisms, a much more difficult proposition. Herein, Boucot’s seven-tiered scheme of reliability classes is applied as a measure of confidence of the recognition of putative parasitism in two echinoderm classes, Upper Palaeozoic crinoids and a Cretaceous echinoid (high confidence is 1, low confidence 7). Of the five examples, the parasitic(?) organism is preserved in only two of them. A zaphrentoid coral on the camerate crinoid Amphoracrinus may have robbed food from the arms (Category 1 or 2B). A pit in what appears to be a carefully selected site on the disparid crinoid Synbathocrinus is associated with a growth deformity of the cup (Category 4). Multiple Advances in Parasitology, Volume 90 ISSN 0065-308X http://dx.doi.org/10.1016/bs.apar.2015.05.003

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pits in an Amphoracrinus theca are also associated with a deformed cup, but it is more difficult to interpret (Category 4 or 7). Some specimens of the camerate crinoid Neoplatycrinites have circular grooves or depressions posteriorly, presumably produced by coprophagic/parasitic platyceratid gastropods (Category 1). Site selectivity of pits in the echinoid Hemipneustes places them preferentially adjacent to respiratory tube feet (Category 4). From these examples it is deduced that sparse infestations of borings or epizoozoic organisms permit a more confident interpretation of organism/organism interactions; dense accumulations, possibly following multiple spatfalls, mask such patterns.

1. INTRODUCTION Consider the task of the parasitologist. There may or may not be an actual physical manifestation of the attentions of a parasite in a human being, sheep, favourite pet dog or fish bought from a fishmonger, but its presence is easily confirmed (or otherwise) using the wide range of biomedical, biochemical and gene sequencing tools currently available. A stool is collected, blood sampled or the fish cut open, and the hunt is on. Not only can the parasite be identified, but its life cycle elucidated and its genes sequenced. In the twentyfirst century, all this can be done before lunch. The hunter of fossil parasites, in my own case, in ancient echinoderms, has none of these advantages. We may confidently speculate that many or most parasites in ancient echinoderms left no evidence of their presence and we will never know that they were ever there. Such navel contemplation is the easy part. Commonly, where there is evidence of some interaction between an organism, parasite or not, and the host, this is preserved as some invasive structure (boring) into the echinoderm’s endoskeleton. This may or may not be associated with a growth deformation of the host. Borings without growth deformities must be regarded as not proven parasitism, as such traces of interaction can occur after the death of the echinoderm, either soon after (Donovan, 2014; Donovan et al., 2014a) or millions of years later (Donovan and Lewis, 2011; Donovan, 2013). Associated growth deformities show that the boring was engendered while the echinoderm was alive and able to react to the invasion. What commonly does not get preserved is the producer of the boring, which almost invariably lacks a mineralized (and thus easily preserved) skeleton, so our interpretation of its purpose (parasitism, or failed or successful predation, or something else) must be made in ignorance of the simple fact, whodunit? The parasitologist looks for parasites; the palaeoparasitologist works by necessity without

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parasites, except for rare examples such as parasites with preservable skeletons such as parasitic snails (see below) or rare mineralized producers of pits such as Phosphannulus M€ uller et al., 1974 (Welch, 1976; Werle et al., 1984; Boucot, 1990, pp. 32e34). So, what can we hope to achieve? As already intimated, many palaeontological investigations of echinoderms and putative parasites begin with the recognition of pits and boreholes in the echinoderm endoskeleton. Pits, borings and related structures in ancient substrates, such as tracks, trails, burrows and coprolites, are trace fossils, representing evidence of ancient organic activity. The study of trace fossils is ichnology. Only rarely is the producing organism preserved adjacent to a trace except in certain settings, such as the shells of boring bivalves which may be preserved in their borehole in limestone (for example, Donovan and Jagt, 2013a). It is a mantra of ichnology, the study of trace fossils, that a given organism may have produced a range of trace fossils, representing different activities, and that a particular morphology of trace fossil may have been produced by more than one group of organisms, involved in similar activities. Trace fossils are given Latinized binomens, but these do not refer to an organism per se, but to the sedimentary structure that is the trace fossil. That is, their classification as sedimentary structures is analogous to, but not part of, Linnean classification. It is a common ‘game’ in ichnology to speculate on the identity of producing organisms, but it is incorrect to be too dogmatic about such assertions (Donovan, 2010). Pits in live echinoderms commonly produce growth reactions in the endoskeleton, either inhibiting growth or causing swellings of various morphologies, but these are pathologies of the echinoderm and are not part of the trace fossil (Donovan, 2015). Further, trace fossils are named on morphology and not substrate (Pickerill, 1994); for example, it was suggested that borings in the echinoderm test that cause a range of growth deformations should be referred to Tremichnus Brett, 1985, but all morphologically similar small round holes are more correctly referred to Sedilichnus M€ uller, 1977, a senior synonym of the widely used Oichnus Bromley, 1981 (Zonneveld and Gingras, 2014; see also Pickerill and Donovan, 1998; Donovan and Pickerill, 2002). If this sounds daunting, then add to this the confusion introduced by the taphonomy, the study of the preservation of our infested echinoderm. There are some organisms which have simple skeletons that are commonly preserved whole, such as gastropods, shelled cephalopods, tube-dwelling worms, foraminiferans and stony corals, or disarticulated into just a few pieces, including bivalve molluscs, brachiopods and ostracods. Most other

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groups of organisms have complicated, multielement skeletons that fall apart soon after death; one individual can be preserved as tens or hundreds of individual pieces. The latter include the vertebrates, arthropods, plants and echinoderms. Commonly, evidence of a possible parasitic interaction is found in a fragment of echinoderm that cannot be classified with any confidence any closer than class or order. And, of course, it may be that the parasitic infestation weakened the skeleton so that it is more prone to disarticulation postmortem than otherwise. So, palaeoparasitology of echinoderms most commonly involves recognizing pathological growth deformities produced in response to structures generated by parasitic(?) organisms. The producing organisms are not themselves commonly preserved or otherwise identifiable (although two specific examples where the parasite is preserved are discussed below) and the echinoderm may be preserved as only a fragment of endoskeleton that can only be classified to class level, such as a fragment of crinoid column. If we accept this as the starting point for this paper, then we can, at least, describe some good examples that lead to reasonable interpretations. The morphological terminology of the crinoid endoskeleton is explained in Ubaghs (1978) and Moore et al. (1978); for that of the echinoid test, see Smith and Kroh (2011). Specimens discussed below are deposited in the following institutions: Department of Earth Sciences, the Natural History Museum, London, England (BMNH); Naturalis Biodiversity Center, Leiden, the Netherlands (RGM); and Natuurhistorisch Museum Maastricht, Maastricht, the Netherlands (NHMM).

2. INTERPRETATIONS AND CONFIDENCE A great diversity of disease-carrying and parasitic organisms infest extant echinoderms (Jangoux, 1987a,b,c,d), although they are rarely parasitic themselves (Rouse in Rhode, 2005, pp. 248e250). It is only in examples where infestations of ancient echinoderms caused some recognizable deformity in skeletal growth, or the exceedingly rare cases in which the infesting organism itself is fossilized, that an indication of disease or parasitism can be identified in the fossil record (Conway Morris, 1981; Boucot, 1990; Littlewood and Donovan, 2003). For example, parasites may produce distinctive galls or cysts in echinoid radioles (Warén and Moolenbeek, 1989), asteroid arms, crinoid pinnules and cirri, and ophiuroids discs (Grygier, 1988). Examples of non-cyst-like structures produced by

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purported parasites which are considered below infest Upper Palaeozoic crinoid thecae and Cretaceous echinoid tests.

2.1 Problems of interpretation Interpretations of exotic interactions between ancient (or even extant) organisms are commonly problematic and rarely leads to hard conclusions, apart from examples such as simple encrustations or boring invasions with numerous modern analogues. For an example of the problem of interpreting ancient interactions with echinoderms which is not parasitism, but certainly exotic, consider the lectotype specimen of the primitive mollusc Phthipodochiton thraivensis (Reed, 1911) (see Sutton and Sigwart, 2012; Figure 1

Figure 1 Phthipodochiton thraivensis (Reed, 1911), BMNH G47258, lectotype, from the Upper Ordovician of south-west Scotland. (After Donovan et al. (2010), Figures 2 and 3(c), respectively.) (a) The specimen showing the valves of the chiton, preserved as natural moulds and curving up from the lower centre to the right, past the label and towards the top left. Scale bar represents 10 mm. (b) High-resolution X-ray microtomography image of the complete gut contents (valves removed). Scale bar represents 1 mm.

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herein) from the Upper Ordovician Lady Burn Starfish Beds of south-west Scotland. Mark Sutton and Julia Sigwart imaged the concealed structure of this specimen using high-resolution X-ray microtomography (for full details, see Donovan et al., 2010, pp. 935e936). This revealed a string of shelly material preserved in a position that would correspond to the gut in an extant chiton. The most prominent component of this string is a group of nine crinoid columnals of more or less similar morphology that are interpreted as being derived from an individual of the camerate Macrostylocrinus cirrifer Ramsbottom, 1961 (Donovan et al., 2011b), a common taxon at Lady Burn. Multiple lines of evidence indicate that this association is not a hydrodynamic accumulation (Donovan et al., 2010). The columnals represent ingested hard parts that were passing through the spiral gut of the chiton at the time of death. Chitons are commonly thought of as simple grazers, feeding on encrusting algae on rock surfaces, but many living chitons live on animal matter (Fulton, 1975; Latyshev et al., 2004) and examination of gut contents in living species shows a variety of food preferences, in some species highly specialized (Sirenko, 2000). Almost nothing is known regarding the predators and scavengers of Ordovician crinoids (Meyer and Ausich, 1983; Baumiller and Gahn, 2003). Determination of predation and scavenging of Ordovician crinoids has been mainly inferential, although there is suggestive evidence for predatory decapitation in some disparids (Donovan and Schmidt, 2001), perhaps a Category 3 association sensu Boucot (1990; see below). Category 1 associations of crinoids as prey are rare throughout the fossil record, and the example discussed herein is the oldest and the most unexpected. Crinoid columnals may have been consumed by this chiton due to predation, scavenging or ingestion of sediment rich in crinoid bioclasts. The last seems unlikely; unless the chiton was particularly unselective, it would more likely have harvested organic matter from finer grained sedimentary particles. Predation or scavenging is thus more probable, but equally plausible. The speculation of predatory versus scavenging behaviour may appear trivial in this example, but it is analogous to the sometimes heated discussions of the habits of Tyrannosaurus rex Osborn, 1905 e predator or scavenger e which have engendered a diverse correspondence (for a recent discussion, see Erickson, 2014). Whichever, such crinoidivory in this ancient Scottish mollusc is unexpected, being unknown from extant chitons; like T. rex, we lack a modern analogue to provide an answer.

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To give a further echinodermal example of an organismeorganism interaction that defies entirely confident interpretation, consider the well documented record of otherwise well-preserved Palaeozoic crinoids that retain evidence of regeneration of one or more arms (see Baumiller and Gahn, 2003, 2004). These are commonly interpreted as evidence of successful predation on the arms of crinoids, but as of yet there is no entirely satisfactory explanation of why anything should have been eating such a poorly nutritious part of the animal. Extant crinoids carry their gonads mainly in their arms and pinnules (Breimer, 1978, pp. T18eT19), making these nutritious organs the principal targets for predators. If eaten, an arm can be regenerated; the comatulid Antedon bifida (Pennant, 1777) is gravid throughout the year, presumably to tempt predators and divert them from the visceral mass, although the reproductive season is only a month (Nichols, 1994). Palaeozoic crinoids lacked this adaptation and it is assumed that the gonads were included within the cup, although some taxa may have adapted their large anal sacs to bear the gonads (Lane, 1984). Both I and other authorities (V.J. Syverson, October 2013, personal communication) are of the opinion that predation on the arms of Palaeozoic crinoids may be evidence of predation, not on the innutritious arms of crinoids, but on some nutritious organism(s) or group(s) of organism(s) that lived on the arms. This is entirely speculative as I am not aware of reports of likely prey organisms being preserved on the arms; they may have been unmineralized and thus unlikely to be fossilized. The evidence is good for the predation of the arms of Palaeozoic crinoids, but not good for the reason why.

2.2 Limits of confidence The two examples given above e one particular, one general e demonstrate something of the difficulties of making a precise interpretation of the interactions between echinoderms and other organisms even when the data is good. What is needed at this juncture is some qualitative measure that researchers can apply to their deliberations to give their readers a ‘feel’ of the level of confidence with which they are made. I suggest one way forward, admittedly preliminary, is an adaptation of Boucot’s (1990, pp. 9e10) original reliability classes which he applied to myriad examples that he examined for evidence of behaviour and coevolution in the fossil record. The reader is referred to the original publication for more explanation and many more examples, as this tabulation is merely a brief abstract of a

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much greater body of argument and evidence. Briefly, Boucot’s categories are summarized thus: Category 1 Category 2A Category Category Category Category Category Category

2B 3 4 5A 5B 6

Category 7

The rare examples where the evidence is incontrovertible. Organisms preserved in close association, but not actually in position. Arguments based on functional analogy with closely related taxa. Fairly certain, based on known behaviour of living analogues. Less certain due to the producer of evidence being unknown. High degree of uncertainty about the maker. Examples where modern biogeographic evidence is crucial. Fairly speculative, such as functional determinations of wholly extinct taxa. Highly speculative, little reliability.

Of the two examples given above, I would place the Ordovician crinoidivorous chiton in Boucot’s Category 2A and would change it to Category 1 if a modern analogue was discovered. Predation on the arms of Palaeozoic crinoids is best assigned to Category 4 or, perhaps, 5A.

3. SOME EXAMPLES The structure of this paper was determined by personal preference. It could have written as the echinodermal parts of Conway Morris (1981) brought up-to-date, a revision of the parasitism parts of various reviews of echinoderm taphonomy (such as Meyer and Ausich, 1983; Donovan, 1991b) or a parasitism paper modelled on the review of predation on crinoids by Baumiller and Gahn (2003). Rather, I have something a little different in approach from all of these, preferring to focus on a few selected examples from my own experience rather than a review that attempted to be too broad and, in consequence, lacked detail. Actual examples of putative parasitic infestations of fossil echinoderms are desirable at this stage to demonstrate something of the range of evidence available and how it has been interpreted. Most of the examples lean heavily on my own research, which explains why they preponderantly concern my beloved crinoids. I consider it preferable to discuss the familiar in this review than try to spread the text too thinly across the many extinct and extant classes of echinoderms. My intention here is to demonstrate broad principles that can be extrapolated to a reader’s own investigations.

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3.1 A coralecrinoid association from the Mississippian (Figure 2) Material, locality and horizon: BMNH EE5797 (Figure 2) is from Salthill Quarry, Clitheroe, Lancashire [SD 7550 4265], England, one of the most important localities for Mississippian (Lower Carboniferous) echinoderms in north-west England (Donovan et al., 2003; Kabrna, 2011). The crinoid theca was found in the Cover Mudstone, present at the top of the lower Viséan (¼ upper Chadian) Salthill Cap Beds of the Bellman Limestone Member. Description: (Based on Donovan et al., 2005, pp. 43e44.) BMNH EE5797 is an undeformed calyx (Figure 2(a) and (b)) of the monobathrid camerate crinoid Amphoracrinus gilbertsoni (Miller in Phillips, 1836). Preservation of camerate crinoids as their golf ball-like thecae, lacking most if any of the contiguous arms and stem, is common at this locality. The most noticeable variance is that Wright (1955, p. 195) noted ‘. posterior interbrachial area [¼ CD interray] much wider than the others .’ BMNH EE5797 has an AB interray that is almost as wide as the CD interray at the level of the base of the free arms; the other three interrays are narrower and all of about the same width. The solitary rugose coral may be a zaphrentoid (Mitchell, 2003). It is small in comparison to the crinoid calyx. It is preserved in transverse section (Figure 2(c)) and is apparently less than 2.0 mm high, although it has obviously been depressed into the crinoid calyx as indicated by a series of more or less concentric fractures. More precise systematic identification has not been possible on the basis of this single section. The coral is situated in the AB interray, in close contact with the anterior branch of the B ray arm. Discussion: There are a number of lines of evidence to indicate that the solitary coral was attached to the crinoid calyx in life (Donovan et al., 2005), although an actual attachment area per se is not clearly apparent and, assuming it to be present, could only be exposed by destructive techniques. The corallite is small (Figure 2(c)). Although solitary rugose corals were typically unattached in adulthood, as larvae (and, plainly, in subsequent early growth stages) they were capable of cementation to a variety of hard substrates (see, for example, Hubbard, 1970, p. 203). The coral corallite is preserved more or less perpendicular to the surface of the crinoid calyx and has been pushed into it, being surrounded by concentric cracks which have broken across plates, probably due to post-depositional

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Figure 2 (aec) BMNH EE5797, Amphoracrinus gilbertsoni (Miller, 1821, in Phillips, 1836), encrusted by a solitary rugose coral. (After Donovan et al. (2005), Figure 1.) Scale bars represent 10 mm. (a) Theca of crinoid. A ray (¼ anterior) central; note the coral in the AB interray (left) at the same level as the base of the free arms. The anal pyramid is subapical and situated about mid-way between the apex of the tegmen and the arms on the opposite side of the specimen to the A ray (¼ CD interray). Note that the AB interray is broader than the EA interray (right of A ray arm). (b) Apical view. A ray (¼ anterior) towards top of page, AB interray upper right, CD interray (posterior) towards bottom of page. Note regular pentagonal outline of undeformed specimen. (c) The corallite of the coral. Note how the curved breakage of the crinoid around the coral follows the outline of the coral theca and has not resulted in disarticulation of plates. (def) BMNH E71430, Synbathocrinus conicus Phillips, 1836, dorsal cup and proximal column, with single borehole of Sedilichnus paraboloides (Bromley, 1981). Scale bar represents 5 mm. (d) Lateral view with E ray central. Note boring and oral surface sloping anteriorly (that is, to left). (e) EA interray central, showing the prominent boring in the R:R:B plate triple junction (compare with Figure 3(a)). (f) D ray, showing slope of oral surface towards EA interray (compare with Figure 3(b)).

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compactional strain. Although the position of the coral on the crinoid could be merely coincidence, the unusual width, which we interpret as growth rather than postmortem deformation (Figure 2(b)), of the AB interray is reminiscent of the sorts of deformities that are known to be induced in echinoderms by interactions with encrusting organisms (Meyer and Ausich, 1983). All these lines of evidence support the supposition of an original biotic relationship between the host crinoid and its attached coral in life; that is, the living coral was an epizoozoan (sensu Taylor and Wilson, 2002) on the living crinoid. In the Mississippian of the British Isles, it is more common to find crinoids, particularly their columns, encrusted by colonial tabulate corals than by either solitary or colonial rugose corals (see, for example, Donovan and Lewis, 1999). The close association of A. gilbertsoni with a solitary rugose coral would thus be worthy of comment under any circumstances, but it is the position with respect to the crinoid calyx and the presumed life orientation of the latter that excites particular comment. In attaching to the calyx of a crinoid, the solitary coral has gained an advantage from its elevated position would have been above the turbid bottom layers of the water column, so water currents would have been essentially sediment free. The importance of feeding is further emphasized by the corallite being hard against the B ray arm in the AB interray. The A ray is anterior and, if A. gilbertsoni formed a parabolic filtration fanlike modern rheophilic crinoids (Macurda and Meyer, 1974), the coral would have been directed into the clean water currents, being positioned up-current from the anal pyramid. The situation in close contact with the B ray arm is at least suggestive that the coral may have actively harvested food with its tentacles from the adoral groove of the crinoid’s arm. Although obviously speculative, this supposition is supported by the unusual width of the AB interray, a growth deformity which probably resulted from a reaction to the coral and prevented it from interfering with the feeding activity of the A ray arm, too. The available evidence is at least highly suggestive that this coral was both a filter feeder and a parasite on the crinoid. Reliability: Category 1 or 2B. Boucot (1990, p. 9) stated (Category 2B) that ‘With organisms belonging to extinct higher taxa [such as rugose corals and camerate crinoids] functional analysis of behavior from morphology is clearly less reliable’. But other groups of crinoids and stony corals are extant and well known, so Category 1 is at least plausible.

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3.2 A growth deformity in a Mississippian crinoid (Figures 2(def) and 3) Material, locality and horizon: BMNH E71430 (Figures 2(d) and 3) is from Salthill Quarry, Clitheroe, Lancashire [SD 7550 4265], England (Donovan et al., 2003; Kabrna, 2011; Section 3.1 herein). The crinoid theca was found in the lower Viséan (¼ upper Chadian) Salthill Cap Beds of the Bellman Limestone Member. Description: (Based on Donovan, 1991a, p. 2.) The specimen is a dorsal cup, with the two most proximal columnals of the column, of the disparid crinoid Synbathocrinus conicus Phillips, 1836 (Wright, 1952, pp. 134e136, pl. 36, Figures 10, 21 and 22). The cup has been bored once, in the EA interray, at the triple suture between the E and A radials, and the basal in the EA interray (Figures 2(d) and 3(a, b)). The boring is circular with a rounded margin; the cavity is a conical, flat-bottomed pit which does not break through into the body cavity and is assigned to Sedilichnus paraboloides (Bromley, 1981). The cup is not swollen around the excavation, unlike the common reaction to borings seen on some crinoid columns from the same site, but the cup is less developed on the bored side, the oral surface sloping towards the EA interray (Figures 2(f) and 3(b)).

Figure 3 BMNH E71430, Synbathocrinus conicus Phillips, 1836. (a, b) Camera lucida drawings of the dorsal cup and proximal column. (After Donovan (1991a), Figure 2.) Scale bar represents 5 mm. (a) EA interray central (compare with Figure 2(e)), showing the position of the boring. (b) DE interray central, showing how the oral surface slopes down towards the region of infestation, presumably a growth reaction to the disturbance. Key: RR ¼ radial circlet; BB ¼ basal circlet; COL ¼ most proximal part of column. (c) Schematic oral view based on BMNH E71430. (After Donovan (1991a), Figure 3.) Carpenter rays (AeE) indicated, corresponding to the positions of the arms; X is the position of the anal series (¼ posterior). Small arrows mark positions of cryptic B:B:R plate triple sutures; large arrows mark positions of prominent R:R:B plate triple sutures. Key: 1 ¼ in the same position of the anal series; 2 ¼ adjacent to the anal series; 3 ¼ distant from the anal series; * ¼ position of boring. Current flow would have been from the top of the page.

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Discussion: Borings in the cup of Synbathocrinus are rare. Brett (1978) suggested that pit-forming organisms on Palaeozoic crinoids were host specific; I have looked at hundreds of specimens of this genus, from the Mississippian of North America and Europe, and the Permian of Timor, for almost 25 years and have failed to find a second bored specimen. The excavating organism selected its site with some precision. That the boring was made in a live crinoid is undoubted, with growth proceeding with greater vigour on the side opposite to the pit (Figures 2(f) and 3(b)). In life, all sides of the cup would have been equally available for infestation by borers and encrusters with the crown elevated above the substrate. The boring was made precisely at the triple suture between two radial (R) and a basal plates (B) (Figures 2(d) and 3(a)). The three B:B:R triple junctions, in the A, C and E rays are cryptic and can only tentatively be distinguished; in contrast, the five R:R:B sutures are readily apparent (Figures 2(def) and 3(c)). Sutures between plates, bonded together by collagenous ligament fibres, would have been easier to bore into, either mechanically or chemically, than the solid calcite of the plates; therefore, the position of S. paraboloides is interpreted as a choice made for ease of infestation by the boring organism, the identity of which remains unknown. Why bore into the EA interray, rather than at one of the four other triple plate sutures? The sutures labelled 3 in Figure 3(c), in the EA and AB interrays, are the most up-current (¼ anterior) plate triple junctions and, thus, they are also the potential borehole sites most removed from the anal series (X). This suggests that the pit-forming organism was not a coprophage. The most probable life strategy of the pit-former was as a hard substrate dweller that fed by filtration (compare with Brett, 1978, 1985). It would be attached to the highest ‘fixed’ point of the crinoid, just below the oral surface and the arms, and always orientated into the prevalent current by the crinoid. It is presumed to have removed part of the suspended particulate food that would otherwise have been ingested by the crinoid. Whether this contributed to the deformation of the cup or it was mainly a reaction to the formation of the pit must remain uncertain. Reliability: Category 4. ‘For some types of behavioral evidence there is an even larger degree of uncertainty about the maker of this evidence. This is particularly true for many trace fossils’ (Boucot, 1990, p. 9). No determination of the borer can be made apart from that it was small, unmineralized and probably a filter feeding invertebrate.

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3.3 Epizoobionts infesting a Mississippian crinoid (Figure 4) Material, locality and horizon: BMNH EE8728 (Figure 4) is from Salthill Quarry, Clitheroe, Lancashire [SD 7550 4265], England (Donovan et al., 2003; Kabrna, 2011; Section 3.1 herein). The crinoid theca was found in the Cover Mudstone, present only at the top of the lower Viséan (¼ upper Chadian) Salthill Cap Beds of the Bellman Limestone Member.

Figure 4 Multiple Sedilichnus paraboloides (Bromley, 1981) infesting the dorsal cup of the Lower Carboniferous crinoid Amphoracrinus gilbertsoni (Miller in Phillips, 1836), BMNH EE8728. (After Donovan et al. (2006), Figure 1.) (a) Base of dorsal cup, D-ray towards top of page. (b) Enlargement of (a), showing how pits are concentrated on plates, not crossing sutures. (c) Enlarged lateral view of (mainly) dorsal cup, E-ray central, showing sub-horizontal arrangement of closely spaced pits. (d) Theca in lateral view, same orientation as (c). Note absence of pits above the line of the arm facets. Specimen whitened by ammonium chloride. Scale bars represent 10 mm (a, d) or 5 mm (b, c).

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Description: (Based on Donovan et al., 2006, pp. 43e44.) The reader has already been introduced to A. gilbertsoni and S. paraboloides (see above). This description will concentrate on the pattern of infestation of pits on the crinoid theca (Figure 4). The theca preserves the dorsal cup, fixed arms and tegmen. Sedilichnus paraboloides is found on all plates of the dorsal cup (basal and radial circlets), not including the articular facet for the column (Figure 4(a) and (b)); on fixed brachial plates (Figure 4(c)); and on interbrachial plates up to just above the mid-height of the facet for the free arms (Figure 4(c), upper left). There are no pits on the tegmen above this level (Figure 4(d)). The hemispherical pits may be close packed together on individual plates, but are rarely in contact; they do not occur on the depressed sutures between thecal plates, that is, those of the dorsal cup and proximal fixed brachials (Figure 4(c)). Pits (n > 50, all c.1 mm diameter) are common throughout the defined area and ‘bald’ areas seen on some parts of the specimen are covered with pits elsewhere in analogous positions in relation to the arms. The base of the cup is angled to the long axis of the theca and slopes up towards the CD interray. Discussion: This infestation occurred while the crinoid was alive. Most obviously, pits are distributed on the theca, below the level of arms, through 360 , but are not found on articular facet of the column. Thus, the embedding organisms had access to the entire lower half of the theca, but the column facet would have been covered by the column in a living crinoid. The absence of pits on the tegmen above the level of the arms is most easily explained by the crinoid itself keeping this region free of any infestation by the action of the tube feet. These are situated on the adoral surface of the free arms, enabling them to ‘clean’ the tegmen, but not the region below arm level. Presumably, the proximal column and aboral surfaces of the free arms, which are not preserved, could also have been infested. Further, there is evidence for a growth deformity, that is, the sloping base of the theca, which is analogous to the specimen of S. conicus described above (Section 3.2). The palaeoecology of the pit-forming organism is, in part, decipherable, even if its identity remains obscure. There is the obvious segregation of S. paraboloides on the substrate (see above), indicating that they were unable to survive the attentions of the tube feet. The pits are concentrated on the more elevated parts of the lower half of the theca, that is, they occur on the more concave, central areas of plates (Figure 4(b) and (c)). The plate sutures, which would presumably be easier regions for embedment (Section 3.2), are

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avoided; these sutures are sunken between the plates, so it is probable that the small difference in height between sutures and plate centres was important to the producers. This strongly supports a suggestion that they were filter feeding. Interestingly, S. paraboloides is distributed on the lower part of the theca through 360 , and is apparently not selective with respect to the life orientation of the crinoid, there being no obvious preference for anterior (A-ray) or posterior (CD-interray) (but see Section 4, ‘Discussion’, below). Pits are close packed, but in only very few instances overlap, suggesting that this represents a gregarious accumulation of an organism that thrived on elevated calcareous substrates, rather than successive pits formed by one or a few individuals (compare with Donovan and Lewis, 2010). Reliability: Category 4 (compare with Section 3.2) or 7, ‘. so highly speculative as to have little reliability at all .’ (Boucot, 1990, p. 9). The sloping base of the theca is analogous to the example of S. conicus, above, in which a single pit is interpreted as engendering the aberration. In the present example, with the theca heavily covered by borings below arm level, there seems little connection between a growth deformity and an infestation through 360 . The pits would have gained advantages attached to an elevated cup, but any evidence that the association may have been parasitic is masked by the dense accumulation of pits. The pit producer may have been conspecific with that in Section 3.2; the specimens are from the same locality.

3.4 Platyceratid gastropods infesting Upper Palaeozoic crinoids (Figures 5 and 6) Material, locality and horizon: All specimens are members of the monobathrid camerate genus Neoplatycrinus Wanner, 1916, from the Permian of West Timor. RGM B9, Neoplatycrinus major Wanner (Figure 5(a) and (b)), from Basleo (Charlton et al., 2002, Figure 2), Noil Tonini, West Timor (presumably about sites 6e8 of Webster, 1998). RGM ST.32842[1], Neoplatycrinus dilatatus Wanner, 1916 (Figure 5(cef)), comes from Toenino. RGM T.4439[1], Neoplatycrinus sp. cf. N. dilatatus Wanner (Figure 5(g)), no associated locality data. RGM T.3851[1], N. dilatatus Wanner (Figure 6(aec)), no associated locality data. Description: (After Donovan and Webster, 2013, pp. 990e991.) The gross morphologies of the Neoplatycrinus crinoid species from West Timor were described in Wanner (1916); herein, only the modifications to the geometry of the form of the CD (posterior) interray in a few specimens are described. Two broad morphologies are identified, one centred below (Figure 5(a)) and the other centred on the periproct. RGM B9 has a theca

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Figure 5 Homing scars of platyceratid gastropods (Lacrimichnus? isp.) on Permian platycrinitid crinoids from West Timor. (After Donovan and Webster (2013), Figure 1.) (a, b) RGM B9, Neoplatycrinus dilatatus Wanner, 1916, posterior (CD interray central) and anterior (A ray central) views of theca, respectively. Note deeply sunken homing scar. (cef) N. dilatatus Wanner, 1916, RGM ST.32842[1]. (c) Posterior view, depressed CD interray central. (d) Lateral view, B ray slightly left of central, note posterior flattening of theca (right). (e) Anterior view, A ray central. (f) Basal view, posterior towards top of page. (g) RGM T.4439[1], Neoplatycrinus sp. cf. N. dilatatus Wanner, 1916, CD interray viewed slightly obliquely from below and showing deep depression in radials. Specimens uncoated. All scale bars represent 10 mm.

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Figure 6 Platycrinitid crinoids and platyceratid gastropods. (aec) Neoplatycrinus dilatatus Wanner, 1916, RGM T.3851[1], Permian of West Timor. (After Donovan and Webster (2013), Figure 3.) (a) Posterior view (CD interray central) showing depressed area around periproct, Lacrimichnus? isp., and on the C and D radials, extending onto basal circlet. (b) Anterior view, A ray central. (c) Lateral view, BC interray central, note posterior flattened in this view (left) and sloping towards base. (def) Platyceratid gastropod preserved on the tegmen of Platycrinites s.s. wachsmuthi (Wanner, 1916). (After Webster and Donovan (2012), Figure 1(aec).) (d) Posterior view. (e) B and C interray. (f) Oral view. Specimens uncoated. Scale bars represents 10 mm.

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that is typically bulbous anteriorly (Figure 5(b)), but, viewed from the side (BC and DE interrays), the CD interray is flattened and slopes down to the basals, slightly protruding just below the level of the arms. The radials of the CD interray bear a prominent sub-circular groove, c. 8.9e9.7 mm in diameter, situated below the periproct and more on the D than C radial (Figure 5(a)); a comparable structure was illustrated by Wanner (1916, pl. 99, Figure 1(a)). The central area is flattened on the C side and onto the D, but otherwise slightly raised. Sutures between the radials are poorly apparent in this region. Outside the groove, the test is sculpted by two (D) or three (C) sub-concentric raised ridges. These structures do not encroach onto the basal circlet. This suggests that they were not produced by the shell of the epizoozoic snail (sensu Taylor and Wilson, 2002), which would not have been so careful as to avoid adjacent plates in this manner. Rather, they are more likely a stereom response to gastropod infestation (compare with, for example, Grygier, 1988; Eckert, 1988; Grygier and Nomura, 1998; amongst many others). The other three thecae (Figures 5(ceg) and 6(aec)) have a similar structure to each other, albeit a little different from RGM B9. These three thecae are distinctly truncated posteriorly (Figures 5(d, f) and 6(c); as is also RGM B9). The radials in the CD interray form a depressed region below the periproct, like an inverted triangle with bowed sides, with the lateral extent determined by the positions of the arm facets. These depressed regions are approximately parallel-sided to convex below the arms (Figures 5(c, g) and 6(a)), becoming constricted towards the base of the thecae. The plate triple junction between the C and D radials, and the supporting CDeDeDE basal are depressed. RGM T.3851[1] (Figure 6(aec)) has the most rounded depressed region with a shallow, sub-circular groove apparently extending around the periprioct. Comparable structures are not apparent on RGM T.4439[1] and ST. 32842[1] (Figure 5(c) and (g)). Discussion: The coprophagic/parasitic relationship between the platyceratid gastropods, and Palaeozoic crinoids and blastoids has been recognized for over 140 years. It persisted from at least the Middle Ordovician to Permian (Bowsher, 1955; Conway Morris, 1981, p. 499; Meyer and Ausich, 1983, pp. 401e403, Figure 5; Baumiller, 1990, 1993; Boucot, 1990; Donovan, 1991b, pp. 251e252; Gahn and Baumiller, 2003, 2006; amongst others). The mollusc is commonly preserved surmounting the anal opening (Figure 6(def)) where it produces no stereom overgrowth (but sometimes a ‘scar’), presumably because the platyceratid is vagile. Bowsher (1955) considered the platyceratidepelmatozoan association to be obligate commensalism, the gastropod being a coprophage, feeding on the echinoderm’s excrement.

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Yet Rollins and Brezinski (1988) demonstrated that crinoids with platyceratid infestations tend to be smaller than those without associated gastropods, thus indicating that the association was detrimental to the host, that is, parasitic. The platyceratid may have utilized the detritus concentrated by the filtration fan of the crinoid. Further, Baumiller (1990) demonstrated that some platyceratids drilled into the crinoid tegmen, which further suggests a parasitic association (see also Baumiller, 1993; Baumiller et al., 1999). One of the common associations by platyceratids in the Late Palaeozoic was with the platycrinitid monobathrid camerates. The Permian of West Timor has provided some of the youngest specimens to demonstrate this interaction (e.g. Wanner, 1937, pl. 11, Figures 7 and 8; Baumiller et al., 2004, pp. 393e395, Figure 1; Donovan and Webster, 2013). Specimens from Timor discussed by Webster and Donovan (2012) either preserved (or, at least, preserved evidence of) platyceratids on the tegmen or along the radial summit of the platycrinitids Platycrinites Miller and Neoplatycrinus Wanner (Figure 6(def)). The specimens described above do not retain any platyceratid shells, but instead show evidence of different patterns of infestation in the CD interray of the theca first discussed by Donovan and Webster (2013). In these associations, the crinoid thecae show distinct modified morphologies, presumed to have been formed in response to the gastropod infestation; whether these changes also altered the feeding capabilities of the crinoids is equivocal. Part of the fascination of this association is its age; ‘Hard substrate communities are poorly known in the Permian’ (Taylor and Wilson, 2003, p. 48). The circular structures (Figure 5(a)) and depressed areas (Figures 5(c, g) and 6(a)) of abutting C and D radials on the Neoplatycrinus thecae described above are interpreted to be the results of the crinoids reacting to infestations by platyceratid gastropods. Unlike other examples known from the Permian of West Timor (Wanner, 1937; Baumiller et al., 2004; Webster and Donovan, 2012; Figure 6(def) herein), these snails were attached subapically in the CD interray rather than apically on the tegmen or adjacent to it. This was undoubtedly, at least in part, due to the posterior position of the periproct of Neoplatycrinus. Note that these patterns of infestation are differently positioned, either below the periproct, or extending between the C and D arms to include the periproct. The two broad morphologies of CD interray described are thus indicative of differing positions chosen by the infesting gastropods and reactions engendered by their hosts. Most obviously, the circular scars indicate the homing positions of the producing gastropods (compare with Boucot,

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1990, Figure 8). These scars are prominent external modifications of the crinoid’s endoskeleton. They may be the result of abrasion by the edge of the aperture of the gastropod shell or chemical etching (Bromley, 2004, p. 463), irregular growth of stereom as a reaction to this by the crinoid or, most probably, a combination of all of these. For example, RGM B9 (Figure 5(a)) has both a deeply depressed, circular groove (situated below the periproct; contrast with Figure 6(a)), but also concentric raised ridges outside it. The former is presumably produced (mainly) by the gastropod, the latter by the crinoid, raised above the level of the adjacent theca. It is considered unlikely that these concentric structures represent occupancy by successively larger platyceratids through time, although they could reflect the growth of a single individual gastropod. Despite these modifications, the gross, slightly inflated morphology of the crinoid theca is retained, except posteriorly. The gastropod must have stood proud of the surface of the theca, presumably giving the CD interray, an inflated appearance in life. Whether the gastropod remained in this position at least semipermanently is unknown, but these modifications to the crinoid suggest that it was at least likely. Figure 6(def) shows a platyceratid gastropod from this locality so that its size and shape e low, moderately broad and cap-like e may be compared to the other illustrations herein; its position on the theca is in sharp contrast to where snails must have infested in Figures 5 and 6(aec). The round groove in the radials in the CD interray is a trace fossil that is close in morphology to Lacrimichnus Santos et al., 2003, based on Neogene gastropod attachment scars. Jagt (2007) identified an older Lacrimichnus? isp. on a barnacle plate from the upper Maastrichtian of the type area. Lacrimichnus? isp. is also applied as an ichnotaxonomic name to the round scars produced by Permian capuliform platyceratid gastropods, such as the specimens illustrated herein and by Boucot (1990, Figure 8). This would rescue such trace fossils from the limbo that referring to them as circular grooves engenders (compare with discussion by Donovan and Pickerill, 2004, p. 483). Although produced by acorn barnacles rather than gastropods, the ichnogenus Anellusichnus Santos et al., 2005, is broadly similar to Lacrimichnus, but typically has an undulating outer furrow. The second morphology described above involves the CD interray of the crinoid being depressed, more so than in RGM B9, but without obvious homing scars except, possibly, faintly in RGM T.3851[1] (Figure 6(a)). Commonly, the test of uninfested Neoplatycrinus is bulbous, conical or bowl-shaped. Infested tests retain this geometry in anterior

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view (Figures 5(e) and 6(b)), but, in other views, there is a marked flattening posteriorly (Figures 5(d, f) and 6(c)), giving the test a prominent anteriore posterior asymmetry, although remaining bilaterally symmetrical along a mirror plane AeCD (that is, anterioreposterior). Such flattening is only developed in the CD interray, that is, posteriorly. This is interpreted as a different expression of infestation by a platyceratid. The depressed CD interray produces a marked change in thecal gross morphology, but, in life, the shell of the coprophagic platyceratid would have been positioned here, presumably filling the depression. The shells of these gastropods are low and cap-like (Bowsher, 1955; Boucot, 1990, Figures 10e13; Webster and Donovan, 2012, Figures 1(aec) and 2(deh); Figure 6(def) herein). It may have been that the gastropod in part ‘restored’ the gross morphology of the theca with its shell by filling the depressed area. That is, with a shell in place in the depressed CD interray, the combined morphology of crinoid þ gastropod may have approximated that of an uninfested theca. The same may be true for the (less depressed) RGM B9. This interpretation is speculative, but could be tested by a carefully defined experiment in a flume tank. If this supposition is accepted as possible, the question must be asked why was it advantageous to host, coprophage or both? The gross morphology of the crown presumably played a part in ensuring water currents for feeding reached the arms (Jefferies, 1989). If, as I suggest, the platyceratid ‘filled the gap’ in the theca, made as a response by the crinoid to the snail’s presence in the CD interray, then the more or less restored hydrodynamics of the crown would have engendered more efficient suspension feeding by the crinoid. This would have resulted in greater production of faeces which, in turn, would have benefitted the gastropod. But, overall, the relationship was probably more parasitic than mutualistic. Such a relationship was more than casual, and the modifications of the theca that favoured this crinoidegastropod association were probably developed early and retained throughout life. The two morphologies of CD interray seen in Neoplatycrinuseplatyceratid associations are indicative of two different patterns of infestation. The depressed CD interrays (particularly Figures 5(c, g) and 6(a)) suggest a mode of infestation in which the gastropod extended between the C and D arms, perhaps covering the periproct. This arrangement suggests a long-term relationship between crinoid and gastropod, the former showing large thecal modifications to accommodate the snail.

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In contrast, other Neoplatycrinus grew to produce a typically radially symmetrical theca with no depressed regions in any ray. If, in maturity, such a theca became infested, the thecal outline could not be modified as much and the CD interray developed a homing scar morphology, positioned below the periproct and not between the arms, that is, somewhat different in gross form (for example, compare Figure 5(a) with Figures 5(c, g) and 6(a)). It is an axiom within the life sciences that, when a host goes extinct, so does its biota of parasites and commensals specific to that host (Vickery and Poulin, 1998; Dobson et al., 2008; Dunn et al., 2009). When the camerate crinoids went extinct at the end of the Palaeozoic, presumably so did the associated platyceratids. However, this may not have brought to an end this biotic association that spanned over 200 million years. Although the camerates became extinct, platyceratids persisted at least until the Late Triassic (Bandel, 1992, 2007; Bandel and Frýda, 1999) or even Mid Jurassic (Carmel Limestone of Utah; P.D. Taylor, written comm.), although their associations with Mesozoic crinoids, if any, are equivocal. Reliability: ‘Category 1 for those taxa found in place on a host pelmatozoan. Despite the fact that the platyceratids and their host pelmatozoan taxa are extinct, there is enough information provided by a wealth of specimens preserved in situ to leave little doubt about the reliability of the basic coprophagous relation. Platyceratids found unassociated with pelmatozoans pose the serious question concerning whether or not all platyceratids were coprophages. It appears most reasonable to conclude that only those platyceratid taxa closely associated with pelmatozoans were potentially coprophages, and that only those platyceratid taxa actually found in situ on a host pelmatozoan may be safely considered to have been coprophages’ (Boucot, 1990, p. 26). Specimens described herein with gastropod shell scars in the CD interray might be considered Category 3 based on the above arguments.

3.5 Site selectivity of pits in echinoid tests, Upper Cretaceous (Figure 6) Material, locality and horizon: Many specimens of the holasteroid echinoid Hemipneustes striatoradiatus (Leske, 1778) infested by the nonpenetrative pit Sedilichnus excavatus (Donovan and Jagt, 2002) in the NHMM collections, including those discussed and illustrated by Donovan and Jagt (2002, 2005; Figure 7 herein). The two specimens discussed in detail below are bored and encrusted tests from the uppermost Maastrichtian (Upper Cretaceous) of southern Limburg, the Netherlands. NHMM RZ

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Figure 7 Holasteroid echinoid Hemipneustes striatoradiatus (Leske, 1778) and the pits Sedilichnus excavatus (Donovan and Jagt, 2002), all Upper Cretaceous (Maastrichtian) of the Netherlands and Belgium. (After Donovan and Jagt (2002, Figures 2(a, c), 3(a, b) and 5(aee).) (a, c, d) NHMM MK 4689. (a) Apical view, showing holotype (arrowed) and paratype borings. (c) Holotype (arrowed) with two paratypes. Scale bar represents 5 mm. (d) Paratype with outline partly controlled by adjacent ambulacral column. Scale bar represents 5 mm. (b) NHMM 699, right lateral view, paratypes; note the linear arrangements of some groups of borings. (e, i) NHMM RN 452b, profile (test external surface to left) and internal surface. (f, h) NHMM RN 452c, profile (test external surface to left) and internal surface. (g) NHMM RN 452a, internal surface. Scale bars represent 10 mm unless stated otherwise.

00162 (Figure 8(aee)) is from the base of subunit IVf-6 of the Meersen Member, Maastricht Formation, at the former Blom quarry, Berg en Terblijt (for locality map, see Donovan et al., 2011a, Figure 1). NHMM MA 0234-1 (Figure 8(feh)) is from the same subunit (IVf-6), but from the nearby Ankerpoort-Curfs quarry, now defunct, near Geulhem. Description: (Based on Donovan and Jagt, 2013b, pp. 113e114) The test of H. striatoradiatus, NHMM RZ 00162, was used as a substrate by a variety of encrusting and boring invertebrates. The oral surface bears three attached pycnodonteine oyster valves in close association; a cheilostome bryozoan colony in the depressed region anterior of the peristome; more than three poorly preserved spirorbid worm tubes; and a slot-like, figureof-eight boring aperture just posterior of the peristome, probably Caulostrepsis isp. (Figure 8(b)). Spirorbid worms occur at or just above the ambitus;

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Figure 8 Holasteroid echinoid Hemipneustes striatoradiatus (Leske, 1778) and the pits Sedilichnus excavatus (Donovan and Jagt, 2002), all Upper Cretaceous (Maastrichtian) of the Netherlands and Belgium. (aee) NHMM RZ 00162. (After Donovan and Jagt (2013b), Figure 1.) (a) Apical surface with the positions of four pits, S. excavatus, marked by asterisks (*). The numerical designation of ambulacra (Roman numerals, IeV) and interambulacra (Arabic numerals, 1e5) is provided as an explanation of the notation used in the text. (b) Oral surface showing episkeletozoans (oysters, bryozoan colony, spirorbids) and annelid boring, Caulostrepsis isp. (c, e) Two views of S. excavatus in ambulacrum 4. (d) Sedilichnus excavatus in ambulacrum V; compare rounded outline to (c, e). (feh) NHMM MA 0234-1. (After Donovan and Jagt (2013b), Figure 2.) All oblique views of the apical surface. (f) Ambulacrum II (right anterior) central with closely grouped pair of S. excavatus pits. (g) Ambulacrum IV (left anterior) right of centre, with one poorly developed S. excavatus in the upper part of the ambulacrum and two further pits, in close association, in interambulacrum 3 (left anterior). (h) Ambulacrum V (left posterior) right of centre with S. excavatus between the columns of pore pairs; other specimens are in interambulacrum 4 (left lateral). An encrusting oyster, situated posteriorly, partly overgrows a S. excavatus (far right). Specimens uncoated. Scale bars represent 10 mm.

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a small circular hole in the posterior column of plates in ambulacrum V (left posterior) is Sedilichnus simplex (Bromley, 1981). On the apical surface (that is, supra-ambitally) are small pits and borings (S. simplex, probable Caulostrepsis isp.), four specimens of S. excavatus (Figure 8(a, cee)), spirorbids and a fragment of a shell that may or may not be encrusting. Only S. excavatus occurs on the upper half of the test. Each S. excavatus is in close association with an ambulacrum of the echinoid. Sedilichnus excavatus occurs within ambulacrum II (right anterior), straddling the perradial suture between the two plate columns (Figure 8(a)). Anterior pores or pore pairs appear weakly developed adapically of the pit. In ambulacrum I (right posterior), S. excavatus is anterior to the anterior pore pairs, straddling the adradial suture with interambulacrum 1 (Figure 8(a)). Again, pores or pore pairs are only weakly developed adapically. In ambulacrum V (left posterior), S. excavatus is lower on the test than either pit on the right side and is anterior to the anterior column of pore pairs, situated adjacent to the adradial suture with interambulacrum 4 (Figure 8(a) and (d)). This is the furthest away from a pore column of any of the four pits; the adjacent pores appear to be normally developed. Each of these first three pits is shallow; they are rounded to subangular rounded in outline. Sedilichnus excavatus in ambulacrum IV (left anterior) is deeper and has straighter walls, the central boss being elongated; it occupies a central position in the ambulacrum, straddling the perradial suture, but abutting the anterior pore column with a straight side (Figure 8(a, c, e)). Pore pairs in the anterior ambulacral column are only strongly developed abapically of this pit. The posterior column of pores is strongly deflected towards this pit. The second specimen, NHMM MA 0234-1 (Figure 8(feh)) is less markedly encrusted, but more heavily pitted by S. excavatus. Other traces include some small pits and perforations, situated apically, and referred to S. simplex and Caulostrepsis? isp. Other scratch marks and excavations of (mainly) ambulacra in this region are probably the spoor of grazing regular echinoids, although typical Gnathichnus pentax Bromley, 1975, is not apparent. Only S. excavatus is considered a pre-mortem infestation. Sedilichnus excavatus is moderately common on this test with 11 pits, 4 of which are closely associated with ambulacra (Figure 8(feh)). The ambulacral infestations are high on the test, as in NHM RZ 00162. However, unlike that specimen, ambulacrum I (right posterior) is not infested, whereas ambulacrum II (right anterior) has two S. excavatus in close association (Figure 8(f)). Ambulacra IV and V (left anterior and posterior, respectively)

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each have one associated pit (Figure 8(g) and (h), respectively). In two interambulacra, pits are vertically one above the other (Figure 8(g) and (h)); in the posterior interambulacrum (5; Figure 8(h), far right, oblique view) a pit sits on the interradial suture at about mid-height of the test, about as far as it is possible to be situated away from an ambulacrum, and partly overgrown by an oyster. Discussion: Donovan and Jagt (2002) erected the ichnospecies Oichnus (now Sedilichnus) excavatus on the basis of locally common infestations of pits in the late Maastrichtian echinoid H. striatoradiatus (Leske). Ample evidence was presented to indicate that this association occurred while the echinoid, which probably lived more or less epifaunally, was alive, most particularly by the growth of internal blisters within the test and beneath the pits (Donovan and Jagt, 2005, pl. 1, Figure 2; Figure 7(eei) herein). Sedilichnus excavatus was diagnosed as ‘Circular to elliptical, non-penetrative Oichnus, almost invariably with a broad, high, raised central boss. Aperture of boring overhanging, and walls concave’ (Donovan and Jagt, 2002, p. 69). The type series and related material of S. excavatus included pits in numerous tests of H. striatoradiatus, some of which were densely infested; most notably, Donovan and Jagt (2002, p. 69, Figure 2(c)) counted ‘at least 61 individual borings’ on NHMM JJ 699. Despite this wealth of material, there was not any strong indication of site selectivity, although some pits did occur in linear associations (Figure 7(b)) and most infested the test supra-ambitally. The two analogous specimens of H. striatoradiatus described above, although relatively sparsely infested by S. excavatus, provide stronger indications that the settling behaviour of the infesting organism was site selective. All encrustations on these tests are interpreted to have occurred after the death of H. striatoradiatus (¼ episkeletozoans sensu Taylor and Wilson, 2002). In life, the tests would have been protected by both densely packed spines and pedicellariae which would have prevented such varied infestations. A holasteroid such as H. striatoradiatus would not have been a deep burrower; rather, it would have lived epifaunally, possibly furrowing through the sediment at the surface. The occurrence of a partial marginal (subanal) fasciole under the periproct points to such a mode of life. Thus, the oral surface would have been in intimate contact with the sediment, precluding infestation of the oral surface of either specimen by oysters, bryozoans, or spirorbid or serpulid annelids (Figure 8(b)). Further, with the exception of S. excavatus, the tests preserve no evidence of the growth of the echinoids being adversely affected by any boring or attachment. Thus,

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the only borings interpreted to be pre-mortem are those of S. excavatus, a deduction which is in agreement with the observations on other specimens infesting this echinoid species by Donovan and Jagt (2002, 2005, 2013b). The four examples of S. excavatus on NHMM RZ 00162 (Figure 8(aee)) show a distinct pattern of infestation not otherwise noted on H. striatoradiatus. This may be because other specimens are either too densely (Figure 7(a) and (b)) or too sparsely infested, or it may be that the present example preserves a rare behaviour (but see Jagt, 2000, pl. 24, Figures 4 and 5). Whatever, in this example at least, each S. excavatus is associated with a different ambulacrum (Figure 8(a)). It is notable that the only ambulacrum (anterior, III) on the apical surface that was not infested is also functionally different from all the others (Smith, 1984, pp. 93e95; Jagt, 2000, p. 281). That is, in NHMM RZ 00162, S. excavatus is only associated with ambulacra bearing well-developed respiratory tube feet, although, as noted above, infestations seem to be associated with reactions by the test. Most notably, the posterior plate column in ambulacrum IV is deflected towards the pit (best seen in Figure 8(e)). There is also a suspicion that in some anterior plate columns of ambulacra (I, II, IV) the pores/pore pairs are weakly developed, but, as these are invariably less prominent than those of the posterior pore pairs, this may equally be a preservational artifact or an inaccurate observation. These observations are supported by the second specimen, NHMM MA 0234-1 (Figure 8(feh)). Although more densely infested by S. excavatus, this test supports four pits in close association with three respiratory regions of ambulacra (II  2, IV, V). These are on the upper half of the test and in positions analogous to those of NHMM RZ 00162 (compare Figure 8(aee) and (feh)). But if a close association with a respiratory ambulacrum was advantageous, it is unknown why seven other O. excavatus infested interambulacra. Two pits are on the interradial suture (Figure 8(f), lower right; Figure 8(h), far right) and all but two (Figure 8(g), centre of image) are located towards the middle of an interambulacrum. Figure 7(a) shows an analogous specimen to NHMM MA 0234-1. However, more densely bored specimens (such as Figure 7(b)) distracted them from recognizing an association between ambulacra and S. excavatus. This association was presumably advantageous to the organisms forming certain S. excavatus, which selected positions to settle on live H. striatoradiatus with precision, either between columns of pore pairs (II, IV, V) or anterior to the anterior column of pore pairs (I, II, V). This pattern begs a palaeoecological explanation, but this must be speculative, particularly as S. excavatus

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also successfully infested other areas of the test. All S. excavatus in Figure 8 are above the mid-height of the test and, thus, were presumably above the sediment surface in this shallowly furrowing echinoid. None of the pits shows a particularly strong association with the well-developed respiratory tube feet situated posteriorly on each of the ambulacra of interest. We suggest, tentatively, that this pattern of infestation may have placed the producers of O. excavatus in advantageous positions to feed on plankton, anterior of the tube feet on an echinoid moving slowly across the seafloor. The function that the respiratory tube feet performed for the producer of O. excavatus is uncertain, but may have been protective in part. Reliability: Category 4. ‘For some types of behavioral evidence there is an even larger degree of uncertainty about the maker of this evidence. This is particularly true for many trace fossils’ (Boucot, 1990, p. 9).

4. DISCUSSION The echinoderms are a promising group of fossils with which to investigate the nature of biotic reactions because the endoskeleton may produce growth deformities of various types if infested in life. Other reviews of parasitism on echinoderms have tried to do too much in a restricted space (such as Kowaleski and Nebelsick, 2003, pp. 294e295, on echinoids); I have aimed to be expansive, but selective. There are some good examples that I have chosen to ignore because they are well covered elsewhere (such as various entries for parasitism on echinoids in Boucot, 1990). Five specific examples are given in this essay, but none belong to the typical swollen deformity for which the echinoderms are so well known (Figure 9) and which have been determined as parasitic infestations by many authors (Moodie, 1918). Although such structures are locally common, I suggest that they are more difficult to interpret than some of the examples discussed in detail herein. Certainly, some modern parasites produce identifiable galls and cysts in echinoid spines, asteroid arms, ophiuroids discs, and crinoid pinnules and cirri (see, for example, Grygier, 1988). But similar pits and swellings may be the result of embedment by an organism that is merely seeking elevation above the substrate. It will gain an advantage, but is it parasitism (Zapalski, 2011)? Pits in the endoskeleton in crinoids and blastoids (such as Figure 9(a)) are difficult to interpret. A crinoid column would provide very little nourishment, so a bored fossil pluricolumnal should best be interpreted as an

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(a)

(b)

Figure 9 (a) Pentagonocyclicus (col.) sp., RGM 544 426 (After Donovan and Lewis (2010), Figure 2.), perforated by three pits. Wenlock Edge, Shropshire [NGR SO 588 980], England; Much Wenlock Limestone Formation, Lower Silurian (Wenlock, Homerian). Note the irregular outline of the pluricolumnal, due to swelling, and the large size and irregular outline of the pit in the centre; the other two pits, including one at the top, are more circular and assigned to Sedilichnus paraboloides (Bromley). Specimen whitened with ammonium chloride for photography. (b) A strongly swollen pluricolumnal, RGM 791 727, in which the living crinoid grew over an encrusting coral. (After Donovan et al. (2014b), Figure 4(g).) Salthill Quarry, Clitheroe, Lancashire [SD 7550 4265], England; lower Viséan (¼ upper Chadian) Salthill Cap Beds, Bellman Limestone Member. Scale bars represent 10 mm.

interaction with an unmineralized invertebrate seeking elevation above the substrate and protection from the environment. (The latter could also be provided by the dead parts of a dead crinoid.) An embedding organism that elicited a reaction by the host to induce stereom growth and produce a more robust, ankylosed structure would be further protected. This surely is not what is commonly interpreted as parasitism. Reasonably, a boring/ embedding parasite sensu stricto would be more likely to infest a crinoid through the more nutritious dorsal cup, tegmen (including the anal tube) and arms, and would have perforated the endoskeleton (Baumiller, 1990) rather than just embedding in it. Even though I have specialized in the systematics and palaeobiology of the crinoid stem for 35 years, I trust it is now obvious why I have included no bloated and bored crinoid stems in the examples that I have given above. If you want to read further on such ancient cysts and galls (reviewed in Conway Morris, 1981; Meyer and Ausich, 1983, pp. 412e414), their literature is both broad and diffuse, and may be overly speculative. Instead, I have concentrated herein on examples of ectoparasites in which there are obvious interactions with the crinoid theca by organisms

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that apparently were exploiting part of the crinoid’s feeding capability sensu lato and one example of a bored echinoid where site selectivity suggests an interaction in life with the ambulacra. In two examples we actually know (or at least have a very strong suspicion of) the producing organism. The interaction between a solitary stony coral and a crinoid theca (Section 3.1) in the Mississippian is an unexpected one. There are strong indications that the coral was interfering with the crinoid’s feeding, including its situation at the level of the base of the crinoid arms and the unusual width of this interray, suggesting that growth of the crinoid was minimalizing the interference by the parasite. What this interference was is the subject of informed speculation and was most probably as simple as robbing food from the adoral grooves of the arms. The coprophagic/parasitic association of platyceratid gastropods and Palaeozoic crinoids is one of the best known organism/organism associations in the fossil record, being based on many hundreds of specimens worldwide. The circular scars on or below the anal pyramid in a posterior position on Neoplatycrinus from Timor, Lacrimichnus? isp. (Section 3.4), provide data on the nature of these associations additional to than commonly available, that is, with the snail astride the anal pyramid on the apical surface. It is apparent from the above examples that sparse infestations provide a more cogent tale of organic interactions than dense infestations, which are more likely to confuse the issue. The crinoid theca with multiple pits through 360 (Section 3.3) preserves excellent evidence of biotic interactions e the pit-forming organisms could not settle on those parts of the theca that could be swept clean by the tube feet of the arms and the theca itself shows a growth deformity (Figure 4) e but was any of it parasitism? To use this example as an excuse for speculation, as in the title of this paper, perhaps the multiple pits in this specimen represent more than one spatfall. All pits are of similar size and spacing, but they could have formed in a progression of multiple reproductive seasons if the producing organism had a much shorter life history than an adult crinoid. The pits of dead producers may even have been recycled by juvenile settlers. But if the earliest pit(s) was solitary or sparse and concentrated on one side of the cup, it may have produced the sloping base as a growth reaction analogous to that in Section 3.2 (Figures 2(def) and 3). Later, perhaps larger spatfalls were excluded from making new pits where the originals were now inhabited by larval ‘squatters’ because of biological constraints determined by the size of the adult organism (¼ regular spacing of pits) and avoidance of sunken plate sutures (Figure 4(b) and (c)). If we think in terms of a progressive

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invasion by pit-forming organisms, the single pit in Synbathocrinus represents the start of an infestation (Figures 2(def) and 3) whereas the densely bored Amphoracrinus is an end point (Figure 4). The earliest invaders can be selective and gain a feeding advantage, indicated by the uneven growth of the cup, as well as elevation above the substrate; one or two spatfalls later, the only advantage available is elevation. Thus, early spatfalls gain a feeding advantage in an optimum position, which produces a growth deformity in the crinoid theca and quite rightly may be regarded as a parasitic reaction. Later spatfalls (this may all have happened over a few weeks or months) did not produce an obvious growth deformity in the cup; was this parasitism or not? The Maastrichtian echinoid H. striatoradiatus (Leske) allows a similar analysis to be made on one species. When originally described by Donovan and Jagt (2002), it was plainly apparent that the pits of S. excavatus were formed while the host echinoid was alive by the evidence of the thickened ‘blisters’ of test calcite beneath them (Figure 7(eei)). The pits themselves are of more complex morphology (Figure 7(c) and (d)) than those infesting either of the pitted crinoids (Sections 3.2 and 3.3) and it can be more confidently proposed that they were produced by members of a single species of unmineralized invertebrate showing a particular boring behaviour. Individual echinoid tests are more or less well infested on the apical surface, particularly the upper two thirds (Figure 7(a) and (b)), the ‘record’ being 61 individual pits, including 2, unusually, on the oral surface. It was readily apparent that the producers of S. excavatus were ‘hitching a ride’ on H. striatoradiatus, a hard substrate that elevated them above the seafloor (in most examples) and permitted them to feed by whatever means. Whether this was parasitism and how so is difficult to determine. Perhaps comparing infested and noninfested tests from a single horizon may indicate a size variance (compare with Rollins and Brezinski, 1988), but no qualitative differences are obvious. Certainly, when first described, there was no suspicion of a host/parasite relationship between H. striatoradiatus and the producer of S. excavatus. Contrast these early deliberations with the sparsely infested tests of H. striatoradiatus described later by Donovan and Jagt (2013b; Figure 8 herein). Take away the ‘noise’ of dense infestation and a pattern appears, particularly in NHMM RZ 00162 (Figure 8(aee)). The four individual pits of S. excavatus are each closely associated with an ambulacrum; only the anterior ambulacrum, of different gross morphology and function, remained without an associated pit (Figure 8(a)). Donovan and Jagt (2013b) deduced that the close association of the pit-forming organism and echinoid

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ambulacra provided some feeding or protective advantage to the borer; either interpretation might be regarded as parasitic, particularly where the ambulacral morphology was deformed as a response (Figure 8(cee)).

5. CONCLUSIONS ‘The fossil record contains many examples of the interactions that occurred between organisms . evidence of interactions may be . cryptic or difficult to interpret, none more so than the evidence of ancient parasitism’ (Littlewood and Donovan, 2003, p. 136). The evidence provided by the endoskeletons of fossil echinoderms may be particularly rich, but difficult to interpret. Too rarely is there a good answer to basic questions; what was the parasite; what was being parasitized exactly and why infest an innutrious structure like a crinoid stem when the real tasty guts of the animal was in the cup? Some structures that give the superficial impression that they were formed by parasites, such as deformities in the crinoid column, are difficult to explain and probably do not represent parasitism per se. Most, at least, probably represent dwelling traces, the pit or gall produced looking like parasitism, but being little removed behaviourally from an encruster attached to the outside of the test which would rarely, if ever, be thought to be truly parasitic. Dense infestations may mask patterns that are apparent in weakly infested specimens. And, in the absence of the producing organism in many examples, which is represented by its trace fossil, a sedimentary structure, we are forced to speculate not just on whodunit, but also what it was that they were doing.

ACKNOWLEDGEMENTS I thank the editors, Tim Littlewood (The Natural History Museum, London) and Kenneth De Baets (Friedrich-Alexander Universit€at, Erlangen), for inviting me to contribute to this volume. I also thank my co-authors of the papers that form the backbone of this contribution for their collaboration and collegial companionship, namely John Jagt (Natuurhistorisch Museum Maastricht), David Lewis (the Natural History Museum, London), Paul Kabrna (Barnoldswick, Lancashire) and Gary Webster (Washington State University, Pullman).

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Bandel, K., Frýda, J., 1999. Notes on the evolution and higher classification of the subclass Neritimorpha (Gastropoda) with the description of some new taxa. Geol. Palaeontol. 33, 219e235. Baumiller, T.K., 1990. Non-predatory drilling on Mississippian crinoids by platyceratid gastropods. Palaeontology 33, 743e748. Baumiller, T.K., 1993. Boreholes in Devonian blastoids and their implications for boring by platyceratids. Lethaia 26, 41e47. Baumiller, T.K., Gahn, F.J., 2003. Predation on crinoids. In: Kelley, P.H., Kowalewski, M., Hansen, T.A. (Eds.), Predator-prey Interactions in the Fossil Record. Kluwer Academic/ Plenum, New York, pp. 263e278. Baumiller, T.K., Gahn, F.J., 2004. Testing predator-driven evolution with Paleozoic crinoid arm regulation. Science 305, 1453e1455. Baumiller, T.K., Gahn, F.J., Savill, J., 2004. New data and interpretations of the crinoidplatyceratid interaction. In: Heinzeller, T., Nebelsick, J.H. (Eds.), Echinoderms. Taylor and Francis, London, pp. 393e398. Baumiller, T.K., Leighton, L.R., Thompson, D.L., 1999. Boreholes in Mississippian spiriferide brachiopods and their implications for Paleozoic gastropod drilling. Palaeogeogr. Palaeoclimatol. Palaeoecol. 147, 283e289. Boucot, A.J., 1990. Evolutionary Paleobiology of Behavior and Coevolution. Elsevier, Amsterdam xxiii þ 725 pp. Bowsher, A.L., 1955. Origin and adaptation in platyceratid gastropods. University of Kansas Paleontological Contributions. Mollusca Article 5, 1e11. Breimer, A., 1978. Recent crinoids. In: Moore, R.C., Teichert, C. (Eds.), Treatise on Invertebrate Paleontiology, Part T, Echinodermata 2, vol. 1. Geological Society of America and University of Kansas press, Boulder and Lawrence, pp. T9eT58. Brett, C.E., 1978. Host-specific pit forming epizoans on Silurian crinoids. Lethaia 11, 217e232. Brett, C.E., 1985. Tremichnus: a new ichnogenus of circular-parabolic pits in fossil echinoderms. J. Paleontol. 59, 625e635. Bromley, R.G., 1975. Comparative analysis of fossil and recent echinoid bioerosion. Palaeontology 18, 725e739. Bromley, R.G., 1981. Concepts in ichnotaxonomy illustrated by small round holes in shells. Acta Geol. Hisp. 16, 55e64. Bromley, R.G., 2004. A stratigraphy of marine bioerosion. In: McIlroy, D. (Ed.), The Application of Ichnology to Palaeoenvironmental and Stratigraphic Analysis, vol. 228. Geological Society Special Publication, pp. 455e479. Charlton, T.R., Barber, A.J., Harris, R.A., Barkham, S.T., Bird, P.R., Archbold, N.W., Morris, N.J., Nicoll, R.S., Owen, H.G., Owens, R.M., Sorauf, J.E., Taylor, P.D., Webster, G.D., Whittaker, J.E., 2002. The Permian of Timor: stratigraphy, palaeontology and palaeogeography. J. Asian Earth Sci. 20, 719e774. Conway Morris, S., 1981. Parasites and the fossil record. Parasitology 82, 489e509. Dobson, A., Lafferty, K.D., Kuris, A.M., Hechinger, R.F., Jetz, W., 2008. Homage to Linnaeus: how many parasites? How many hosts? Proc. Natl. Acad. Sci. U.S.A. 105 (Suppl. 1), 11482e11489. Donovan, S.K., 1991a. Site selectivity of a lower carboniferous boring organism infesting a crinoid. Geol. J. 26, 1e5. Donovan, S.K., 1991b. The taphonomy of echinoderms: calcareous multi-element skeletons in the marine environment. In: Donovan, S.K. (Ed.), The Processes of Fossilization. Belhaven Press, London, pp. 241e269. Donovan, S.K., 2010. Cruziana and Rusophycus: trace fossils produced by trilobites. in some cases? Lethaia 43, 283e284.

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Donovan, S.K., 2013. Curiouser and curiouser: more on reworked Echinocorys (Echinoidea; Late Cretaceous) on the beaches of north Norfolk, eastern England. Swiss J. Palaeontol. 132, 1e4. Donovan, S.K., 2014. Enigmatic branching structures within Upper Devonian crinoids, north Devon, UK. Lethaia 47, 151e152. Donovan, S.K., 2015. When is a fossil not a fossil? When it is a trace fossil. Lethaia 48, 145e146. Donovan, S.K., Jagt, J.W.M., 2002. Oichnus Bromley borings in the irregular echinoid Hemipneustes Agassiz from the type Maastrichtian (Upper Cretaceous, The Netherlands and Belgium). Ichnos 9, 67e74. Donovan, S.K., Jagt, J.W.M., 2005. An additional record of Oichnus excavatus Donovan & Jagt from the Maastrichtian (Upper Cretaceous) of southern Limburg, The Netherlands. Scr. Geol. 129, 147e150. Donovan, S.K., Jagt, J.W.M., 2013a. Aspects of clavate borings in the type Maastrichtian (Upper Cretaceous) of the Netherlands and Belgium. Neth. J. Geosci. 92, 133e143. Donovan, S.K., Jagt, J.W.M., 2013b. Site selectivity of the pit Oichnus excavatus Donovan and Jagt infesting Hemipneustes striatoradiatus (Leske) (Echinoidea) in the type Maastrichtian (Upper Cretaceous, The Netherlands). Ichnos 20, 112e115. Donovan, S.K., Jagt, J.W.M., Goffings, L., 2014a. Bored and burrowed: an unusual echinoid steinkern from the Type Maastrichtian (Upper Cretaceous, Belgium). Ichnos 21, 261e265. Donovan, S.K., Jagt, J.W.M., Lewis, D.N., 2011a. Notes on some trace fossils and other parataxa from the Maastrichtian type area, southeast Netherlands and northeast Belgium. In: Jagt, J.W.M., Jagt-Yazykova, E.A., Schins, W.J.H. (Eds.), A Tribute to the Late Felder Brothers e Pioneers of Limburg Geology and Prehistoric Archaeology, Netherlands Journal of Geosciences, vol. 90, pp. 99e109. Donovan, S.K., Kabrna, P., Donovan, P.H., 2014b. Salthill Quarry: a resource being revitalized. Deposits 40, 32e33. Donovan, S.K., Lewis, D.N., 1999. An epibiont and the functional morphology of the column of a platycrinitid crinoid. Proc. Yorks. Geol. Soc. 53, 321e323. Donovan, S.K., Lewis, D.N., 2010. Aspects of crinoid palaeontology, Much Wenlock Limestone Formation, Wenlock Edge, Shropshire (Silurian). Proc. Yorks. Geol. Soc. 58, 9e14. Donovan, S.K., Lewis, D.N., 2011. Strange taphonomy: Late Cretaceous Echinocorys (Echinoidea) as a hard substrate in a modern shallow marine environment. Swiss J. Palaeontol. 130, 43e51. Donovan, S.K., Lewis, D.N., Crabb, P., 2003. Lower Carboniferous Echinoderms of Northwest England, vol. 1. Palaeontological Association Fold-Out Fossils, 12 pp. Donovan, S.K., Lewis, D.N., Kabrna, P., 2005. An unusual crinoid-coral association from the Lower Carboniferous of Clitheroe, Lancashire. Proc. Yorks. Geol. Soc. 55, 301e304. Donovan, S.K., Lewis, D.N., Kabrna, P., 2006. A dense epizoobiontic infestation of a Lower Carboniferous crinoid (Amphoracrinus gilbertsoni (Phillips)) by Oichnus paraboloides Bromley. Ichnos 13, 43e45. Donovan, S.K., Pickerill, R.K., 2002. Pattern versus process or informative versus uninformative ichnotaxonomy: reply to Todd and Palmer. Ichnos 9, 85e87. Donovan, S.K., Pickerill, R.K., 2004. Traces of cassid snails predation upon the echinoids from the Middle Miocene of Poland: comments on Ceranka and Z1otnik (2003). Acta Palaeontol. Pol. 49, 483e484. Donovan, S.K., Schmidt, D.A., 2001. Survival of crinoid stems following decapitation: evidence from the Ordovician and palaeobiological implications. Lethaia 34, 263e270. Donovan, S.K., Sutton, M.D., Sigwart, J.D., 2010. Crinoids for lunch? An unexpected biotic interaction from the Upper Ordovician of Scotland. Geology 38, 935e938.

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