Urchins in the meadow: paleobiological and evolutionary implications of cidaroid predation on crinoids

� 2008 The Paleontological Society. All rights reserved. 0094-8373/08/3401-0002/$1.00

Paleobiology, 34(1), 2008, pp. 22–34

Urchins in the meadow: paleobiological and evolutionaryimplications of cidaroid predation on crinoids

Tomasz K. Baumiller, Rich Mooi, and Charles G. Messing

Abstract.—Deep-sea submersible observations made in the Bahamas revealed interactions betweenthe stalked crinoid Endoxocrinus parrae and the cidaroid sea urchin Calocidaris micans. The in situobservations include occurrence of cidaroids within ‘‘meadows’’ of sea lilies, close proximity ofcidaroids to several upended isocrinids, a cidaroid perched over the distal end of the stalk of anupended isocrinid, and disarticulated crinoid cirri and columnals directly underneath a specimenof C. micans. Guts of two C. micans collected from the crinoid meadow contain up to 70% crinoidmaterial. Two of three large museum specimens of another cidaroid species, Histocidaris nuttingi,contain 14–99% crinoid material.

A comparison of cidaroid gut contents with local sediment revealed significant differences: sed-iment-derived material consists of single crinoid ossicles often abraded and lacking soft tissue,whereas crinoid columnals, cirrals, brachials, and pinnulars found in the cidaroids are often artic-ulated, linked by soft tissue, and unabraded. Furthermore, articulated, multi-element fragmentsoften show a mode of fracture characteristic of fresh crinoid material. Taken together, these datasuggest that cidaroids prey on live isocrinids.

We argue that isocrinid stalk-shedding, whose purpose has remained a puzzle, and the recentlydocumented rapid crawling of isocrinids are used in escaping benthic predators: isocrinids sac-rifice and shed the distal stalk portion when attacked by cidaroids and crawl away, reducing thechance of a subsequent encounter. If such predation occurred throughout the Mesozoic and Ce-nozoic (possibly since the mid-Paleozoic), several evolutionary trends among crinoids might rep-resent strategies to escape predation by slow-moving benthic predators.

Tomasz K. Baumiller. Museum of Paleontology, University of Michigan, Ann Arbor, Michigan 48109-1079. E-mail: [email protected]

Rich Mooi. Department of Invertebrate Zoology and Geology, California Academy Sciences, San Francisco,California 94103. E-mail: [email protected]

Charles G. Messing. Nova Southeastern Oceanographic Center, Dania, Florida 33004. E-mail: [email protected]

Accepted: 4 September 2007

Introduction

Biotic interactions, especially predation,have been argued as major driving forces ofevolutionary innovation and morphologicalchange among many taxa, and crinoids are noexception. (1) Trends of increasing plate thick-ness and spinosity among Paleozoic crinoids(Meyer and Ausich 1983; Signor and Brett1984), (2) offshore displacement of late Me-sozoic/Cenozoic stalked crinoids (Bottjer andJablonski 1988), (3) origin of autotomy (shed-ding) planes in the stalk and arms of articu-lates (Oji and Okamoto 1994), (4) crawlingand swimming abilities in comatulids (Meyerand Macurda 1977), (5) choice of semi-cryptichabits and nocturnal-diurnal behavior amongcomatulids (Meyer and Macurda 1977), and(6) planktonic and pseudoplanktonic lifestyles have all been attributed to predation

pressure. Some of these trends, though specif-ic to crinoids, have often been used to illus-trate some of the best-known global macro-ecological and macroevolutionary patterns,such as the Mesozoic Marine Revolution (Ver-meij 1977), the Mid-Paleozoic Marine Revo-lution (Signor and Brett 1984; Brett and Walk-er 2002), and onshore-offshore patterns (Bo-ttjer and Jablonski 1988).

In the Recent, data suggest that crinoidsmay be distasteful as food for fishes (Mc-Clintock et al. 1999; Baumiller unpublisheddata; Meyer and Baumiller unpublished data),yet the numerous injuries they suffer indicatethat they are subject to predation (Schneider1988). Direct attacks on crinoids are rarely re-ported, but several instances of crinoid-‘‘pred-ator’’ interactions have been documented. TheClown Triggerfish (Balistoides conspicillum)and Saddled Coralfish (Chaetodon ephippium)

23CIDAROID PREDATION ON CRINOIDS

FIGURE 1. A map of the collecting locality (black square) near the west end of Grand Bahama Island.

have been observed attacking crinoids andwith crinoid arms hanging from their mouthsat Lizard Island, Australia (Meyer et al. 1984;Meyer 1985; Vail 1987). Meyer (1985) also not-ed attacks on crinoids by other reef fishes butsuggested that most were of a nonlethal crop-ping or grazing nature. Grazing on crinoidpinnules by fishes was also noted by Fishelson(1974) and Nichols (1994, 1996). In the latterinstance, the Corkwing Wrasse, Crenilabrusmelops, was observed nibbling off the genitalpinnules of the comatulid crinoid Antedon bi-fida; this might represent an instance of cri-noids sacrificing the energy-rich reproductivestructures rather than the less expendable ca-lyx, as suggested by Lane (1984). Crinoid re-mains have also been identified in the fecal re-mains of Recent and fossil fishes (Zangerl andRichardson 1963; Malzahn 1968; Moy-Thomasand Miles 1971; Meyer 1985; Fabricius 1994).

Although most investigations of crinoid-predator interactions have focused on fish,other marine organisms may also interact an-tagonistically with crinoids. For example,Mladenov (1983) reported a swimming re-sponse in a comatulid when perturbed by thepredatory sea star Pycnopodia helianthoides; healso observed a crinoid arm in the claw of thecrab Oregonia gracilis. Halpern (1970) notedthe presence of crinoid pinnulars in the gut of

the goniasterid Plinthaster dentatus, and Brun(1972) found Antedon bifida as part of the stom-ach content of the starfish, Luidia ciliaris. Nev-ertheless, little attention has been given to theevolutionary importance of non-fish predationon crinoids. The goal of this study is twofold:to provide evidence of predation by the cida-roid echinoids Calocidaris micans (Mortensen1903) and Histocidaris nuttingi (Mortensen1926) on stalked crinoids in the Recent and toconsider the biological role and evolutionaryhistory of stalk shedding and crawling amongstalked crinoids in the context of benthic pre-dation.

Stalked Crinoids as Part of Cidaroid Diet

Studies of stalked crinoids near Little Ba-hama Bank south of Settlement Point (westend of Grand Bahama Island, Fig. 1) in 391–434 m of water were conducted using the John-son Sea Link I and II submersibles (HarborBranch Oceanographic Institute, Fort Pierce,Florida) between February 1991 and October1998. These studies revealed that the cidaroidCalocidaris micans is often associated withdense aggregations (‘‘meadows’’) of stalkedcrinoids, including the isocrinid taxa Endoxo-crinus parrae (Gervais [in Guerin 1835]) andNeocrinus decorus (Wyville Thomson 1864)(Fig. 2A,B). A detailed viewing of tens of

24 TOMASZ K. BAUMILLER ET AL.

FIGURE 2. Still frames showing cidaroids and isocrinids. A, Calocidaris micans near the isocrinid Neocrinus decorus.B, C. micans near the isocrinid Endoxocrinus parrae. C, Two individuals of C. micans with crinoid stalk and cirralsegments; E. parrae in the background. Length of C. micans’ spines � 150 mm.

FIGURE 3. A dissected specimen of Calocidaris micans.Arrow points to the pluricolumnal within the gut. Testdiameter � 50 mm.

hours of video taken with an externallymounted video camera showed that the cida-roid was often associated with stalked cri-noids that had abandoned their upright posi-tion in favor of a prone one. By contrast, in theabsence of the cidaroid, crinoids maintainedtheir normal, upright feeding postures (Fig.2B). In one set of close-up video frames, a C.micans could be seen with pieces of crinoid cir-ri underneath (Fig. 2C).

Three individuals of Calocidaris micans werecollected in October 1998 and dissected onboard the R/V Edwin Link. Analyses of theirgut content revealed that, in addition to calcitepellets, coral fragments, and bryozoans, twospecimens contained crinoid stalk elementsincluding columnals and cirri (Fig. 3). Crinoidelements constituted 72% of gut content byvolume in one specimen (C. micans 1), and 6%in a second (C. micans 2); none were found inthe third (Table 1). Crinoid elements representa strikingly high percentage of material in

those guts containing them. By contrast, theycontribute less than 1% by volume to sedimentat this locality. In fact, even when only thosesediment samples containing coarse material(�2 mm) are considered, crinoid elementsrarely constitute more than about one-third ofthe coarse fraction (Llewellyn and Messing1993). Thus, the percentage of crinoid materialin the gut alone suggests that these cidaroidsmay have been actively feeding on live cri-noids rather than incidentally ingesting cri-noid debris while deposit feeding.

Further support for cidaroids having in-gested parts of live crinoids rather than theirdead remains comes from the proportion ofmulti-element, articulated crinoid segmentsfound in their guts. C. micans 1 and C. micans2 contain individual cirrals and columnals aswell as articulated segments of several to asmany as nine columnals long (Fig. 4). Sedi-ment samples, on the other hand, contain pre-dominantly individual crinoid ossicles, as ex-pected given that the ligaments and musclesthat hold together the crinoid skeleton disin-tegrate rapidly after death (e.g., Meyer andMeyer 1986; Baumiller et al. 1995; Baumiller2003). A chi-squared test comparing the de-gree of articulation of crinoid ossicles in thesetwo cidaroids and in the sediment revealedthat cidaroids contain significantly more ar-ticulated material (C. micans 1, p � 0.005; C.micans 2, p � 0.0001). This implies that thesecidaroids attacked living crinoids and con-sumed articulated skeletal components notlong before capture (although we do not knowhow long this material is processed in the ci-daroid gut).


TABLE 1. Data on gut contents of the two cidaroid species examined, Calocidaris micans and Histocidaris nuttingi.

C. micans 1 C. micans 2 C. micans 3 H. nuttingi H. nuttingi

Collections number CASIZ 112817 NMNH e32602Test diameter (mm) 40 53.4 62.8 64.5 57.6

Food items (% volume)Spongy pellets 0 0 19.8 0Calcite-bearing pellets 23.3 80 30.2 40.6Gorgonian (soft coral) 0 7 9.9 28.1Plant* 0 0 3.8 0Solitary coral fragments 1.7 4.4 28.6 0Stylasterid coral fragments 0 2.5 5.5 0Milleporid coral fragments 0 0 0 11.5Bryozoans 3.3 0 0.5 1Echinoid fragments (spines) 0 0 1.7 4.2Crinoid columnals and cirrals 71.7 6.1 0 1 7Crinoid brachials and pinnulars 0 0 0 99 7.3

* Plant material likely consists of seagrass transported from shallow water.

Isocrinid Behavior and Its Biological Role

Although our data bearing on the interac-tion between cidaroids and crinoids are lim-ited, they indicate that stalked crinoids rep-resent part of the cidaroid diet. Furthermore,these data suggest that cidaroids feed on livecrinoids rather than on their postmortem re-mains. This leads to the obvious question ofwhether crinoids possess some means of es-cape. Below we consider two features of thebehavioral repertoire of isocrinids that weconsider antipredatory.

Stalk Shedding. The ability to actively shed(autotomize) body parts is a characteristic ofmost echinoderms including the isocrinids. Is-ocrinids possess articulations specialized forautotomy not only in their arms, but also intheir stalks. Although the former have beeninterpreted as a means of reducing the risk ofdeath from fish predation (Oji and Okamato1994), the reason for autotomy in the stalk hasremained elusive. Some have suggested that itmay be a prerequisite for a mobile mode oflife, given that all extant crinoids use a hold-fast for attachment in early stages of ontogeny(Baumiller and Hagdorn 1995). Studies of is-ocrinid stalk shedding as well as those of theskeletal morphology and soft tissue distributionpermit several conclusions: shedding of stalksegments is restricted to specialized articula-tions (synostoses/cryptosymplexies). Spacedat approximately equal intervals along thelength of the mature stalk, these articulationscan be easily distinguished from non-autoto-

my articulations. Synostoses in particularhave a characteristic skeletal morphology andorganization of soft tissues (Roux 1977; Don-ovan 1984; Emson and Wilkie 1980; Motokawa1984; Wilkie 1984; Grimmer et al. 1985; Baum-iller and Ausich 1992). The mechanism of stalkshedding is likely under neuronal control andinvolves extremely rapid changes in the prop-erties of the connective tissues (Wilkie 2005).An interesting result of long-term, in situ is-ocrinid growth studies revealed that whilestalk growth can reach 36 mm yr�1 in E. parraeand 170 mm yr�1 in N. decorus by the additionof new columnals in the proximal portion be-neath the cup, stalk length remains relativelyunchanged (Messing et al. 2007). These datasuggest that distal portions must be episodi-cally shed (Messing 1994; Messing et al. 2007).

Locomotion. Stalked crinoids have gener-ally been thought of as sessile, but over thepast decades studies of isocrinids have re-vealed some capacity for crawling. Crawlingobserved in laboratory studies was exceeding-ly slow (Baumiller et al. 1991; Birenheide andMotokawa 1994), but recently published videoevidence collected from the Johnson Sea Linksubmersible near Grand Bahama Island at adepth of 420 m revealed rapid (�10–30 mmsec�1) crawling (Baumiller and Messing 2007).

Biological Role of Stalk Shedding and Crawling:Escape from Cidaroids. When considered to-gether, shedding of the distal part of the stalkand crawling could well represent an escapestrategy. The sacrifice of stalk material is an


FIGURE 4. Frequency distribution of segments of crinoid columnals and pluricolumnals in the sediment (black bars)and in the gut of cidaroids. Open bars, Calocidaris micans 1. Stippled bars, C. micans 2.

appropriate response to predation by benthicinvertebrates because it saves the rest of theorganism in a manner akin to the autotomiz-ing ophiuroid arm that allows the animal tocrawl away with visceral mass and associatedgonads intact (Emson and Wilkie 1980).

Although our evidence for this response byisocrinids to cidaroids is largely indirect, a setof low-resolution analog video frames havecaptured what appears to be an instance ofthis very behavior. In the video frame, a ci-daroid is behind a ‘‘thicket’’ of E. parrae intheir normal feeding postures (Fig. 5). One E.parrae lies prone on the substrate within astalk length of the cidaroid in a posture char-acteristic of rapid crawling (Baumiller andMessing 2007). The orientation of the crownindicates that the crawling direction is awayfrom the cidaroid, and that the distal end ofthe stalk is within the cidaroids’ reach, andperhaps within its grasp.

A previously described interaction betweenC. micans and the isocrinid Cenocrinus asterius(Linnaeus 1767) in 250 m depth off George-town, Grand Cayman Islands (Messing et al.1988), and shown here as a sequence of pho-tographs (Fig. 6), is even more revealing. Inthis sequence, a cidaroid can be seen ap-proaching an upright isocrinid. Once the ci-daroid’s long spines contact the isocrinid, theisocrinid crown collapses, and in the last pho-to, the isocrinid appears to be moving away.A distal portion of the stalk can be seen nextto the cidaroid, but it is unclear whether it hasbeen shed or whether it is still attached to theisocrinid and is being dragged behind thecrown.

Discussion

The above data indicate that the interactionsbetween cidaroids and isocrinids are antago-nistic and that two features of isocrinid be-


FIGURE 5. Video evidence of interaction between a cidaroid and the isocrinid Endoxocrinus parrae. In the frame, thewhite arrow points to a spine of the cidaroid, most of which is hidden behind the isocrinids in the foreground. Theblack arrow points to the distal end of the stalk of an isocrinid that is crawling away (to the right) from the cidaroid.The arms of E. parrae are �100 mm in length.

FIGURE 6. A sequence of 35-mm photos showing an interaction between a cidaroid and the isocrinid Cenocrinusasterius, near Discovery Bay, Jamaica. A, Approach. B, Encounter. C, Escape. Length of spines � 150 mm. Photo-graphs courtesy of Research Submersibles, Ltd. and M.-J. Bodden.

havior, stalk shedding and crawling, are usedin escape. Although the latter interpretation isbased on only two sets of in situ observations,it represents a plausible hypothesis thatshould be explored further with laboratoryand field studies. Such studies are also essen-tial for establishing the frequency of cidaroid-crinoid interactions, the mode in which cida-roids detect crinoids, how cidaroids capturethe crinoids and use their teeth in consumingtheir prey, and the exact nature of isocrinid es-cape. Although data are minimal at this time,we can provide some information that sug-gests answers to these questions.

Frequency of Interaction. If stalk shedding isprimarily a response to interactions with ci-daroids, then data on stalk growth rates showthat most measured individuals shed at leastsome parts of their stalk during several-month

intervals (Messing et al. 2007), suggesting fre-quent encounters with cidaroids during thattime interval. This seems quite plausible giventhat cidaroids and isocrinids co-occur at thestudy site and when captured together on filmisocrinids are often found in prone, crawlingpostures. Additionally, damaged or brokenossicles characterized by irregular grooves,pits or fractures accounted for �8–40% of col-umnals in sediment samples collected nearour study site (n � 16; mean � 22.4%; SD �8.9%) and were attributed most likely to ‘‘a bi-ological agent such as a predator or scaven-ger’’ (Llewellyn and Messing 1993: p. 568).This prescient interpretation has now beentested by examining in detail columnals ob-tained from the cidaroid’s gut as well as bro-ken columnals found in the sediment (Fig. 7).Indeed, cidaroid teeth cause the type of dam-


FIGURE 7. Patterns of breakage and abrasion of Neocrinus decorus columnals. A, Internodal extracted from the gutof C. micans showing a rough fracture pattern. B, Internodal extracted from a sediment sample showing a roughpattern of breakage similar to that seen in Figure 7A. C, Pluricolumnal (three columnals long) extracted from thegut of C. micans showing two circular holes on a symplexial suture. Judging from their dimensions and shape, thedamage was cause by the cidaroid’s teeth. D, Nodal from sediment showing slight abrasion (lower left) but noevidence of bite marks. E, Internodal from sediment showing slight abrasion of articular facet but no evidence ofbite marks. F, Pluricolumnal (same as in Figure 7C) showing longitudinal fracture pattern. Failure through col-umnals, rather than through sutures, is characteristic of fresh material where strong ligaments are still maintainingacross-suture integrity of a pluricolumnal. Scale bars, 1.0 mm.

age associated with broken columnals foundin the sediment. If one assumes conservativelythat all of the broken columnals in the sedi-ment represent damage caused by cidaroidsand that the cidaroid digestive process causesno further damage, the 22.4% of broken col-umnals found in the sediments might reason-ably approximate the frequency of cidaroid-crinoid encounters.

Although cidaroid feeding has not receivedmuch attention, our observations match somepreviously reported. For example, our analy-ses of the gut content of Calocidaris and His-tocidaris (Table 1), as well as that of other ci-daroids (Stylocidaris lineata, Cidaris blakei, C.rugosa) suggest a preference for prey withhigh calcium carbonate content. We do notknow whether deep-water cidaroids are seek-ing nutrients, a source of calcium carbonate, orboth in their choice of prey. Many non-cida-roid sea urchins will ingest animal as well as

plant material in detritus, and even gather onfish carcasses (Mooi unpublished data). How-ever, only cidaroids have been suggested toprey actively on other animals and are unlikeother echinoids in being ‘‘primarily carnivo-rous’’ (De Ridder and Lawrence 1982: p. 234).The presence in cidaroid guts of articulatedand sometimes broken skeletal elements isconsistent with the biting rather than grindingaction of the teeth of the Aristotle’s lantern(Lawrence 1982). Beyond that, little is knownabout cidaroid feeding, although it is clearthat they swallow the bitten portions more orless whole. The urchins might also sense theirfood by using olfaction or rely on chancephysical encounters (Sloan and Campbell1982). Most cidaroids have fairly short, rugoseor textured spines that tend to support epifau-nal communities. However, both C. micans andH. nuttingi are atypical in having long, rodlikespines that are usually free of encrusting or-


FIGURE 8. Isocrinid arm fragments extracted from His-tocidaris nuttingi. Note the degree of articulation of bra-chials and pinnulars and the breakage pattern of thebrachial in the upper left-hand corner of the photo. Scalebar, 0.5 mm.

ganisms. These spines are sensitive to me-chanical stimuli (Mooi unpublished data) andcould behave like antennae to detect prey asfar as two body-lengths away.

Rates of locomotion in cidaroids have alsonot been studied rigorously, but like most oth-er echinoids, they are considered sluggish.Therefore, it is plausible that the isocrinidcrawling speed caught on video (�30 mm s�1

[Baumiller and Messing 2007]) is sufficient foroutrunning a cidaroid. More likely, isocrinidsdo not rely on speed in escaping cidaroids butrather crawl for only one to a few meters aftershedding part of their stalk. Given the rela-tively high densities of isocrinids at the studysite, even movement over such a short distancewould reduce the threat of re-encounteringthe cidaroid.

Taxonomic Breadth of Interaction. Data fromthe Settlement Point dive site are taxonomi-cally restricted, but a cursory search of the Na-tional Museum of Natural History, Smithson-ian Institution, and California Academy ofSciences wet collections reveal isocrinid ele-ments in guts of specimens of H. nuttingi, col-lected in another part of the Bahamas atdepths of more than 300 m. As in C. micans,the crinoid ossicles in H. nuttingi consist of ar-ticulated isocrinid elements, but in one of thespecimens a staggering 99% of the gut volumewas filled with articulated brachials and pin-nulars (Table 1, Fig. 8). The Cidaridae, con-taining C. micans, and the Histocidaridae, con-taining H. nuttingi, are phylogenetically dis-tant (Smith and Wright 1989). Roux (1981)placed the two isocrinids apparently attackedby C. micans—E. parrae (this study) and Ceno-crinus asterius (Messing et al. 1988)—in sepa-rate subfamilies. This additional combinationsuggests that the cidaroid-isocrinid interac-tion may involve numerous taxa of bothgroups and that it may not be geographicallyconstrained. Furthermore, the presence of ar-ticulated elements of crinoid arms in H. nut-tingi implies that some encounters might befatal to the crinoid, or that arm autotomy isalso an escape strategy.

It remains unknown whether stalked cri-noids with holdfasts (e.g., Hyocrinidae, Phry-nocrinidae, Bathycrinidae) interact with cida-roids today. Such interactions would likely be

fatal because no evidence exists that crinoidswith terminal holdfasts could reattach and re-gain an erect posture, even if they survivedthe attack. However, crinoids with holdfastsappear to inhabit environments that lack ci-daroids, avoiding them either at greaterdepths or on unconsolidated substrates notconducive to cidaroids. For example, whereasC. micans does not appear to occur below 400m, hyocrinids generally occur in greater than1000 m, and many bathycrinids and bourgue-ticrinids root in sediments (Rasmussen 1978).

Paleobiological Implications. The present-day interaction between cidaroids and stalkedcrinoids is likely to have deeper roots and itwould be interesting to track the history ofthis interaction through geologic time. Where-as most predator-prey interactions leave nosignatures in the fossil record, the mode ofcolumnal breakage generated by cidaroidteeth, described above, could provide a ‘‘fin-gerprint’’ of the interaction. Given the rich re-cord of crinoid columnals, it is reasonable tolook for such data, especially in places wherethe two taxa co-occur. For example, spines ten-tatively identified as those of Calocidaris havebeen found in Oligocene deposits from theKeasey Formation of the Pacific Northwest


(Burns and Mooi 2003). These deposits are fa-mous for their spectacularly preserved Isocri-nus. If the same relationship between cida-roids and crinoids described herein existed inthe Pacific Northwest Oligocene, the spatialand temporal potential for cidaroid predationwould be considerably increased.

In the Paleozoic, archaeocidarids, a groupclosely related to cidaroids, often co-occurredwith crinoids. For example, Schneider (2001)described crinoid fragments closely associat-ed with well-preserved archaeocidarids andconcluded that they might have representedthe echinoids’ ‘‘final meals’’ (Schneider 2001:p. 113). This is a plausible interpretation giventhat by the Carboniferous, archaeocidaridspossessed an Aristotle’s lantern capable of bit-ing (Smith 1984), but we do not know if thearchaeocidarid diet included live crinoids ortheir postmortem remains. A detailed analy-sis of column segment lengths and breakagepatterns might clarify the relationship.

The Carboniferous, when archaeocidaridsand crinoids may have interacted in the sameway as modern cidaroids and isocrinids,marked a major transition between camerate-dominated faunas of the middle Paleozoic andthe advanced cladid-dominated faunas of thelate Paleozoic (Ausich et al. 1994; Baumiller1994; Waters and Maples 1991). In the former,most crinoids attached permanently to thesubstrate by structures such as cementingholdfasts or stiff, largely inflexible cirri,whereas in the latter, taxa closely allied or an-cestral to the post-Paleozoic articulates (andmodern fauna) had developed functional fea-tures necessary for crawling (Simms and Se-vastopulo 1993; Holterhoff and Baumiller1996) (Fig. 9). These features include a stalkwith prehensile cirri bearing a transverseridge and a terminal clawlike cirral that allowrapid oral-aboral flexure, anchoring, releaseand reattachment, and muscular arm articu-lations with a well-developed brachial ful-crum allowing rapid oral-aboral flexure of thearms and crawling (Lane and Macurda 1975;Ausich 1977; Ausich and Baumiller 1993;Simms and Sevastopulo 1993).

Whether some of these Paleozoic advancedcladids were, in fact, capable of stalk autotomyand crawling remains speculative, but it is

clear that following the Permo-Triassic extinc-tion, taxa with traits prerequisite for mobilitybecame dominant. Among them were stalkedcrinoids such as the holocrinids and isocrinids(Simms and Sevastopulo 1993; Baumiller andHagdorn 1995; Baumiller and Messing 2007)and, by the Late Triassic, the stalkless comat-ulids (Hagdorn and Campbell 1993). Al-though the diversity and abundance history ofcomatulids is difficult to track and comparewith that of stalked crinoids because of pres-ervational differences due to habitat and mor-phology, they are certainly the most diverseand abundant crinoids today and the only cri-noids found at depths shallower than 100 m.Compelling arguments have been made thatthe success of comatulids was at least in partrelated to their ability to crawl and, thus, re-duce the impact of fish predation (Meyer andMacurda 1977). However, as we argued above,crawling can also be an effective strategy forescaping benthic enemies, such as cidaroids.Therefore, it may be worth considering thesuccess of the two crawling groups of cri-noids, the isocrinids and comatulids, in thecontext of benthic predation.

Even more intriguing are the swimmingabilities of some comatulids (Macurda 1973;Macurda and Meyer 1983; Shaw and Fontaine1990). When considered in the context of fishpredation, such behavior is more likely to in-crease rather than decrease encounters andrisks. However, even short bursts of swimmingcould allow escape from benthic predators, asituation analogous to the well-known case ofthe escape swimming reaction elicited by seastars in the scallop Pecten maximus (Thomasand Gruffydd 1971). In fact, Shaw and Fontaine(1990) observed that swimming in the comat-ulid Florometra serratissima can be elicited by themere proximity of several invertebrate species,most notably several species of predatory as-teroids, and concluded that this behavior rep-resents an escape response from these preda-tors. Therefore, it is quite plausible that swim-ming may have evolved in response to benthicpredators, perhaps even cidaroids. Unfortu-nately, cidaroids were not included in the Shawand Fontaine (1990) study, although it shouldbe relatively simple to test experimentally howcomatulids respond to cidaroids. It is worth


FIGURE 9. Diagrams summarizing the relationships and history of relevant groups of crinoids and echinoids. Ac-cording to the Treatise on Invertebrate Paleontology (see Lane 1978) the cyathocrines, dendrocrines*, poteriocrines*,and the ‘‘stem group articulates’’ form the order Cladida. The approximate timing of the origin of (1,2) musculararm articulations, flexible and motile cirri, and (3) stalk shedding are indicated. Non-monophyletic groups indicatedby *. Numbers above crown-group crinoids indicate approximate number of species. Among extant taxa, only thecomatulids and isocrinids are known to locomote. After McIntosh (1983), Smith and Hollingworth (1990), Simmsand Sevastopulo (1993), Holterhoff and Baumiller (1996), Simms (1999), Smith (2005).

noting also that spotlighting the isocrinid Neo-crinus decorus under the Johnson Sea Link’s in-tense arc light elicited an active and rapid se-ries of arm flexures reminiscent of comatulidswimming motions, suggesting that the abilityto swim was ‘‘pre-adaptively’’ present instalked crinoids before the lineage that becamecomatulids lost the stalk (C. G. Messing un-published data). The development of putatively

planktonic (e.g., Roveacrinida, Saccocoma tenel-la, Uintacrinus socialis) and pseudoplanktonic(Seirocrinus subangularis on driftwood) life-styles in some post-Paleozoic articulates (pa-pers in Hess et al. 1999) may also represent al-ternative escape-from-benthic-predators sce-narios. However, benthic lifestyles have alsobeen proposed for at least some of these taxa(e.g., Milsom 1994 and Milsom and Sharpe


1995 for S. tenella, and Milsom et al. 1994 andMessing et al. 2004 for U. socialis).

Conclusion

Since the 1970s, research submersibles havegreatly enhanced our understanding of the bi-ology of stalked crinoids. In situ observationshave revealed much about their autecology, es-pecially about their feeding postures, growthrates, patterns of distribution, and locomotoryabilities. Here, we provide another example ofsubmersible-derived evidence, in this case forthe existence of biotic interactions between is-ocrinids, a diverse group of stalked crinoids,and cidaroids, a group of ‘‘regular’’ sea ur-chins. A detailed analysis of cidaroid gut con-tents produced patterns consistent with theirfeeding on live crinoids. High frequencies ofcharacteristically broken columnals in the sed-iments and evidence for common stalk shed-ding among the isocrinids suggest that this in-teraction is not rare. Direct evidence of the in-teraction captured on videotape and still pho-tographs suggests that isocrinids may use a‘‘lizard’s tail’’ strategy of escape that involvesshedding portions of the distal stalk andcrawling away from the cidaroid preoccupiedby the autotomized body parts. In this sense,autotomy of the stalk serves a defensive func-tion, a usage of ‘‘autotomy’’ consistent with itsoriginal meaning (Fredericq 1883 as cited inWilkie et al. 2007).

It is highly probable that the history ofpredator-prey interactions between sea ur-chins and crinoids is long, perhaps extendingback to the middle Paleozoic, and that this in-teraction or interactions with other benthicpredators affected the evolution of crinoids,perhaps to an extent equal to or greater thanthat with fishes. It now appears that in slow-moving, benthic animals such as cidaroidechinoids, we have found the type of predatorthat best explains the significance of some ofthe otherwise enigmatic behaviors and mor-phology of crinoids, both extant and fossil.

Acknowledgments

We would like to thank the crews of the sub-mersibles Johnson Sea Link I and II, and theR/V Johnson, Seward Johnson, and Edwin Linkfor their help, support, and excellent ship and

sub handling. Thanks are due to T. Askew,head of Marine Operations at the HarborBranch Oceanographic Institution, Fort Pierce,Florida, who facilitated the scheduling of ourcruises. W. I. Ausich, D. L. Meyer, and D. Ken-drick provided thoughtful comments. Wethank B. Miljour for help with the figures. Thisresearch was funded in part by National Sci-ence Foundation grants EAR-9104892, EAR-9304789 (T.K.B.), EAR-9004232, EAR-9218467,and EAR-9628215 (C.G.M.).

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Urchins in the meadow: paleobiological and evolutionary implications of cidaroid predation on crinoids