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Notice: ©1995 Marine Biological Laboratory. The final published version of this manuscript is available at http://www.biolbull.org/. This article may be cited as: Young, C. M., & Emson, R. H. (1995). Rapid arm movements in stalked . The Biological Bulletin, 188(1), 89‐97.

Reference: Biol. Bull. 188: 89-97. (February/March, 1995)

Rapid Arm Movements in Stalked Crinoids

CRAIG M. YOUNG' AND ROLAND H. EMSON2 'Departmentof LarvalEcology, Harbor Branch Oceanographic Institution, 5600 U.S. Hivy 1 N., Ft. Pierce, Florida 34946, and 2Division of Life Sciences, King's College, London, Campden Hill Road, London, W8 7AH, United Kingdom

Abstract. Stalked crinoids in the family Isocrinidaehave Conan et al., 1981; Roux, 1976), and stalked crinoids been observed to wave individual arms actively. Using have recently been observed crawling across the bottom video cameras mounted on a manned submersible, we (Messing, 1985; Messing et al., 1988). When stimulated studied these movements and investigated the factors that by the manipulator arm of a submersible or by very bright elicit them. Crinoids wave their arms in response to sand lights, this same species, Endoxocrinus parrae, rapidly or detritus dropped on their crowns, to entanglement in flexes some or all of its arms in an adoral direction (Mess- tentacles of adjacent sea anemones, and to contact by ing et al., 1988; Young and Emson, unpub.). Except for small crustaceans that might steal from the food grooves. an unpublished anecdotal observation suggesting that cri- There was no evidence that arm waving functions in food noids may respond to suspended sediment (W. I. Ausich, collection. In most cases, the movements could be attrib- pers. comm.), all reports of rapid active arm movements uted directly to mechanical stimulation by some natural have involved strong artificial stimuli. The natural roles stimulus. The rapid effective stroke of an arm flexure is of rapid arm movements remain undocumented. Here, caused by contraction of dorsal longitudinal arm muscles. we describe in detail rapid arm flexures of some bathyal The slower return stroke results from the elastic recoil of isocrinids and present evidence that this behavior defends large ligaments near the aboral sides of the arms. crinoids against various biotic and abiotic threats.

Introduction Materials and Methods Stalked crinoids are passive suspension feeders with Several species of stalked were observed from limited but are nevertheless of several mobility capable Johnson-Sea-Link (JSL) submersibles at depths ranging kinds of movements. The most characteristic behaviors from 400 to 900 m in the northern Bahamas (see map in are slow movements used orient to with respect to currents Young, 1992). Still photographswere taken with a Benthos and to hold the and in arms pinnules a parabolic feeding- 35-mm camera equipped with an 80-mm lens, mounted fan posture (Macurda and Meyer, 1974, 1976; Conan et on the front of the submersible and focused with twin The mechanisms which al., 1981). by these postures are laser beams that converged on a fixed focal plane. Video maintained and controlled are understood. Ori- poorly footage was obtained with a Photosea Camera on a pan- entation of the stalk, which contains no muscles, is de- and-tilt mechanism and was recorded on 1/2"or hi-8 vid- on mutable tissues et pendent collagenous (Wilkie al., eotape. Video still sequences were taken from the tape The tonic of the 1993). posture parabolic feeding fan is with a Seikosha VP-1500 video printer. maintained a similar but there probably by mechanism, We obtained numerical data on arm-waving frequency is as no or evidence for yet morphological physiological and crustacean abundance directly from the videotape. mutable arm ligaments (I. Wilkie, pers. comm.). We stopped the tape every 30 s and counted the number Stalked crinoids occasionally demonstrate fast muscular of arm movements, the number of crinoids involved in movements. Several are to be of species thought capable arm-waving behavior, and the total number of crinoids between attachment moving sites (Carpenter, 1884; visible in the frame. We ran the tape forwards and back- wards a few frames at each census point to be certain that Received 16 March 1993; accepted 2 December 1994. arms counted as waving were really in motion and not

89 90 C. M. YOUNG AND R. H. EMSON

UIIL) I Figure1. (A) Endoxocrinusparrae with armsdrooping in slackcurrent. Note the singlearm waving in the watercolumn (arrow). (B) Cenocrinusasterius in current,showing parabolic feeding fan characteristic of all Bahamianisocrinids. (C) E. parraeengaged in arm-wavingbehavior (arrow indicates moving arm). (D) A densepopulation of E. parraewith numerousindividuals waving arms (indicated by arrow). beingheld in a staticposture. The numberof small crus- six differentoccasions, while recordingthe responsesof taceansin a framewas estimatedby repeatedlypassing crinoidson videotape.On some occasions,the sediment the video forwardand back, frameby frame,while scan- consisted of fine silt; at other times, it was dominated ning each partof the framein successionfor moving or- eitherby coarsesand or coarse,flocculent organic parti- ganisms. cles. The velocity of arm movement during effectiveand Crinoidarm pieces were fixed in 4%neutral buffered recoverystrokes was documentedby layingdown a time formalin,decalcified in 70%acid alcohol,then embedded code on the videotapewith a hi-8 video editingmachine in paraffinby standardhistological procedures. Sections (SonyEVO-9700), then, duringframe-by-frame analysis, werecut at a thicknessof 8 lzmand stainedwith Milligan's recordingthe time that movements were initiated and trichrome(Humason, 1972). completed(resolution: 0.067 s). To investigatethe possibilitythat sediment particles Results might elicit arm waving,we used a suction tube on the Descriptionand mechanicsof arm waving manipulatorarm of the submersibleto pick up a small amount of sedimentand releaseit about 1 m above an At times of slack current,three Bahamianisocrinids, aggregationof crinoids.This experimentwas repeatedon Endoxocrinusparrae, Cenocrinus asterius, and Diplocri- ARM WAVINGIN SEA LILIES 91

ir . i. I f|j ?.?i } i^^

" 4 , ,I' ' - '/ . jr - I ,,, .?, . '.. Figure2. Videosequence of characteristicarm waving behavior in Endoxocrinusparrae. (A-C) Sequential stepsof the effectivestroke. (D) Maximumarm extension. (E-F) Recoverystroke.

nus maclearanus, stand erect with arms drooping down the durationsof effectiveand recoverystrokes (Fig. 3) nearthe stalk(Fig. 1A). In a current,these same species show that the recoverystrokes were more variableand formtheir arms into a parabolicfan for feeding(Fig. 1B; often longerthan the effectivestrokes, but the two distri- see also Macurdaand Meyer, 1974, 1976), though the butions overlappedsubstantially. For individualstrokes, uppermostfew arms of the fan may sometimes be ex- the ratio of the effectivecomponent to the recoverywas tendedstraight up into the watercolumn. All threespecies nearlyalways greater than 1 (Fig. 4), and the difference have been observedwith individualarms waving up and between the durationsof paired effectiveand recovery down rapidly(Fig. 1A, 1C). In dense populations,large strokes was highly significant(paired Student's t test, numbersof individualshave been observedto engagein 54 d.f., t = 5.75, P < 0.0000). The arms were flexed arm-wavingbehavior simultaneously (Fig. 1D), particu- througharcs rangingfrom a few degreesto more than larly after several minutes of illuminationby the sub- 180 degrees.Most armswere flexedonly once beforean- mersible. other arm was broughtinto play. Often, one arm was Althoughwe have occasionallyobserved arm flicking flexed while another on the same was in its re- or waving in with their arms extended in the coverystroke. feedingposture, arm-waving behavior has been observed Examinationof histologicalsections of the arm of E. morecommonly in animalswith drooping arms. The arm parraerevealed the presenceof largedorsal (oral) longi- is moved rapidlyaway from the stalk,sweeping outward tudinalmuscles linking the arm segments(Fig. 5). These and upwarduntil it is fully extendedabove or to the side muscles, which are describedelsewhere (Hyman, 1955) of the calyx (Fig. 2). The arm pausesonly brieflyat the as flexor muscles,are clearlyresponsible for the flexure end of the strokebefore reflexing downward more slowly of the arms.There are no opposinglongitudinal muscles, to its initialposition. This entiremovement may take as but largeligaments are found ventral (aboral) to the flexor little as 2 s or as much as 21 s. Frequencyhistograms of muscles(Fig. 5). The recoveryphase of arm wavingmust 92 C. M. YOUNG AND R. H. EMSON

25 with the idea that crustaceansstimulate arm waving,we couldnot dismissthe possibilitythat density of crustaceans covariedwith some otherfactor (e.g., illuminationtime) 20 until video cameraswith higherresolution were installed in 1991. ' 15 On 24 October1991 at a depthof 642 m off EggIsland, CU) we located a of E. 0 large aggregation parrae. By focusing . on inactiveindividuals, we recorded10 instancesof arm I. 10 E wavingthat were clearly stimulated by a singlecrustacean. z A representativeencounter is shownin Figure7. The time 5 requiredfor initiationof a visibleresponse to the impact of this crustaceanwas 0.47 s. In everycase, the crustacean

1-^-i j " contactedthe crinoidon the oralside of the armbetween -, r I -,- , ao ^^*m*^Ii^ in the of the food In one 0 5 10 15 the pinnulesand region groove. observedencounter, the crustaceanremained attached Durationof Stroke(s) during three sequential flexures before becoming dis- Figure 3. Frequency histogram comparing the durations of the ef- lodged;in all otherinstances, the crustaceanwas dislodged fective strokes (hatched) and recovery strokes (solid black) during arm by the initial arm movement and swam away. On sub- flexure of Endoxocrinus parrae. sequentdives, crustacean-inducedarm movementswere also recorded for C. asterius, one of which is shown in Figure8. Here, the crustaceanwas swimmingupstream in the turbulentdownstream wake of a crinoid feeding passivelyin the current.When the crustaceancontacted thereforebe achieved elasticrecoil. Small dark-staining by the oral side of the arm, a small flexurewas elicitedim- cell bodies at the insertionsof the ligaments (Fig. 5B) mediately(Fig. 8), andthe crustaceanmoved downstream. to be juxtaligamentalcells (Wilkie, 1984), which appear We droppedsediment from the manipulatoron six are known to regulatecollagen viscosity in other echi- separateoccasions with two to four attemptson each ex- noderms.The largestaxons in arm cross sections mea- periment. Sediment containing a mixture of particles sured 3.75 ,gm in diameter,and most were between2.5 rangingin size from 1 to severalmillimeters elicited dis- and 3.5 um in diameter. creteflexures of individualarms when individual particles struck(Fig. 9). Small amounts of very fine silt did not Functions of arm waving Withthe use of a close-upvideo camera, we determined that flexuresoften occurredin responseto mechanical stimuli caused various and For 20 by organisms particles. / example,when the arms of stalkedcrinoids become en- (I) trappedin the tentaclesof adjacentsea anemones,arm 0) 0 / 7, flexuresallow them to escape. Arms are also flexed in -se 15 7 - TI I T I ') 7' responseto contactsby small crustaceans.Such crusta- 0) ceansare alwaysattracted to the lightsof the submersible in largenumbers, affording us increasedopportunities for 0L) 10 w * observingencounters between crinoids and crustaceans. 0 ? On 17 February1980, we came upon a sup- 0 7 0 rockyridge 0' more than 200 E. and C. asterius at a 5 porting parrae 0 depth between 409 and 500 m off Booby Rocks, New LLa Providence Bahamas.As we the Channel, passedup ridge 0 without stopping,we filmed 49 crinoidsin two aggrega- 0 5 10 15 20 tions, all the while two instancesof arm- observing only Durationof RecoveryStroke (s) wavingbehavior. We then restedthe submersiblenear a third largeaggregation and filmed it from a distanceof Figure 4. Durations of individual effective strokes plotted against 3 m for 7 min. The percentageof animals participating durations of corresponding individual recovery strokes for individual in arm and the numberof arm waves indi- arm flexures of Endoxocrinus parrae. If flexure and recovery were of the waving per same duration, all points would fall on the dashed line. Most points lie vidualincreased linearly with the numberof crustaceans below the line, indicating that recovery strokes are generally, but not visible(Fig. 6). Althoughthese regressionsare consistent always, longer than effective strokes. ARM WAVING IN SEA LILIES 93

Discussion Virtually all sessile animals have neuromuscular mechanisms for ridding themselves of impinging organ- isms or objects that threaten them or that interfere with the feeding process. It is not surprising, therefore, that stalked crinoids would have an active mechanism of pro- tection appropriate to their form and life style. In echi- noderms, some protective mechanisms involve the use of giant nerve fibers and very rapid (0.25 s) reaction times (Cobb, 1985; Cobb and Ghyoot, 1993). The nerve fibers of E. parrae measured between 2.5 and 3.75 gm in di- ameter, only about 30% as large as the giant fibers in Ophiura ophiura (Cobb, 1985). However, these are larger than the 1 ,m diameter neurons found in most echino- derms (Cobb, 1985). Reaction times of stalked crinoids (about 0.5 s) were about twice as long as those reported for ophiuroids (Moore and Cobb, 1985). On the basis of behavioraland histological observations, it appears that arm flexure results from the contraction of large flexor muscles, and that recovery results from the elastic recoil of ligaments. This interpretationis consistent

2.5 ._'o

'r.- 2.0 0 Figure 5. Cross section (A) and longitudinal section (B) of an arm . 1.5 of Endoxocrinus parrae showing longitudinal flexor muscles (M), and extensor of ossicles Individual 0) ligaments (L) connecting portions (0). ._ bundles of collagen (CB) are visible in the ligaments. Cell bodies ofjux- > 1.0 taligamentalcells (JC) are visible at the points where collagen fiberbundles into muscle of a insert the brachial ossicles. PM: longitudinal pinnule 0.5 cut in cross section. I

0.0 0 5 10 15 20 25 30

cm 1.0

0.8 stimulate waving, but fine sediment in large quantities 3 CO sometimes elicited a dramatic arm-waving response in- o 0.6 volving numerous arms. Figure 10 shows the response of one E. parrae individual to a large piece of flocculent - 0.4 organic matter that lodged firmly on an arm. The crinoid o0 moved the affected arm as well as arms several ' adjacent 0.2 0o times until the material was dislodged. 0. Various kinds of crabs and ophiuroids (e.g., euryalids) a. 0.0 commonly perch on sessile organisms, including large 0 5 10 15 20 25 30 and on the Bahamian sponges, gorgonians, antipatharians, Numberof Crustaceans Visible slope. These same organisms live on the stalks of crinoids, crustacean and the but we have never seen a single individual occupying the Figure 6. The relationships between density number of arms crinoid and of crinoids crown We that arm deter waving per (top panel) proportion region. suppose waving might waving arms (bottom panel) during a single 7-min taping session in a occupation of the crown by ophiuroids and crabs, but dense bed of Endoxocrinus parrae at 409 m depth at Booby Rocks, Ba- cannot prove this with observations. hamas. 94 C. M. YOUNG AND R. H. EMSON

Figure7. Responseof Endoxocrinusparrae to an individualcrustacean contacting the arm. (A-C) Crustacean(position and directionof swimmingindicated by arrows)enters rapidly from the rightside of the field and moves into crown regionof crinoid.(D) Arm beginsto flex immediatelyafter crustacean contactsit, andcrustacean responds by swimmingrapidly away (arrow). (E-F) Armcontacted by crustacean continuesto flex until it is maximallyextended. with the views of most previous workers (e.g., Muller, tension, has been put forward by Candia Carnevali and 1843; Breimer, 1978; Grimmer and Holland, 1987). An Saita (1985). Grimmer and Holland (1987), however, alternative hypothesis, invoking hydraulic pressure in the showed experimentally that destruction of these coelomic coelomic canals of the arms as a mechanism of arm ex- canals did not affect recovery from flexure in the coma-

Figure8. (A) Smallcrustacean swimming upstream (in directionof arrow)within the turbulentwake of a feedingCenocrinus asterius. (B) Smallarm flexurefollowing contact by crustacean(arrow), which is throwndownstream. ARM WAVINGIN SEA LILIES 95

Figure9. Armflexures of Cenocrinusasterius in responseto sandparticles dropped on the crown.Sand particles(one is indicatedby arrowin A) werefalling throughout this sequence,which involved movements by armson all sidesof the crown.

tulid Florometra serratissima. In fact, their experimental tissues (Wilkie and Emson, 1988) which require little resultsdemonstrate that elastic forcesin the aboralsoft energy expenditure.Our observation of apparentjux- tissuesof the arm of a comatulidwere alone sufficientto taligamental cells (Fig. 5B) is equivocal evidence for drivea powerstroke in activeswimming. We suggestthat mutablecollagenous tissues in stalkedcrinoid arms. The a similarmechanism is involvedin the recoverystroke of use of arm flexing for filter feeding seems unlikely, but stalkedcrinoids such as E. parrae. cannot be discounted completely. Existingevidence does not supportthe idea that arm Arm-wavingbehavior appears on present evidence wavingis involvedin food collection.Unlike some other to be principallya mechanism to eliminate inorganic sedentaryfilter-feeding at bathyal depths particlesfrom the crown and to deter small organisms (e.g., brisingid asteroids: Emson and Young, 1994), from settling on the arms of the crinoid. Specifically, stalkedcrinoids are not known to capturelarge particles we have demonstratedthat the behaviorhas a deterrent (Meyer, 1982; Lawrence, 1987). Indeed, our observa- effecton smallcrustaceans, preventing them from acting tions indicate that largeparticles contacting the crown as predators,food thiefs, or opportunisticcommensals. arethrown away from the crown,not towardthe mouth. Arm movementsmay preventcolonization of the crown Arm wavingcould enhance encounterswith small par- by crabs,ophiuroids, and other epifauna,and they per- ticles,particularly in still water.However, such a feeding mit escapefrom the feedingstructures of adjacentsessile strategywould seem inefficientin the oligotrophichab- organismssuch as sea anemones.Inorganic and organic itatswhere these animalslive, since arm flexurerequires particles that fall on the arms also elicit arm waving, considerablemuscular involvement and might resultin so the behavior may have evolved as a general mech- a net energyloss. By contrast,the maintenanceof pos- anism for riddingthe crown of unwanted particles.As ture for passive feeding may involve catch connective all stalked crinoids that have been examined histolog- 96 C. M. YOUNG AND R. H. EMSON

Figure 10. Response of Cenocrinus asterius to fine sediment and a large flocculent mass of detritus dropped on the crown. (A) Sediment contacts the crown, and a large particle of detritus (arrow) falls toward one arm. (B) Detrital mass lands on the arm. Note that the fine silt elicits no dramatic responses from the arms. (C) Arm (asterisk) with large detrital particle flexes, dislodging a portion of the mass. (D) Remainder of detrital mass (arrow) remains on the arm. (E, F) Various arms in the region of the detrital mass flex repeatedly, apparently attempting to dislodge the attached detritus. ically have similar flexor muscles, we suspect that arm significance of the muscle-ligament-skeleton system in the arm of waving may be a behavior of and com- the comatulids (Antedon mediterranea). J. Morph. 185: 59-74. great antiquity P. H. 1884. on the Crinoidea collected the mon to and extinct crinoids. Carpenter, Report during many living voyage of HMS 'Challenger'during the years 1874-1876. The stalked crinoids. Challenger Rep. Zool. 11, 442 pp. Acknowledgments Cobb, J. L. S. 1985. The neurobiology of the ectoneural/hyponeural synaptic connection in an . Biol. Bull. 168: 432-446. We thank the skilled pilots of the JSL submersibles for Cobb, J. L. S., and M. Ghyoot. 1993. The giant through conducting neuron? assistance with video. This work was funded neuron of the brittlestar Ophiura ophiura-a key Comp. close-up by Biochem. Physiol. 105A: 697-703. the National Science Foundation (OCE-8916264 and Conan, G, M. Roux, and M. Sibuet. 1981. A photographic survey of OCE-9116560) and by a NATO Collaborative Research a population of the stalked crinoid Diplocrinus (Annacrinus) wyvil- Grant (CRG-900628). Harbor Branch Contribution No. lethomsoni (Echinodermata) from the bathyal slope of the Bay of 1064. Biscay. Deep-Sea Res. 28A(5): 441-453. Emson, R. H, and C. M. Young. 1994. The feeding mechanism of a deep-water brisingid asteroid, Novodinea antillensis. Mar. Biol. 118: Literature Cited 433-442. Grimmer, J. C, and N. D. Holland. 1987. The role of ligaments in Breimer,A. 1978. Recent crinoids. Pp. 9-58 in Treatiseon Invertebrate arm extension in feather stars (Echinodermata:Crinoidea). Acta Zool. Paleontology,Part T, Echinodermata, 1, R. C. Moore and C. Teichert, 68: 79-82. eds. University of Kansas Press, Lawrence,and the Geological Society Humason, G. L. 1972. Animal Tissue Techniques. W. H. Freeman, of America, Inc., Boulder, CO. San Francisco. 641 pp. Candia Carnevali, M. D., and A. Saita. 1985. Muscle system organi- Hyman, L. H. 1955. The Invertebrates.IV. Echinodermata. McGraw- zation in the echinoderms: II. Microscopic anatomy and functional Hill, New York. 763 pp. ARM WAVING IN SEA LILIES 97

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