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Rapid Arm Movements in Stalked Crinoids

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Rapid Arm Movements in Stalked Crinoids FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. 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 crinoids. 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 an unpublished anecdotal observation suggesting that cri- There was no evidence that arm waving functions in food noids may respond to suspended sediment (W. I. Ausich,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 crinoid 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 animal was in its re- or waving in animals 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
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