Comment on "Predator Classification by the Sea Pen Ptilosarcus Gurneyi (Cnidaria): Role of Waterborne Chemical Cues and Physical Contact with Predatory Sea Stars''^

DISCUSSION / DISCUSSION

Comment on "Predator classification by the sea pen Ptilosarcus gurneyi (Cnidaria): role of waterborne chemical cues and physical contact with predatory sea stars''^

James E. Dalby, Jr. and Joel K. Elliott

Al>str;ift: In ihcir sliii.i>' of bcbaxioural ivsjioiises ot' peniialuhiccuiis lo ])h\sical cnniaci vvifh asicroitK ni 2()i)2, Wciiihtmaii and Arscnaiilt ciairn to be the I'irst io dcnionstrak; ihai fiiidai iaii-> ha\c ihc abilil\ to tiisiinyiiish prcdaEors IVoni nonpredaturs. In lad, il has been kiuiun siiici' at least ihc l^bOs Ihat cnidatians an- capahk' oi" picilator ivco,L;ni lion. We brit-'fly Jcscrihe sonif oJ' lhe abtindanl tHcralurc nn this lopic, cspt'ciallv suidics on aiilho/oan--,

Kdsume ; Dans kun" elude des coiiipiiiteiiienls des |iennaiuiacL's en reaction a des eontacls physRjue'- a^ce de\ asu-roT- dcs dans 2002. Wcighimaii ct ArscnaulE prcleiiilciU eire les iireniiers a cieiiioiilrcr (.|uc les cnidaires -,oni k'apahies dc ciistinguei' les predalcurs des organismcs non prcdaleurs. }:n (ail deja dans les annees I 9()i), ct memc a\..n;L oi] savail les cnidaires capablcs de reconnailre des pre'dateui's. Noiis deerivims hfiescmeni une paitie de rabondante htieraliirc disponibic sur ec sujet. particuiicremcnl les eludes poriant sur les aiilho/duires.

I'l'iaduil par la Redac!inii|

Science's all consuiiiiny drive lo iiiakc new disemcrics Although prcdalor-elas^it'ication abilities are docuineiiicd ofieii risks losing sight of what was alread> known al one in several invertebrate and \erlebraie laxii iKaK and Dill lime — that which already exists in Ihe published litera- N9S]. our sludv provides the firsl e\pcri!!icn:al e\ idence ture, lnadequale attention to the published literature and oi' such abilities in enidaiians. one of the iiiost uneieiii insufTicient time devoted lo iis niinini: and synthesis into meta/oan phyla in the aniniat kingdom. neu knowledge is a problem faced by all disciplines.,,. While the atillnirs present eouvincing evidence thai pen- [{"'.('., Danghioii 2()i)l| naUilaeeans are able to distinguish asieroii.1 speeies aeeoidiug 'I'he aho\c staicnicnl refers io a per\;tsivc prohlcni in ciin [{) the degree of threat they pose as predators, ilicir asseriion ai*} scieiUific literaltirc: [oo many aulhors fail in ac- Ihat they are the first to reveal predator-elassificaiion abihiies knowlcdgc anil huiltl iip(iii Ihe work cil' previotis reseaichers. in enidarians is (jtiile incorrect, in ILICI. auioiig jus! the untho- This unfortttnaie faet has been identifieil repeaicdly In the /oans, several speeies have been known for a long iinie lo Cuninienis sections ii!'\'ariotis JoLirnals. and ways lo improve have the ahility to distinguish pretlaiors froni nonpredatois the siluation have been suggested (e.g.. DauglUon 2001. 2002: (reviews hy Rohson 1966: Ross i'-)67: Mackie and (irari! Cjinshiiig 2001: Garfiekl 2002), The objective oi our eom 1974; Sloan 1980; Shiek 19^)1), ment is lo idenlii'y one sueh example reeently published in Studies ol the res])ouses of the aetinian isea anenionel the Canadian Jonnud of Zoologx. and to iuforni the seieii- Sionipliia i-(>cclncii to seveiai luidibraneh (sea -^iug) aiul aster- lii'ie eomnitmily of lhe plentiful liteialure rclaliuL: lo lhe oid speeies repirsent some of the cailiest evicknce ihat aniho- topic of Ihat paper. /.oans ean recogni/e their pietlators. This aetinian tleiaehes Irom In their note ou behavioural interaetions between a penna- the substratum aud switns av\ay when bioughl into ei>ii!act tttlaeean (sea pen) speeies anil three asteroid {sea star) spe- wilh Ihe predatt>i"y nudihraneli .Acolklia papillosa. but does not eies. Weighinian aud Arsenauh (2O02i write: do so when totiehed by anv of three nonpiedaUiry nudibtaneh

Received 28 M; y 201)2. Accept :d 7 ,lanuary 2 ){)^. !'ubhshed on the NRC Research Press Weh Site at Utp://et/,nrc.ea on l,> April 20(1.^

J.E. Oalbv, Jr.^ British Cokunbia Ministry ol Waiei , Land, ami Air Prolcclion, 2I1SI)A 1 ahieu \ Road. NaiianiK), HC V')T 6,1'), Canada, J.K. Elliott. Depaitmen of Bio Ihmersilv of Puget Sound. "Cacoma. WA 98410. L' S.A '.Appears in Cai . ,!, /,oo , SO: 1 -1 ConespoiidinL: aiithnr (cmaii: ,1 uiies,i)alhvfr"L' em si. •ov,be,c;!i.

Si; Dalby and Elliott 557 species (Robson 1961). IJkewise, .S. coccinea detaches und sponse of the actinian Stomphia didemon to certain asteroids: swims when touched by any of 3 predatory or 2 nonpredatory dislribLilional and phylogenelic implications. Can. .1. Zool. 66: asteroid species, bul does not show these responses to 12 non- 2484-2491. predatoiT asteroid species or any ophiuroid species (Yentsch Daughton, C.G. 2001. Literature forensics? I3oor to what was known and Pierce 1955; Sund I95S: Robson 1961; Ward 1965: Mauzey but now forgotten. Hnviron. Forensics, 2: 277-282. el al. 1968). Weighlman and Arsenaull (2002) overlooked key Daughton. C.G. 2002. f.iierature forensics? Navigating through tlot- informaUon in at least two of the papers they cited (Yentsch sam, jetsam, and lagan. Scientist. 16: 12. and Pierce 1955; Mau/cy ct al. I96S). Hdmunds, M.. Potts, G.W., Swinfen. R.C. and Waiers, V.L. 1976. We have also published studies showing that actinians Defensive behaviour of sea anemones in response to predation have Ihc ability lo distinguish predatory asteroid species by the opisthobranch mollusc Aeolidia piipillosa (I..). ,1. Mar. from nonpredatory ones. Our research, like that of Weightman Biol. Assoc. U.K. 56: 65-83. and Arsenault (2002). was performed at Bamfield Marine Elliott. J., Dalby. J., Jr., Gohcn. R.. and Ross, D.M. 1985, Beha\ioral Station and published in the Canadian Journal of Zooloiiy. intcracti()ns between the actinian Tealia piscivora (Anthozoa: Acti- The actinian Unicina (formerly Tealia) piscivora releases its niaria) and the asteroid Deniiastenas imhricata. Can. J, Zool. 63: pedal disc from the substratum when brought into contact 1921-1929. with ils asteroid predator Dcrmasterias imbricala., but shows Garflcld. H. 2002. Demand citation vigilance. Scientist, 16: 6, no such response lo 19 olher nonpredalory species (Elliott el Ginsburg. I. 2001. The disregard syndrome: A menace lo honest al. 1985). Similarly, the actinian Stomphia didemon (formerly science? Scientist. 15: 5\. Aciinosiola sp,) detaches and swims away when touched by cer- Harris, L.G,. and Howe. N.R. 1979. An analysis of the defensive tain asteroid species, showing strong responses to its predator mechanisms observed in the anemone Anihopleura clcgantlssima D. imhricata and to two nonpredatory species, weak responses in response to its nudibraneh predator Aeolidki piipillosa. Biol. tt) six nonpredatory species, and no sueh responses to eighl Bull. (Woods Hole). 157: 138-152. nonpredatory species (Dalby et al. 1988). Howe, N.R,. and Harris. L.G, I97H, Transfer of the sea anemone pheromone. anthopleurine. by the nudibraneh Aeolidia paiyiilosa. There is even more published evidence for the predator- J. Chem. Fxol, 4; 551-561, ' recognition abilities of anthozoans. For example, the penna- Kastendiek, .1, 1976. Behaviour o( the sea pansy Reuilla koeUikeri tulacean (sea pansy) Rcnilla koeUikeri uproots itself from the Pfeffer {Coelenterata: Pennatulacea) and its influence on the dis- sediment when attaeked by its nudihraneh predator Arniina tribution and biologieal interaetioiis of the speeies. Biol. Bull, caUfomica, hut shows no such response to several non- (Woods Hole), 151: 518-537. predatory molluscs, crustaceans, and echinoderms (Kastendiek Kats, L.B,. and Dill. L,M. 1998, The scent of death: chemosensory 1976). Another example is the response of the actinian Antiio- assessment o[ predation risk by prey animals, F.coScience, 5: pleiira clegantissltna to three nudibraneh species. It responds 361-394. to contact with, or mueus from, its predator A. papillosa hy Lav^'n, I.D., and Ross, D,M, 1982. The behaviouriii physiology o{ pedal locomotion and detachment from the substratum, but the swimming sea anemone boloceroides iiicm/irrichi. Proc. R. exhibits weaker responses lo mucus from the nonpredalory Soe. Lond, B Biol, Sei, 216: 315-334. Phidiana (formerly Hermis.senda) cmssiconii.s. and shows Maekie, A.M., and Grant, P.T. 1974. Interspeeies and intraspecies no sueh responses Id mueus from the nonpredalory Auiso- ehemoreeeption by marine Invertebrates, hi Chemoreeeption in doris nohilis (Waters 1973; Hdmunds et al. 1976; Howe and marine organisms. Edited by A,M, Maekie and PT, Grant, Aca- Harris 1978; Harris and Howe 1979). Lastly, the aetinian demic Press, London, pp, I05-I4L Boloceroides mcmurrichi releases its pedal disc and swims Mackie. G.O, 1995. Defensive strategies in plankionie coelenterates. away from its nudibraneh prcdatt>r Berghia major, but does Mar, Freshw. Behav. Physiol. 26: 119-129. not react in this fashion to the nonpredator}' nudibraneh Mauzey, K.P., Birkeland, C, and Dayton, P.K. 1968. Feeding be- Fheslilla siboi^ac (Lawn and Ross 1982). haviour o{ asteroids and escape responses of lheir prey in lhe It should also be noted ihat anthozoans are not the oniy Pugei Sound region. Ecology. 49: 603-619. enidarians that have the ability to identify their predators. Robson. L.A. 1961. The swimming response and its pacemaker sys- For instance, there is evidence that certain hydrozoans can tem in lhe anemone .Stomphia cccinea. J. Exp, Biol, 38: 685-694. do this as well (review by Mackie 1995). Robson, E.A. 1966. Swimming in Aetiniaria. Symp. Zool. Soe. In eonelusion, Weightman and Arsenault (2002) neglected to Lond. 16: 333-360. cite mueh literature (in enidarians. including both primary and Ross, D.M. 1967. Behavioural and eeologieal relationships between secondary and recent and historical literature. This oversight sea anemones and other invertehrates. Oeeanogr. Mar. Biol. Annu. may have resulted from a reliance on one broad review attiele Rev. 5: 291-316. covering all major animal phyla. If so, this comment ser\'es as Shick, J.M. 1991. A funetional hiology of sea anemones. C'hapman a reminder of the need to perform complete literature searches, and Hall. Melbourne, Australia. both electronically and manually. When researchers are well Sloan, N.A. 1980. Aspects of the feeding biology of asteroids, read in their area of interest, they ai'e belter able lo expkun the Oeeanogr. Mar. Biol. Annu. Rev. 18: 57-124. significance of their findings Jn relation to those of other work- Sund. P,N. 1958. A study ofthe muscular anatomy and swimming ers. This type of hibliographie research is an integral part of the behaviour of lhe sea anemone Sfomphia coccinea. Q. J. Microsc, scientific process, and is essential to maintaining a high level of Sei. 99: 401-420. quality assurance in scientific publieations (Daughton 2001). Ward. .I.A. 1965. An investigation on the swimming reaction of the anemone Siomphia coccinea. i. Partial isolation of a reacting References substanee from the asteroid Derma.sterias imhricata. J. Exp. Zool. 158: 357-364. Dulbv, i.v... Jr.. Bliiotl. J,K.. and Ross, D.M. 1988. The swim re- Waters. V.L. 1973. Food preference of the nudibraneh Aeolidia

O ;;()l>3 NRC Ciinada 558 Can, J, /nol Voi, 81, ?(}iX>.

papillosa and the ctfeet ofthe defenses ofthe prey on predaiion, chemical enes and physical coniaci with ])rt'd,iU)f} MLM -.iitis. Can. Vchgcr. 15: 174 192. J. Zool. 80: IS5 190," Weightman. J.O.. and Aiseriaiilt. D.J. 2002. Predator classiftcaliori Ycnisch. C,S.. and Pierce. D.C, 19^.^, '"Swimming" aiicnioiic Iruni by the sea pen Flilosarcus ;j,!iniL'\i (Cnidariaj: role of waterbt)rnc Puget Sound. Science. 122: 12,^ I -1233.