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8-1-2018 Antipredatory Escape Behaviors of Two Benthic Ctenophores in South Florida Peter W. Glynn University of Miami

Brian Coffman Florida International University

Jeongran Vanderwoude University of Miami

Nicolas Martinez Florida International University

Joshua H. Dominguez University of Miami

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Find out more information about Nova Southeastern University and the Halmos College of Natural Sciences and Oceanography. Follow this and additional works at: https://nsuworks.nova.edu/occ_facarticles Part of the Marine Biology Commons, and the Oceanography and Atmospheric Sciences and Meteorology Commons

NSUWorks Citation Peter W. Glynn, Brian Coffman, Jeongran Vanderwoude, Nicolas Martinez, Joshua H. Dominguez, Julie M. Gross, and Dorothy-Ellen A. Renegar. 2018. Antipredatory Escape Behaviors of Two Benthic Ctenophores in South Florida .Ecology : 1 -11. https://nsuworks.nova.edu/occ_facarticles/950.

This Article is brought to you for free and open access by the Department of Marine and Environmental Sciences at NSUWorks. It has been accepted for inclusion in Marine & Environmental Sciences Faculty Articles by an authorized administrator of NSUWorks. For more information, please contact [email protected]. Authors

Julie M. Gross University of Miami

Dorothy-Ellen A. Renegar Nova Southeastern University, [email protected]

This article is available at NSUWorks: https://nsuworks.nova.edu/occ_facarticles/950 Antipredatory escape behaviors oftwo benthic 5 4 3 2 1 W.Peter Glynn 33004, USA Oceanography, University, NovaSoutheastern 8000North OceanDrive, Dania Beach,Florida Florida33146, Gables, USA Atmospheric University Science, of Miami, 1365MemorialDrive,210Ungar Building, Coral Univer UniversityofMiami,Science, Causeway, 4600Rickenbacker 33149, Miami, USA Florida Dominguez This article isThis article by protected copyright. All rightsreserved. This article acceptedhas been for publication andundergone fullpeer review buthasnotbeen Manu NaturalistManuscript Type andRunningHead:TheScientific type NaturalistArticle :TheScientific 10.1002/ecy.02497 differences thisbetween andVersion version the ofRecord.c Please the through copyediting, typesetting, pagination and proofreading process, to whichmay lead Accepted Author.Corrsponding E Department and ofMarine Environmental Halm Science, Undergraduate Marine and Science Atmospheric SchoolProgram, ofMarine Rosenstiel and ArticleSE Department ofMarine SchoolBiology and Ecology,Rosenstiel ofMarine andAtmospheric Environmental Center Research & Department ofBiological Sciences, Florida International script received 17 April 2018; revised 1 script received17 2018;revised JuneApril 2018;10July 2018. sity, Miami, 33199,USA Florida 3 , Julie M.Gross, Julie

1, 1, 5 , BrianCoffman

- mail: [email protected] 3

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D. Abigail RenegarD. Abigail 2 , Jeongran Vanderwoude Jeongran ,

4 ctenophores South in Florida

os College ofNatural Sciences College and os

3 , Nicolas MartinezNicolas

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than formerlythan recognized.most Coeloplanid aremembers ctenophores ofthe family speciose of aremore andCtenophora) widespread inand abundant tropical subtropi Eeckhaut tentacles involved in the capture ofzooplankton (RankinWhitfield 1956,Emson and 1991, focusedonthepredatorygenerally behaviorofbenthic ctenophores with functionalthe role of 2018), both of ac whichplay componentsmeroplankton. planktonic These often fish eggsandlarvae(Glynn include al. et 5 least (sticky colloblasts cells) assistinpreycap that employing ofextensible numeroustentacles apair with (side tentilla short stems.octocoral multiformis individuals m Vallicula multiformis individuals habitatscan occupy preferred <1 in m benthic invertebrates (Matsumoto 2015). 1999,Alamaruetal. Hundredstothousands of Vallicula benthic ctenophores, with33recognizedspeciesof This article isThis article by protected copyright. All rightsreserved. Editor:JohnCorresponding Pastor Accepted Article - 10 times capturing bodylength, mesozooplankton, the bothholoplankton and Like many of their pelagicLike many their benthicctenophores counterparts, areefficientpredators, of ctenophores,Benthic members ofthefamily Coeloplanidae(Order Platyctenida, Phylum

(Mills 1998).The majority ofcoelop et 1997).However,al. recent observationshave shown may tentacles that an serve

inhabiting macroalgae, and 1,000 to 1,500 individuals of macroalgae,and1,000to1,500individuals inhabiting - 2 . Also, in South Florida Glynn et al. (2017) observed100s SouthFloridaGlynnetal.(2017) ofindividuals . Also,in

inhabiting Hawaiiatpopulationdensitiesashigh10,000 in rucial rucial role inpopulation counts ofStudiesmany have species.

ture. Whenture. the fishing, attentacles canextendto lanids areectosymbionts and ofalgae diverse 2

Coeloplana of substrate patches.Galt (1998)noted substrate of

and one species oftheand onespecies genus waltoniCoeloplana cal marine environments - branches) armed with

on V.

biofouling communities,biofouling commonly2 ranges 2014.& Renegar behaviorsof defensive maytentacles functiondefensively protection also in againstpredators. Herewe purpose.alternative Hereand weofferevidence photographic coeloplanid behavioral that multiformis of predators [ known crabpredator themdislodging positionfromresting byforceful aj water magnification. Agitation orpredator simulation was effected bypricking ctenophores, madeObservations were withthenaked microscopically visually eyeand 35X at8to octocorals and algae served natural for as substrates weeks’few several from durationonmultiple daysto occasions host 2014to2018.Ctenophore calyce by of are ctenophoredefensive behaviors herein described, extensionof the compact tangles tentacle inhabit species habitats, is1 of biotic its host. Woods & Kanazawa 1951,Woods ctenophore Kanazawa were offered prey & (see Glynnet 2018). al. m gastropod This article isThis article by protected copyright. All rightsreserved. Accepted Article V. multiformis s and by polyps All behaviorshere observed reported were incaptive over insoutheast Florida a

, sea the anemone ollusk ollusk - V. 2 mm inbodylength, cryptic.translucent, Both andnotably ctenophore species -

rich communities with

(Fig. 1a,b),andshelter Coeloplana waltoni Vallicula multiformis Cyphoma Portunus C. waltoni Vallicula multiformis Vallicula

gibbosum Exaiptasia pallida Exaiptasia pallida

sayi

(Fig. 1c,d). (Gibbes

occurs occurs at 2 numerous potential predatorsnumerous and potential competitors. Two types

Linnaeus 1758andthe pygmy Linnaeus angelfish occurs occurs in (0.25 shallow - seeking andoctocoral behavior beside within

- 1850)]. Additionally, Rankin 1956and 8 mm inbodylength,

(Agassiz (Agassiz in 1864),Verrill, of and - 10 m inexposed onoctocorals depth coastal V. multiformis

ets, ofa andprobingwith acheliped Coeloplana waltoni - 2.0 msheltered depth),

and naturally occurring and often assumes color the C. waltoni Centropyge argi describe the

, respectively.

C. waltoni Glynn, Bayer

live

host , the

length, with length, regularlytentilla spaced theirand deployed along lengths. withzooplankton.water were greatlyextended, Tentacles several times ctenophore’s body the cond water individuals settledindividuals aroundusually bases with partialentry or the ofcal polypsoccupying thatexpanded and blockedphysically entry. As a result, ctenophore often insmaller individuals (~1mm usually length). were Thectenophores repulsed in bythe thepolyp’scalyxand attemptto enter protective (a Thisbehavior cup). escape occurredmo rate fleeing of Meancontact. escape l Upon stimulation, rims ofoctocoral calicesposition tobetter themselves fortentacle extension water inthe column. of that tangles, mmlocomotion was0.13 s motionless.and remainedstimulation Uponrepeated theywould begin to move; mean escape extrusion,tentacle typical the ctenophores bothtentacles extended dense as a ofthe tangle oneach side 1a,body (Fig. Accompanying b). example byperforminga simulated predator attack This article isThis article by protected copyright. All rightsreserved. Accepted Article V. When tentacleof extension feeding,the behavior individuals of Individuals of

while others while others left them extended.

multiformis itions. In feedingitions. In trials,tentacleextension occurred amatterminutes in of inflowing V. multiformis C. waltoni . of However, individuals V. multiformis ocomotion 0.067mm was s - 1

. Fleeing individualswould typically approach polyp anoctocoral (n = 6individuals).(n = Some ctenophoresretractedthetentacle fleeing

would quickly tentaclesretract its andmoveaway fromof point the

remained motionlesslow under light andlow flow tostill

ly flattened bodies side) their (oral against substratethe C. waltoni - 1 –

(n = 5individuals),(n = aboutone ctenophores quickly, afew within seconds,

would typically movewould typically outer the to yces they where werestill

C. waltoni Upon agitation

- was similar to half the –

for st individuals individuals of bo 30to60seconds.between camouflaged virtuallywell and 1c, invisible (Fig. d). Thetime seek usually to refuge ranged greatly reduced.greatly consumed shelt in resulted ctenophore fleeing behavior seeking and gastropods shelter. Grazing invariably contractions andtentacle retraction. Continuing by andpursuit mollusk grazing, the angelfish non al.(Glynn et successful 2018),anemones wereinsubduingandingesting usually the feeding During vertical trials, whenctenophores were introducedontothe discfrom oral above fromdisengage encounter, with the tentaclerelaxation, thus individuals in engaged rapid tentacle contraction and relaxation. Theanemone first to wasthe Thus tentacles. begana back andforth “tug response, the ctenophore quickly ejected tentacle tanglesthatseveralensnared ofthe anemon immediately grasping the ctenophore with atentacle andpulling it towardmouth. its In from plankton)could the prey beacritical factorin captureor escape. ctenophores, suggesting that the angle This article isThis article by protected copyright. All rightsreserved. Accepted Article - visual and mollusk grazer the vi Active encounters between encounters Active individuals of exposurePetriHorizontal in dishesof equal nearly

ering ctenophores, butcaptureof the success ctenophores by fishpredators was th

V. multiformis V. multiformis

and anemone the sual fishsual predator generallyinvolved body ctenophore

of contact (horizontallyof contact verticallyfrom or benthos the - of - war” thatlastedminutes, from with 2to3 both C. waltoni E. pallida

- sized 1(< cm body length) greatest

allowing the toctenophore escape. on their hosts withthe octocoral , resulted in the sea inthesea , resulted anemone

e’s e’s

multiformis ctenophore ctenophore controlpopulation and structure. bedirectedtoward identifyingpredatorsshould ofbenthicctenophores the and theirinfluence on observationsoccurrence underof laboratory these field natural attention conditions. Further, communities Florida. Achief studies insubtropicalSouth focusfuture of sh highnotably of abundances ctenophores benthic in species the injuriesrole in reducing and l to octocoral mimicrycalyces and Inaddition, polyps. ascompact,both tentacles twisted masses. madethat themmore visible. slightly individualslarger of intimidation, nobioluminescent responses wereinthebenthiccoeloplanids;observed however speciesperformedboth ctenophore Indifferent stylesofescape behavior. regards to – categories revieweddefensive byMackie damage byassociated zooplankters caused instead ofdamage from Of predators. three major the andctenophores, heemphasizedcnidarians thei contractions review ofthebody.InMackie’s (1995) strategiesofpelagic defensive the swimmingshowed increasing stimulation, to effected andmuscular responses byciliary activity etal.(Mackie 1993, 1992,MatsumotoHarbison pe Mackie 1995). All and This article isThis article by protected copyright. All rightsreserved.

Accepted ArticleC. waltoni There arefew involvedThere behavioralobservationsofctenophores escape in responses In conclusion, thevarious described defensive herebehaviors likely contribute to the , colorand host texture and by

often demonstrated a type slight ofinvolution,i.e. crumpling whenstimulated, and C. waltoni osses fromosses predators. visual assumed color in the warmermonths(June apinkish

V. multiformis – C. waltoni

C. waltoni C. involution, intimidation displays),(visual andescape

mportance of mportance reducingaccidentalcontact and

typically remained motionless and extruded (by virtue oftranslucency)

– would usu

adoption ofhostcolorationby adoption

- rich octocoralrich andbiofouling ally flee, takingrefuge adjacent lagic species studied ould verify the –

likely playsa - October) October) V.

, Thanks are personnelThanks are due the oftheandOpen Recreation Parks, Spaces Department, namely Alamaru, B.W. A., Hoeksema, T.vanderMeij, and D.Huchon. S.E. 2017.Moleculardiversity Alamaru, E.Brokovich,andY.Loya.2015.Fournewspeciesthreerecordsof A., Cited Literature DOI:10.1038/s41598017 (Coeloplanidae). Scientific ctenophores of Nature 7:6365 benthic Reports, benthic ctenophores (Family: from Coeloplanidae) RedSea.Marine the Biodiversity 46:261 suggestions that improved note. this ctenophoreBeach DiversClub,forhelpwith collections. Claudia E.Mills offered helpful laboratoryloaned supplies. We Samand thank Maddingly also Tom Florida South Hughes, access allowing andcollections theat Crandon ParkMa Robert McQueeny, MarjorieSuarez Miamiand Chantal Victor, This article isThis article by protected copyright. All rightsreserved. Accepted Article

- 06505 - 4.

Acknowledgments

rina. Lizarina. MerlyandBrand Larry kindly

- Dade County, FloridaDade County, for - 279.

Emson, R. I.,P.Eeckhaut, andC.LoBue. Flammang, 1997.Functional and morphology ofthetentacles Invertebrate Invertebrate Biology 1 insouthCoeloplanidae) env Florida: W.,Glynn, P. B.Coffman, S.G. M.P.C.Fuller, Williams, Moorhead, M. K. K. D. Primov, T. W.,Glynn, P. F.M.Bayer,andD.AbigailRenegar. 2014. ofthe C.P. Galt, 1998.Natural history benthicctenophore N. Fortson, R. N. Barrales, andP.J.Glynn.N. Fortson,R.Barrales, ctenophores 2017.Benthic (Platyctenida: Biological minute ctenophore (: benthic Platyctenida) from Florida. south Proceedings ofthe AmericanBay, Hawaii.(Abstr.) 38(5):181a. Zoologist platyctenean ctenophore setosum Zoomorphology (Echinodermata, Echinoidea). 117:165 oftentilla Coeloplana bannworthi (Ctenophora,Platyctenida), anectosymbiontofDiadema This article isThis article by protected copyright. All rightsreserved. Accepted Article

H. andP.J.Whitfield. 1991. Behavioral andultrastructural on studies the sedentary Society ofWashington 127(2):423 - 15. https://doi.org/10.1111/ivb.12189. Vallicula multiformis ironmental conditions, habitats, abundances, and behaviors. - . Hydrobiologia 216/217:27 436.

Coeloplana waltoniCoeloplana Vallicula multiformis

- 174.

- 33. , of a newspecies

in Kaneo

he

Mackie, G. Mackie, inplanktoniccoelenterates. strategies O. 1995.Defensive Mar. Behav. Fresh. W.,Glynn, P. B.Coffman, K.D. S.J.Vanderwoude, R.M. Primov, Moorhead, G.N.Barrales, Matsumoto, observations G.R. G.I.and 1993.Insitu offoraging, Harbison. feedingandescape Rottnest Island,Western D.I.WalkerWellsAustralia. andF.E.pp. 385 (Eds.), Coeloplanidae)Platyctenida: from Australia. The Western In: Flora andFaunaSea Grass of Matsumoto, thompsoni G.I.1999.Coeloplana sp.nov.,anewbenthic ctenophor G. Mackie, C.O., Mills, E.,andC.L.Singla. 1992. Giantaxons andescape swimming in 26:119 Physiol. 117: 279 beh Australia, Western AustralianJanuary 1996.Western Museum, Australia. Perth, Western Proceedings ofthe9 Euplokamis dunlapae Florida:south predator Williams,K. andR.P.Roemer.B 2018. This article isThis article by protected copyright. All rightsreserved. Accepted Article avior avior in threeorders Beroida. ctenophores: MarineBiologyofLobata, Cestida, and oceanic - 287.

- 1 29. th

(Ctenophora: BiologicalCydippida). 182:248 Bulletin International Biological Workshop,Marine heldat Rottnest Island,

- prey interactions. Biologyprey Invertebrate 1 enthic ctenophores enthic (Platyctenida: in Coeloplanidae)

- 18. doi:10.1111/ivb.12212. - 256. - 393, e (Ctenophora:

Rankin, J. J. 1956. The structure and Rankin, J.of 1956.Thestructure biology C.E.Mills, 1998.PhylumCtenophora: list ofall speciesnames.valid online Available at and 208 fully extended tentacle tangles, ~5 mm anindividual bodylengths; of of Fig. 1Photomicrographs oftwoindividuals platyctenid platyctenid ctenophore. ofthe Journal ofLondon,Zoology43: Linnaean Society 1998, updatedestablished March last 12June2017. http://faculty.washington.edu/cemills/Ctenolist.html. Pu This article isThis article by protected copyright. All rightsreserved. Accepted Article 209

octocoral hostoctocoral

attempting to 1.5 enter a calyx (d), mm bodylength. Eunicea tourneforti

moving rapidly inescape responsepast a calyx (c), Vallicula multiformis Vallicula multiformis Vallicula

blished by the author,webpage bythe blished

(a, b)(a, motionless with , gen. nov., etsp. a Coeloplana Coeloplana waltoni 55 - 71.

on This article isThis article by protected copyright. All rightsreserved. Accepted Article