Copepod sensitivity to flow fields: detection by copepods of predatory ctenophores

MARINE ECOLOGY PROGRESS SERIES Vol. 323: 205 211, 2006 Published October 5 Mr Ecol Prog Ser Copepod sensitivity to flow fields: detection by copepods of predtory ctenophores Rebecc J. Wggett 1, *, Edwrd J. Buskey 2 1 Ntionl Ocenic nd Atmospheric Administrtion, Ntionl Ocen Service, 101 Pivers Islnd Rod, Beufort, North Crolin 28516-9701, USA 2 The University of Texs t Austin, Mrine Science Institute, 750 Chnnel View Drive, Port Arnss, Texs 78373, USA ABSTRACT: Copepods hve the mechnoreceptive bilities to detect velocity grdients generted by pproching predtors nd the bility to respond to these predtors within milliseconds. Ctenophores produce low-velocity feeding current to entrin slow-swimming nd non-motile prey. Since copepod species vry in their sensitivity to hydrodynmic disturbnces, it is possible tht species will differ in their bility to distinguish flow-generting ctenophores from the surrounding fluid. Predtorprey interctions were recorded between the ctenophore Mnemiopsis leidyi nd 3 copepod species, Acrti tons, Prclnus prvus nd Temor turbint. Although A. tons is more sensitive to hydrodynmic disturbnces, T. turbint ws most successful in escping the ctenophore predtor. T. turbint entered the inner lobe re (cpture surfces) of the ctenophore significntly less thn either A. tons or P. prvus nd were better ble to escpe both encounters nd contcts with the inner lobes. These results suggest tht sensitivity to velocity grdients my ply only minor role in determining escpe success nd n intermittent swimming pttern my increse susceptibility to cpture by flow-generting predtors. KEY WORDS: Mechnoreception Predtor prey interctions Ctenophore Escpe behvior Resle or republiction not permitted without written consent of the publisher INTRODUCTION Ctenophores Mnemiopsis leidyi A. Agssiz (1865) re common nd importnt predtors in plnktonic communities. Their bility to rpidly cpture nd ingest prey (Bishop 1967,Wggett & Costello 1999) nd their high growth (Reeve & Wlter 1978) nd reproductive rtes (Bker & Reeve 1974) llow them to significntly lter plnkton dynmics. Their impct on plnktonic communities hs been documented in esturies long the US Atlntic cost where they occur nturlly (Burrell & Vn Engel 1976, Deson 1982) nd in the Blck Se nd the Se of Azov where they hve been introduced (Shignov et l. 2001). Lobte ctenophores, such s Mnemiopsis leidyi, forge by swimming forwrd with their lobes spred open (Min 1928, Mtsumoto & Hmner 1988). They re propelled by the beting of their 8 exterior ctene rows (Mtsumoto & Hmner 1988). Continuous beting of interior, uriculr cili cretes low velocity inwrd flow field, which slowly drws wter into the orl lobe re (Mtsumoto & Hmner 1988, Costello & Coverdle 1998). Ctenophores re mbush-entngling predtors (Greene 1985) tht possess specilized cpture surfces such s tentcles or tentill, nd colloblsts (mucus-producing cells) (Frnc 1978, Crré & Crré 1993, Wggett & Costello 1999). The ctenophore Mnemiopsis leidyi employs 2 mechnisms for cpturing prey: (1) uriculr cili generte n inwrd flow field to cpture zooplnkton tht hve little to no motility nd (2) highly motile zooplnkton, such s copepods, swim directly into the cpture surfces, primrily the inner orl lobe re, where they dhere to the sticky surfce (Wggett & Costello 1999). The flow field produced by the uriculr cili my lso induce escpe rections in motile prey tht enter the orl lobe re, either through direct swimming or entrinment in the flow field *Emil: rebecc.wggett@no.gov Inter-Reserch 2006 www.int-res.com

206 Mr Ecol Prog Ser 323: 205 211, 2006 (Hmner et l. 1987, Mtsumoto & Hrbison 1993). The flow field frequently strtles the prey into the cpture surfces of the ctenophore, specificlly the inner orl lobes nd the tentille (Hmner et l. 1987, Mtsumoto & Hrbison 1993). Copepods rect to smll-scle hydrodynmic disturbnces in the surrounding fluid (Yen et l. 1992, Kiørboe et l. 1999), which my ffect their susceptibility to predtion by flow-generting predtors, specificlly the ctenophore Mnemiopsis leidyi. Although dult copepods possess the cpcity to detect nd void moving nd even innimte objects in the wter column, certin copepods re unble to void predtion by ctenophores (Bishop 1967, Wggett & Costello 1999). Since copepod species hve vrying degrees of sensitivity to hydrodynmic disturbnces (Fields & Yen 1997, Kiørboe et l. 1999), it is possible tht ctenophores re hydromechniclly invisible to those copepod species with lower sensitivity. The present study exmines the hypothesis tht in voiding cpture by flow-generting predtors, copepods with greter sensitivity to hydrodynmic disturbnces would hve greter escpe success from the flow-generting predtor, Mnemiopsis leidyi. Three similrly sized, esturine copepod species, Acrti tons, Prclnus prvus nd Temor turbint, were exposed to the ctenophore M. leidyi nd predtor prey interctions were observed. The sensitivity of A. tons hs been exmined by number of reserchers. In response to siphon flow, the threshold sher vlue of dult A. tons hs been reported to be <0.6 s 1 (Fields & Yen 1997 [djusted by Kiørboe et l. 1999], Kiørboe et l. 1999, Wggett & Buskey 2006). Recently, threshold sensitivities of 4.25 nd 2.71 s 1 were obtined for P. prvus nd T. turbint, respectively (Wggett & Buskey 2006). Given this informtion, we would therefore expect A. tons to hve the gretest escpe success during interctions with M. leidyi, with T. turbint escping slightly more often thn P. prvus. MATERIALS AND METHODS Animl collection nd cre. Mnemiopsis leidyi were collected by hnd-dipping with plstic beker from the surfce wters of the mrin t The University of Texs Mrine Science Institute, Port Arnss, Texs, USA (27 50.3 N; 97 03.1 W). They were mintined in 8.3 l quri into which continuously-flowing filtered sewter from the Arnss Ship Chnnel ws pumped slowly. Ctenophores were fed 1 to 2 times dily with newly htched Artemi slin nuplii, nd their diet ws supplemented 2 to 3 times week with wild zooplnkton. We chose 3 clnoid species of similr size nd vrious routine swimming behviors (see below), Acrti tons, Prclnus prvus, nd Temor turbint, to evlute the bility of copepods to detect flow-generting predtors. Copepods were collected by tying 0.5 m dimeter 153 µm mesh plnkton net to The Mrine Science Institute pier nd llowing it to strem in the Arnss Ship Chnnel for pproximtely 10 min, depending on the velocity of the current. Contents of the cod end were plced in smll plstic bucket nd diluted with sewter prior to returning to the lbortory. Plnkton smples were gently scooped from the bucket using plstic ldle nd were exmined under dissecting microscope. Adults of the 3 clnoid species were isolted using wide-bore pipette into 50 ml plstic bekers contining 0.2 µm porosity filtered sewter. Copepods were used for experimenttion within 1 h of sorting. Copepod swimming ptterns. For ech copepod, 8 groups of 5 individuls were isolted. A single group ws then dded to 2.3 8.0 4.0 cm cler crylic plstic chmber filled with 0.2 µm porosity filtered sewter. They were given 10 min cclimtion period. Routine swimming behvior of the copepod species ws then recorded for 2 min with stndrd videogrphic techniques using video cmer (Cohu model 3315) equipped with Nikon Nikkor 55 mm lens. The chmber ws bcklit using ring of ner-infrred light emitting diodes. Experiments were repeted for the remining copepod groups (24 groups in ll). Swimming behvior ws nlyzed to determine both routine swimming speeds nd ptterns. Predtor prey interctions. We rn 5 sets of experiments for ech copepod species. In ech experiment pproximtely 100 copepods were used long with different individul ctenophore predtor c. 2 cm in totl length. Interctions were recorded (30 frmes s 1 ) for 30 min using cmer (Cohu, model 3315) equipped with Nikon Nikkor 55 mm lens. Detils of copepod escpe rections were exmined by recording predtor prey interctions. A smll ctenophore (<2 cm) ws plced within nrrow 9.1 5.0 9.7 cm cler crylic plstic chmber filled with 0.2 µm filtered sewter. The ctenophore ws held sttionry by tethering it to 20 µl borosilicte cpillry pipette, using the method described by Wggett & Costello (1999). The pipette ws ttched to the borl end of the ctenophore by pplying slight vcuum pressure, nd ws held in plce by smll clmp. After 10 min cclimtion period, pproximtely 100 copepods of single species were dded to the chmber. Escpe rections were recorded t 1000 frmes s 1 using Redlke MotionMeter model 1130-0003 nd plyed bck t 30 frmes s 1 for recording on stndrd video using Pnsonic AG1960 videocssette recorder. Experiments were replicted 6 times for Acrti tons nd Prclnus prvus, nd 8 times for Temor turbint, in order to observe pproximtely

Wggett & Buskey: Copepod sensitivity to ctenophore flow fields 207 50 escpe rections per species. Illumintion ws provided by fiberoptic light centered on the ctenophore nd ring of infrred light-emitting diodes to increse light for imging nd to compenste for the shortened exposure time of the high-speed cmer. A ruler ws videotped t the end of ech experiment for clibrting distnces. Video-computer motion nlysis techniques were used to determine escpe speed, ccelertion, nd number of thrusts per jump for ech species (Buskey et l. 2002). Video nlysis. Interctions between the ctenophore nd the copepods were reviewed vi slow-motion plybck. Frme-by-frme nlysis llowed quntifiction of the events. Events in the interction were ctegorized using the terminology nd criteri defined by Wggett & Costello (1999) (Tble 1). These criteri were dpted from the predtion model first described by Holling (1959). Interctions between copepod nd ctenophore re interpreted s chronologicl sequence in which the copepod my exhibit n escpe rection upon encountering the ctenophore or it my require direct contct with the ctenophore to initite the rection (Tble 1). The high-speed video recordings of individul copepods jumping to escpe from the ctenophore were nlyzed to evlute the kinetics of ech species escpe rections. Components mesured included speed, ccelertion, nd the number of pereiopod thrusts per escpe rection. Individul escpe jumps were plyed through the Motion Anlysis VP-110 video-to-digitl processor nd digitized imges were then processed using the ExpertVision Cell-Trk system. Swimming pth, speed, ccelertion, nd number of thrusts per jump were clculted for ech of the observed escpe rections. Sttisticl nlysis. Sttisticl nlyses were performed with Systt softwre (v11). Results of predtion events were compred using 1-wy nlysis of vrince (ANOVA) with pirwise multiple comprisons using the Tukey HSD (honestly significntly different) test. High-speed kinetics of the 3 species escpe rections were compred with Kruskl-Wllis 1-wy ANOVA with pirwise multiple comprisons using Dunn s Method. RESULTS Copepod swimming ptterns Swimming ptterns differed mong the 3 copepod species. However, no significnt differences were found in the men swimming speeds of Acrti tons, 1.42 ± 0.18 mm s 1 (men ± SD), Prclnus prvus, 1.83 ± 0.47 mm s 1 nd Temor turbint, 1.81 ± 0.55 mm s 1. A. tons nd P. prvus both displyed typicl hop-nd-sink swimming pttern (Fig. 1A,B); however, A. tons exhibited more frequent hops nd reched greter speeds during these hops thn P. prvus (Fig. 1A,B). T. turbint ws continuous cruiser, mintining more constnt forwrd swimming pttern (Fig. 1C). Predtor prey interctions Despite the bilities of the copepods to perceive rtificilly produced flow fields, ll 3 species frequently encountered the ctenophore predtor, Mnemiopsis leidyi, determined either by the direct contct of the copepod with the ctenophore or by the detection nd escpe response of the copepod. All species hd similr rte of encounters over time with the ctenophore; however, there were significnt differences between the species in the frequency of encounters with the inner (Fig. 2, ANOVA, p < 0.0005) nd outer surfces of the ctenophore (ANOVA, p < 0.0005). Temor turbint hd significntly more encounters with the outer surfces of the ctenophore thn either Acrti tons (Fig. 2, Tukey HSD, p < 0.001) or Prclnus prvus (Tukey HSD, p < 0.0005) nd less encounters with the inner surfces. The number of escpe rections over time from the ctenophore lso differed significntly mong the 3 copepod species (ANOVA, p = 0.002). Temor turbint displyed significntly more escpe rections thn Acrti tons (Tukey HSD, p = 0.0005). The mjority of T. turbint s escpe rections were in response to the outer ctenophore surfces wheres Prclnus prvus hd significntly more escpe rections Tble 1. Terminology used for clssifiction of predtion events between copepods nd ctenophore predtor, Mnemiopsis leidyi (modified fter Wggett & Costello 1999) Behvior Encounter Contct Escpe rection Escpe Cpture Criteri Initited either by direct contct, lobe response by the ctenophore, or copepod escpe rection Contct between copepod nd ctenophore or cpture of copepod by the ctenophore Rpid locomotor response by copepod propelling the copepod forwrd t high speed Copepod voids ensnrement nd consumption Copepod is consumed by the ctenophore

208 Mr Ecol Prog Ser 323: 205 211, 2006 Fig. 2. Acrti tons, Prclnus prvus nd Temor turbint. Percentge of copepod encounters with the inner nd outer surfces of the orl lobes of Mneniopsis leidyi Fig. 1. Exmples of routine swimming speed ptterns for the 3 copepod species (A) Acrti tons, (B) Prclnus prvus, nd (C) Temor turbint. Ech pth is bsed on the swimming pth of single copepod during 10 s period to the inner surfces of the ctenophore thn either A. tons or T. turbint (Tukey HSD, p = 0.01 nd p < 0.0005, respectively). Prclnus prvus hd sttisticlly more direct contcts with the ctenophore thn either Acrti tons or Temor turbint (Tukey HSD, p = 0.048 nd p = 0.037). There were significnt differences mong species in the number of contcts with the inner surfces of the ctenophore (ANOVA, p < 0.0005). P. prvus contcted the inner lobe surfces with the gretest frequency nd T. turbint with the lest (Tukey HSD multiple comprisons). Significnt differences were found mong the rte of cptures of the 3 copepod species (Fig. 3, ANOVA, p < 0.0005). Prclnus prvus ws cptured significntly more often thn Acrti tons or Temor turbint (Fig. 3, Tukey HSD, p = 0.002 nd p = 0.000, respectively). T. turbint ws cptured significntly less often thn A. tons (Tukey HSD, p = 0.003). Fig. 3. Acrti tons, Prclnus prvus nd Temor turbint. Percentge of encounters with the inner orl lobe surfce of Mnemiopsis leidyi tht resulted in copepod cpture or escpe Escpe performnce from the ctenophore lso vried mong copepod species. Prclnus prvus hd the fstest verge (Fig. 4, 207.7 mm s 1 ) nd mximum (Fig. 5, 413.4 mm s 1 ) escpe speeds (Kruskl-Wllis ANOVA on Rnks, p 0.0005). These speeds were significntly fster thn those reched by Temor turbint (Dunn s method, p < 0.05). P. prvus lso displyed significntly fster mximum ccelertions then either Acrti tons or T. turbint (Fig. 6, Kruskl- Wllis ANOVA, p 0.0005, Dunn s method, p < 0.05).

Wggett & Buskey: Copepod sensitivity to ctenophore flow fields 209 DISCUSSION Of the 3 copepod species exmined, Temor turbint ws best ble to void contct with the inner surfces of the ctenophore. The surfce re of the outer nd inner lobes of ctenophore c. 1.5 cm long would be 3.6 cm 2 nd 0.98 cm 2, respectively. If copepod encounters were proportionl to the surfce re of the ctenophore, we would expect significntly more encounters with the outer lobes. This ws observed only by T. turbint, suggesting tht either Acrti tons nd Prclnus prvus were ctively voiding the outer lobes, or they were more frequently entrined by the ctenophore s flow field. This finding is interesting, since A. tons is known to hve lower threshold deformtion rte (0.57 s 1, Wggett & Buskey 2006, 0.34 s 1 Fields & Yen 1997 [djusted by Kiørboe et l. 1999], 0.38 s 1, Kiørboe et l. 1999), i.e. greter sensitivity to hydrodynmic disturbnces, thn either T. turbint (2.71 s 1, Wggett & Buskey 2006) or its congener T. longicornis, (6.50 s 1, Kiørboe et l. 1999). T. turbint ws better ble to escpe n encounter with the ctenophore once it contcted the sticky inner surfces of the ctenophore. Severl fctors my contribute to the escpe success of Temor turbint. First, its morphology my reduce the number of cptures. Copepods re most vulnerble to cpture when their pereiopods become entngled in the mucus coting on the inner orl lobe surfces of the ctenophore (Costello et l. 1999). The rounded dorsl exoskeleton provides the lrgest surfce re on T. turbint nd contributes to disproportiontely lrge percentge of its totl body surfce re, compred to other copepod species. This lrge dorsl surfce re, nd the contributing body proportions, my reduce the chnce of contct with the vulnerble pereiopods. Furthermore, T. turbint hs shorter ntennl sete, suggesting tht they too re less susceptible to entnglement. Routine swimming ptterns of the 3 copepod species lso vried, nd T. turbint ws the only continuous cruiser observed. We speculte tht the intermittent swimming pttern displyed by Prclnus prvus nd Acrti tons my llow them to become entrined in the ctenophore flow field nd brought into the inner lobe re more frequently. Although A. tons hs lower verge sher threshold thn T. turbint, their sensitivity would differ during the hops nd sinks of their hop-nd-sink swimming. During hops, A. tons swims t men speed of 5.7 mm s 1. At this speed, A. tons would be cpble of detecting sher greter thn 22.5 s 1 (clculted from Visser 2001) vlue much higher thn the threshold of T. turbint (2.71 s 1 ). Copepods re lso cpble of modifying their behvior reltive to the type nd strength of the ssocited Averge escpe speed (mm s 1 ) 250 200 150 100 50 0 b A. tons (n = 49) b P. prvus (n = 50) Species T. turbint (n = 56) Fig. 4. Acrti tons, Prclnus prvus nd Temor turbint. Averge speed chieved by copepods during escpes from Mnemiopsis leidyi. Speeds of species tht shre the sme letter (,b) re not significntly different (Kruskl- Wllis 1-wy ANOVA, p < 0.05) Averge mximum escpe speed (mm s 1 ) 500 400 300 200 100 b 0 A. tons P. prvus T. turbint (n = 49) (n = 50) (n = 56) Species Fig. 5. Acrti tons, Prclnus prvus nd Temor turbint. Averge mximum speeds chieved by copepods during escpes from Mnemiopsis leidyi. Speeds of species tht shre the sme letter (,b) re not significntly different (Kruskl-Wllis 1-wy ANOVA, p < 0.05) Averge mximum escpe ccelertion (m s 2 ) 200 150 100 50 0 A. tons (n = 49) b b P. prvus (n = 50) Species T. turbint (n = 56) Fig. 6. Acrti tons, Prclnus prvus nd Temor turbint. Averge mximum ccelertions chieved by copepods during escpes from Mnemiopsis leidyi. Accelertions of species tht shre the sme letter (,b) re not significntly different (Kruskl-Wllis 1-wy ANOVA, p < 0.05)

210 Mr Ecol Prog Ser 323: 205 211, 2006 stimulus. Kinetic performnce of Prclnus prvus nd Temor turbint hs been evluted in response to n ttcking fish, the hemisessile blenny Acntheblemri spinos, nd ll 3 species were exposed to repetble ner-field hydrodynmic stimulus (Wggett 2005). T. turbint responded with greter mximum nd verge speeds nd mximum ccelertions in response to the blenny compred to the ner-field hydrodynmic stimulus. P. prvus hd similr escpe speeds to both the blenny nd the ctenophore; however, ccelertions were much greter in response to the ctenophore. The ner-field hydrodynmic stimulus elicited much weker escpe responses in ll 3 species in comprison to the blenny nd ctenophore results. Copepod escpe behvior indictes tht the blenny nd the ctenophore predtors creted stronger hydrodynmic stimuli nd were perceived s greter thret to survivl thn the ner-field hydrodynmic stimulus (Wggett 2005). Copepod escpe success from the ctenophore, Mnemiopsis leidyi, is function of swimming behvior, body structure, nd orienttion t the time of contct. Their sensitivity to wter movements my ply only minor role in their bility to successfully void cpture by mbush-entngling predtors such s the ctenophore, M. leidyi. Copepods re lso highly susceptible to predtion by visul predtors nd were cptured lmost 80% of the times they were ttcked by Acntheblemri spinos (Wggett & Buskey 2006b). Although Prclnus prvus hs significntly fster response ltency nd displys n intermittent swimming pttern, they were still cptured frequently by the blenny, indicting these behviorl components did not enhnce their escpe success. A similr result ws found in the predtor prey interctions with M. leidyi. Temor turbint escped significntly more often thn either P. prvus or the more sensitive (lower sher threshold), Acrti tons. Copepod escpe success is therefore complex process, resulting from the integrtion of vrious components (i.e. kinetics, response ltency, sher threshold etc.), which re difficult to predict, considering the copepod s bility to modify its behvior nd the predtor s bility to djust their ttck behvior. Despite their bilities to detect minute fluid disturbnces on the scle of nnometers (Yen et l. 1992, Buskey et l. 2002), copepods re still preyed upon nd consumed by flow-generting predtors, such s ctenophores, t high rtes. Ctenophores hve been estimted to crop s much s 31% of zooplnkton popultion density dily (Bishop 1967, Deson 1982). The wter disturbnces creted by the ctenophore pper to be below the threshold for detection by mny copepod species. As mbush-entngling predtors, ctenophores rely on flow-generting mechnisms nd the movement of their prey to initite encounters. Ctenophores swim slowly through the wter column t rtes of 0.6 cm s 1 while forging for prey (Mtsumoto & Hrbison 1993, Kreps et l. 1997). The low velocity flow field creted by the constnt beting of their uriculr cili my ct to reduce the production of the forwrd bow wve mde by the forwrd swimming ctenophore. Acknowledgements. We gretly pprecite the guidnce, dvice nd comments offered by L. A. Fuimn, G. J. Holt, P. A. Montgn nd P. H. Lenz. We thnk S. Strtmnn for ssisting in the collection, cre, nd mintennce of the ctenophores. Funding for this reserch ws provided by the Ntionl Science Foundtion through Grnt OCE-9910608, The University of Texs Mrine Science Institute E. J. Lund Fellowship nd the Lur Brooks Flwn, M.D. Endowment Fund. This is The University of Texs Mrine Science Institute contribution number 1407. LITERATURE CITED Bker D, Reeve MR (1974) Lbortory culture of the lobte ctenophore Mnemiopsis mccrdyi with notes on feeding nd fecundity. Mr Biol 26:57 62 Bishop JW (1967) Feeding rtes of the ctenophore, Mnemiopsis leidyi. Chespeke Sci 8:254 261 Burrell JVG, Vn Engel WA (1976) Predtion by nd distribution of ctenophore, Mnemiopsis leidyi A. Agssiz, in the York River Estury. Estur Cost Mr Sci 4:235 242 Buskey EJ, Lenz PH, Hrtline DK (2002) Escpe behvior of plnktonic copepods in response to hydrodynmic disturbnces: high speed video nlysis. Mr Ecol Prog Ser 235: 135 146 Crré D, Crré C (1993) Five types of colloblst in cydippid ctenophore, Minicten lutelo Crré nd Crré: An ultrstructurl study nd cytologicl interprettion. Phil Trns R Soc Lond B 341:437 448 Costello JH, Coverdle R (1998) Plnktonic feeding nd evolutionry significnce of the lobte body pln within the Ctenophor. Biol Bull 195:247 248 Costello JH, Loftus R, Wggett R (1999) The influence of prey detection on cpture success by the ctenophore Mnemiopsis leidyi feeding upon dult Acrti tons nd Oithon colcrv copepods. Mr Ecol Prog Ser 191:207 216 Deson EE (1982) Mnemiopsis leidyi (Ctenophor) in Nrrgnsett By, 1975 1979: Abundnce, size composition nd estimtion of grzing. Estur Cost Mr Sci 15:121 134 Fields DM, Yen J (1997) The escpe behvior of mrine copepods in response to quntifible fluid mechnicl disturbnce. J Plnkton Res 19:1289 1304 Frnc J-M (1978) Orgniztion nd function of ctenophore colloblsts: An ultrstructurl study. Biol Bull 155:527 541 Greene CH (1985) Plnktivore functionl groups nd ptterns of prey selection in pelgic communities. J Plnkton Res 7: 35 40 Hmner WM, Strnd SW, Mtsumoto GI, Hmner PP (1987) Ethologicl observtions on forging behvior of the ctenophore Leucothe sp. in the open se. Limnol Ocenogr 32(3):645 652 Holling CS (1959) The components of predtion s reveled by study of smll-mmml predtion of the Europen pine swfly. Cn Entomol 91:293 320

Wggett & Buskey: Copepod sensitivity to ctenophore flow fields 211 Kiørboe T, Siz E, Visser AW (1999) Hydrodynmic signl perception in the copepod Acrti tons. Mr Ecol Prog Ser 179:97 111 Kreps TA, Purcell JE, Heidelberg KB (1997) Escpe of the ctenophore Mnemiopsis leidyi from the scyphomedus predtor Chrysor quinquecirrh. Mr Biol 128: 441 446 Min RJ (1928) Observtions of the feeding mechnism of ctenophore, Mnemiopsis leidyi. Biol Bull 55:69 78 Mtsumoto GI, Hmner WM (1988) Modes of wter mnipultion by the lobte ctenophore Leucothe sp. Mr Biol 97: 551 558 Mtsumoto GI, Hrbison GR (1993) In situ observtions of forging, feeding, nd escpe behvior in three orders of ocenic ctenophores: Lobt, Cesti, nd Beroid. Mr Biol 117:279 287 Reeve MR, Wlter MA (1978) Nutritionl ecology of ctenophores review of recent reserch. Adv Mr Biol 15: 249 287 Shignov TA, Mirzoyn XA, Studenikin EA, Volovik SP nd 5 others (2001) Popultion development of the invder ctenophore Mnemiopsis leidyi, in the Blck Se nd in other ses of the Mediterrnen bsin. Mr Biol 139: 431 445 Visser AW (2001) Hydromechnicl signls in the plnkton. Mr Ecol Prog Ser 222:1 24 Wggett RJ (2005) Ecologicl, biomechnicl nd neurologicl correltes of escpe behvior in clnoid copepods. PhD disserttion, The University of Texs, Austin, TX Wggett RJ, Buskey EJ (2006) Copepod escpe behvior in non-turbulent nd turbulent hydrodynmic regimes. Mr Ecol Prog Ser (in press) Wggett RJ, Buskey EJ (2006b) Clnoid copepod escpe behvior in response to visul predtor: sensory nd behviorl chrcteristics contributing to escpe success. Mr Biol (in press) Wggett R, Costello JH (1999) Cpture mechnisms used by the lobte ctenophore, Mnemiopsis leidyi, preying on the copepod Acrti tons. J Plnkton Res 21:2037 2052 Yen J, Lenz PH, Gssie DV, Hrtline DK (1992) Mechnoreception in mrine copepods: Electrophysiologicl studies on the first ntenne. J Plnkton Res 14:495 512 Editoril responsibility: Howrd I. Browmn (Associte Editor-in- Chief), Storebø, Norwy Submitted: Jnury 11, 2006; Accepted: Mrch 29, 2006 Proofs received from uthor(s): September 18, 2006