Abstract
Marine invertebrates that move besides lento to evade unfavorable environmental change may rather exhibit phenotypical malleability, allowing them to adjust to varying conditions. The orange-footed ocean cucumber Cucumaria frondosa is a slow-moving suspension eater that is preyed on by the purple sunstar Solaster endeca. The sea cucumber ’ sulfur antipredator behavior involves changing form and detaching from the substrate, which might increase its probability of being displaced by water apparent motion into an unsuitable environment. We hypothesized that sea cucumbers ’ antipredator responses would be diminished under stronger hydrodynamic forces, and that behavioral strategies would be flexible so that individuals could adjust to frequent changes in water flows. In a natural orange-footed sea cucumber habitat, individuals lived along a pronounce hydrodynamic gradient, allowing us to measure antipredator behavior under different water flow strengths. We placed purple sunstars in physical touch with sea cucumbers living at respective points along the gradient to elicit antipredator responses. We then repeated this routine in a lab mesocosm that generated fallible and strong hydrodynamic forces similar to those observed at the field site. Subjects in the mesocosm experiment were tested in both wave conditions to determine if their antipredator behavior would change in response to sudden environmental change, as would be experienced under deteriorating sea conditions. Antipredator responses did not covary with hydrodynamic forces in the field. however, antipredator responses in the mesocosm experiment increased when individuals were transplanted from firm to weak forces and decreased when transplanted from weak to hard forces. overall, our results indicate environmentally induced malleability in the antipredator behavior of the orange-footed ocean cucumber .
Introduction
slow-moving and sessile marine invertebrates that populate dynamic environments can not well relocate to a more favorable habitat when environmental conditions deteriorate. alternatively, individuals may mitigate deleterious effects in situ through alterations in morphologic, physiological, or behavioral traits that are induced by environmental change, a phenomenon known as phenotypical malleability ( Stearns 1989 ; Dukas 1998 ; Price et aluminum. 2003 ; Padilla and Savedo 2013 ). For example, when exposed to relatively high wave forces, mutualistic sponges ( Haliclona caerulea ) and red alga ( Jania adherens ) develop larger attachment surfaces and increase organic density, which allows them to better withstand the sharpen mechanical try ( Carballo et alabama. 2006 ). similarly, mussels Mytilus edulis increase doggedness by producing more byssal threads during the winter months when flows tend to be stronger ( Carrington 2002 ). even some free-moving nautical organisms exhibit phenotypical malleability when they can not escape deteriorating conditions. Purple ocher stars Pisaster ochraceus, for case, alter their morphology to reduce scuff when exposed to higher hydrodynamic forces ( Hayne and Palmer 2013 ). such adaptations allow slow-moving organisms to withstand environmental fluctuations that more mobile species frequently avoid ( Gibson 2003 ). Along with a dynamic environment, slow-moving and sessile marine organisms must besides cope with mobile predators. consequently, a cortege of specify antipredator responses, known as inducible defences, have evolved ( Adler and Harvell 1990 ). When the predation threat is not contiguous, prey organisms may produce morphologic defences. For example, Membranipora membranacea, a colonial bryozoan, produces modern zooids with defensive spines soon after exposure to chemical cues from predators ( Harvell 1984, , 1986 ). effluent body of water from predatory crabs similarly induces shell-thickening in mussels ( for example, M. edulis, Leonard et alabama. 1999 ; Freeman and Byers 2006 ; Semimytilus algosus, Caro and Castilla 2004 ). Although morphologic change can occur relatively quickly ( e.g., a cabalistic response ; Hultgren and Mittelstaedt 2015 ), it may not occur cursorily enough when an approach is at hand. In these situations, behavioral responses may be faster and more successful ( Padilla and Adolph 1996 ; Heynen et alabama. 2017 ). For model, scallops contacted by predators produce defensive responses ranging from valve closure to a dramatic “ swimming ” escape, depending on the perceive level of threat ( for example, Pecten maximus, Thomas and Gruffydd 1971 ; Argopecten irradians, Winter and Hamilton 1985 ) ; numerous marine invertebrates exhibit similar mobile escape behaviors ( Feder 1972 ).
defensive behaviors may facilitate escape but are frequently subjugate to environmentally mediated trade-offs. For exemplar, fresh water clams Corbicula fluminea evade humble predators by retracting vulnerable tissues and closing their valves ( Saloom and Duncan 2005 ). While protected, the clams can not properly ventilate, and, when dissolved oxygen levels become besides low, the clams are forced to reopen their valves ; frankincense, clams face a greater tradeoff between depredation risk and physiological demands when live in hypoxic conditions ( Saloom and Duncan 2005 ). conceivably, most slow-moving and sessile marine invertebrates in shallow habitats must respond to predators under assorted environmental conditions, since conditions immediately surrounding the animal are often changing. The calculate of the award cogitation was to use complementary color field and mesocosm experiments to investigate environmentally induce malleability in the antipredator demeanor of a slow-moving marine invertebrate with a non-centralized anxious system. Our focal animal, the orange-footed ocean cucumber, is a benthic abeyance feeder ( Klugh 1923 ). In eastern Canada, it is hunted chiefly by the purple sunstar Solaster endeca, which removes up to 2 % of its population per annum ( Himmelman and Dutil 1991 ; Legault and Himmelman 1993 ; So et aluminum. 2010 ). Upon attack by a purple sunstar, orange-footed sea cucumbers exhibit a rapid ( ca. 2 min ) antipredator reception : body elongation and compression, followed, if necessary, by an increase in buoyancy and withdrawal from the ocean floor ( Legault and Himmelman 1993 ; So 2009 ; Gianasi et aluminum. 2015 ). Some testify suggests that this response is adaptive. indeed ( 2009 ) noted that, out of 22 attacks by juvenile purple sunstars on juvenile orange-footed sea cucumbers in a lab experiment, all 5 sea cucumbers that detached successfully escaped ; in contrast, 13 out of 17 ocean cucumbers that remained attached were consumed. additionally, orange-footed sea cucumbers are more likely to exhibit antipredator responses when attacked by imperial sunstars than when attacked by other sea stars that rarely or never consume the sea cucumbers ( Legault and Himmelman 1993 ). This leaning to scale antipredator behavior to the horizontal surface of predation threat foster suggests that the answer is adaptive ( Sih 1986 ; Helfman 1989 ; Lima and Dill 1990 ; Hölker and Stief 2005 ; Edelaar and Wright 2006 ). Body form change and insulation as antipredator responses have besides been documented in early holothurians ( Francour 1997 ). detachment resulting in successful escape from predaceous gastropods ( Tonna spp. ) has been reported in Holothuria scabra and Stichopus horrens ( Kropp 1982 ; Morton 1991 ), and Parastichopus californicus escapes from imperial sunstars and sunflower ocean stars ( Pycnopodia helianthoides ) by swimming ( Mauzey et alabama. 1968 ; Shivji et alabama. 1983 ). thus, detaching probably affords orange-footed sea cucumbers the highest casual of escaping a marauding attack. The risk associated with detach may vary with a sea cucumber ’ s hydrodynamic environment. Small sea cucumbers typically live on shallow seabed ( < 10 megabyte ; Hamel and Mercier 1996 ), possibly because the warm body of water at shallow depths provides safety from sunstars ( Legault and Himmelman 1993 ; So et aluminum. 2010 ). indeed, purple sunstars chiefly target small ( < 15 centimeter in body distance ) ocean cucumbers and broadly avoid shallow seabed ( < 20 megabyte ), where water temperatures frequently exceed the sunstar ’ s optimum foraging temperature of 6°C ( Ursin 1960 ; Franz et alabama. 1981 ; Himmelman and Dutil 1991 ; Hamel and Mercier 1996 ; So et aluminum. 2010 ). however, shallow benthic habitats are besides prone to sudden, relatively large shifts in hydrodynamic forces ( Denny 1988 ). On airy days, water turbulence induced by higher energy airfoil waves can extend deep into the subtidal zone and well into the sea cucumber ’ s upper berth distributional range ( Harmelin-Vivien 1994 ; So et alabama. 2010 ), where it can cause detachment, injuries, or death in hard attached benthic animals ( for example, López et aluminum. 2008 ; Babarro and Carrington 2013 ). Without the ability to control their displacement while floating in the water column ( So et aluminum. 2010 ), orange-footed ocean cucumbers may therefore face a hazard of stranding when they detach in response to a predator, or for any other rationality, in shallow coastal waters. Behavioral malleability might allow sea cucumbers to adjust to changes in the local menstruate environment. Orange-footed ocean cucumbers actively seek centrist flows and move away from impregnable currents that hinder feed, expose them to increased drag, and increase their likelihood of dislodgment ( Sun et aluminum. 2018 ). other holothurians and benthic invertebrates besides exhibit behavioral malleability that reduces their probability of detaching in disruptive water. The sea cucumbers Thyone aurea, Pentacta doliolum, and Pseudocnella insolens answer to increasing hydrodynamic forces by clumping together, which is thought to decrease puff and provide greater surface sphere for attachment ( Barkai 1991 ). similarly, under stronger water flows, the sea urchins Paracentrotus lividus and Strongylocentrotus droebachiensis engage more tube feet to enhance doggedness, or form tighter intraspecies aggregations ( Frey and Gagnon 2016 ; Cohen-Rengifo et aluminum. 2017 ). Reducing the forte and frequency of antipredator responses might therefore be another scheme that sea cucumbers use to mitigate the risk of being washed away in disruptive waters. We hypothesized that hydrodynamic forces influence antipredator responses ( change in body shape and detachment from substrate ) in orange-footed sea cucumbers exposed to purple sunstars. specifically, we predicted that sea cucumbers would : ( 1 ) exhibit watery or fewer antipredator responses under relatively solid versus weak hydrodynamic forces and ( 2 ) increase their responses when moved from relatively strong into decrepit hydrodynamic forces and diminish their responses when experiencing the antonym. We first conducted a field experiment to test whether the lastingness of hydrodynamic forces covaried with depth in a natural orange-footed sea cucumber habitat, and whether antipredator responses of sea cucumbers covaried with the persuasiveness of hydrodynamic forces along the gradient. We then brought ocean cucumbers from our field site into a testing ground mesocosm to isolate possible effects of hydrodynamic forces on antipredator responses. Midway through the mescosm experiment, we conducted a multiplicative inverse transfer experiment to test if individuals respond to relatively sudden shifts in hydrodynamic forces like to those observed under quickly deteriorating ocean conditions.
Materials and Methods
Study site and subjects
We tested antipredator responses of orange-footed ocean cucumbers at, or collected from, Bread and Cheese Cove ( 47°18′30.8″ N, 52°47′19.1″ W ) on the north prop up of Bay Bulls, Newfoundland, Canada. The fundamentals seabed at Bread and Cheese Cove is colonized by grazing-resistant, bolshevik coralline seaweeds ( chiefly Lithothamnion glaciale ). The green ocean urchin, S. droebachiensis, maintains the biological communities in a “ barrens ” state ( sensu Lawrence 1975 ) for most of the year ( Blain and Gagnon 2014 ; Frey and Gagnon 2015 ). We monitored sea cucumbers naturally distributed along a 110-m-long depth gradient ranging from the churning shallow environment at a rocky point on the north prop up of the cove to the calm deep waters located near the middle of the cove to the south. Subjects in the field experiment were 16 orange-footed sea cucumbers of alike sizes ( see below ) selected randomly at depths of 5–11 m. We marked each subject by placing a alone number lead weight within 30 curium of its location, and by removing neighboring sea cucumbers from within a 1-m spoke. One subject ( depth : 10.6 meter ) was excluded from the final sample distribution because it detached from the ocean floor following an experimental predator exposure and could not be relocated. Three empurpled sunstars ( hateful ±SD diameter : 19.5 ± 1.5 centimeter ) were collected from Broad Cove, St. Philip ’ mho ( near Bread and Cheese Cove ), on 29 September 2015, and used as predators. They were transported in 75-L bins filled with seawater to the Ocean Sciences Centre ( OSC ) of Memorial University of Newfoundland, where they were transferred to 30-L methamphetamine holding tanks supplied with a continuous hang of seawater pumped in from the adjacent Logy Bay. Sunstars were not fed during the study ( 29 September to 27 November 2015 ) to standardize their hunger levels and associated behavioral responses upon contacting sea cucumbers. Sea stars are generally kind to food privation, with no detectable physiologic or behavioral impacts over periods of at least 2 months ( Hancock 1958 ; Jangoux and van Impe 1977 ; Rochette et alabama. 1994 ; St-Pierre and Gagnon 2015a ). Subjects in the testing ground mesocosm experiment were 40 orange-footed sea cucumbers collected from across the cogitation site, including 15 individuals tested in the sphere experiment. During the experiment, 2 subjects became stagnant and were discarded. therefore, the final sample size for the mesocosm experiment was 38 individuals ( average ±SD contracted body length : 14.6 ± 1.9 centimeter ; crop : 10.2–18.6 curium ). Sea cucumbers were collected and transported to the lab on 2 and 31 October 2015. During collection, divers detached the ocean cucumbers from the seabed by lightly rocking them from side to side until all podia disengaged. They were placed in big ( 75 L ), labeled containers filled with seawater, and transported to the OSC. Subjects arrived at the facility within 5 planck’s constant of collection and were transferred to 30-L methamphetamine holding tanks ( utmost of 3 individuals per tank ) supplied with a continuous flow of seawater from Logy Bay. Sea cucumbers were maintained in holding tanks for 3 days, then moved into the mesocosm ( oscillatory wave tank, described below ).
Field experiment
Two train scientific divers ( first and third gear authors of present article ) tested each subject on 9, 17, and 24 October 2015. Each 220-s examination was divided into 3 periods : 40-s baseline, 60-s predator photograph, and 120-s post-predator observation ( Figure 1 ). At the beginning of the marauder vulnerability period, 1 experimenter randomly selected 1 of the 3 purple sunstars from a net bag, placed it on the exposed upper come on of the sea cucumber, and gently held it in place until it attached to the sea cucumber with its tube feet. The 60-s vulnerability began the here and now the sunstar and sea cucumber made contact. The experimenter ’ mho hand never made direct contact with the sea cucumber, and the sunstar was removed after 60 s. The subject ’ s demeanor was video-recorded throughout the test with a submersible, high-definition digital video camera system ( Sony HVR-V1 with an Amphibico Endeavor house ; Figure 1D ). For each of 6 individuals, the baseline period of 1 of their 3 tests was shorter than 40 randomness ( 15–35 s ) because of a technical foul issue with the television camera. once a test was complete, divers moved to the following subject and repeated this process until all subjects had been tested. Subjects were tested in the lapp haphazard ordering ( shortest travel guidebook for the divers ) on each of their 3 test days. however, because of limited dive time, we tested one end of the locate in the dawn and the other end in the good afternoon and alternated the order from one test day to the next.
figure 1 .
Open in new tabDownload slide procedure for experimental tests in the field. ( A ) An URSKI with weight and scale legal profession was placed close to a tagged orange-footed ocean cucumber ( Cucumaria frondosa ). ( B ) After 40 second of baseline video, a purple sunstar ( Solaster endeca ) selected haphazard from a mesh topology base containing 3 sunstars was placed lightly on top of the sea cucumber. The sunstar stayed on the sea cucumber for 60 randomness, untouched by divers. ( C ) The sunstar was removed. ( D ) 120 s of post-predator television was recorded. Either the dive weight unit with orange chase attached or classifiable patches of red coralline algae carpeting the ocean floor ( such as the bandage to which the ocean cucumber is attached in dialog box ( C ) were used as static address points to correct body shape unevenness measurements ( see the “ Materials and Methods ” incision for details ). figure 1 .Open in new tabDownload slide operation for experimental tests in the field. ( A ) An URSKI with weight and scale bar was placed near to a tagged orange-footed ocean cucumber ( Cucumaria frondosa ). ( B ) After 40 s of baseline video recording, a purple sunstar ( Solaster endeca ) selected haphazard from a engage bag containing 3 sunstars was placed gently on top of the sea cucumber. The sunstar stayed on the sea cucumber for 60 randomness, untouched by divers. ( C ) The sunstar was removed. ( D ) 120 south of post-predator video was recorded. Either the dive weight with orange tag attached or classifiable patches of red coralline algae carpeting the ocean floor ( such as the patch to which the ocean cucumber is attached in empanel ( C ) were used as static address points to correct consistency form variability measurements ( see the “ Materials and Methods ” section for details ). We note 2 authoritative points about the predator exposures in this learn. First, each sea cucumber ’ randomness physical contact with a purple sunstar was relatively spontaneous and brief because of time constraints imposed by aqualung diving. however, sudden, ephemeral attacks are not strange ; So ( 2009 ) reports a tendency in purple sunstars to approach orange-footed ocean cucumbers from downstream, likely to facilitate surprise attacks, as seen in other sea cucumber predators ( Kropp 1982 ). second, we did not include a positive control in which ocean cucumbers were exposed to an innocuous detail, alternatively of a predator, because other research has shown that sea cucumbers respond more strongly to predators than to innocuous items. Legault and Himmelman ( 1993 ) found that only 20 % of orange-footed ocean cucumbers responded to direct contact with a synthetic rug, with a beggarly ( 95 % CI ) reaction prison term of 223 ( 97 ) s. In line, all ocean cucumbers responded to contact with a imperial sunstar, with a beggarly reaction time of 59 ( 11 ) s. The latter study consequently established that the sunstar elicits a significantly stronger antipredator demeanor than a plus control. hydrodynamic forces were measured continuously with limited subaqueous relative swell kinetics instruments ( URSKIs ; Figurski et aluminum. 2011 ; Figure 1A ). An URSKI consists of a submersible accelerometer ( Onset HOBO UA-004-64 Pendant G Data Logger ) housed in a penetrate, cylindrical, 8-cm-long container epoxied to one end of a sealed, slightly positively buoyant, 90-cm-long ABS pipe ( 8 centimeter in diameter ). The other end of the pipe was tethered with an 18-cm-long twist to eyebolts drilled into the ocean floor at depths of 5 and 11 megabyte, which approximated the upper berth and lower extremes of the depth spectrum. In calm urine, the instrument stood vertically in the urine column with the accelerometer at the upper, untethered end, approximately 1.15 m above the ocean floor. In the presence of water system hang, the release end of the instrument, and therefore the accelerometer, tilted at a focal ratio, direction, and angle reproducible with predominate flows. The accelerometer recorded its own instantaneous acceleration in the x- ( vertical ), y- ( horizontal ), and z- ( horizontal ) directions every 30 s. The y- and z-direction data were used to calculate, by trigonometry, instantaneous acceleration vectors indicative of the horizontal ( parallel to seabed ) flow acceleration to which sea cucumbers were exposed. From this datum, we calculated bastardly hourly hang accelerations at each end of the depth spectrum between 25 September and 31 October 2015 ( stallion surveil duration ). We besides measured local hydrodynamic forces by each capable during its 3 tests by placing a portable URSKI on the ocean floor approximately 30 curium from the subject. This URSKI recorded its own instantaneous acceleration every second throughout the 220-s tests. instantaneous acceleration vectors were calculated as explained above. Because accelerometers were approximately 1 m above the ocean floor, hydrodynamic forces measured may have differed, albeit slenderly, from those experienced by the ocean cucumber 1 molarity below ( Denny 1988 ; Denny and Wethey 2001 ). Any deviation in flow regimes was deemed inconsequent because : ( 1 ) the give study was concerned with effects of proportional ( not absolute ) hydrodynamic forces among test subjects ; and ( 2 ) all test subjects were laying on the bedrock seabed and hence occupied microhabitats that would have influenced local anesthetic flows in similar ways. Activity level in sea cucumbers, like in many early poikilothermic marine invertebrates, varies with water temperature ( Angilletta et alabama. 2010 ; Frey and Gagnon 2015 ; Kühnhold et aluminum. 2017 ; Tagliarolo et aluminum. 2018 ). To ensure that temperature did not confound our analyses, we recorded water temperature at 15-min intervals from 25 September to 31 October 2015 with a temperature lumberman ( Onset HOBO UA-002-64 Pendant ; accuracy ±0.5°C ) bolted to the seabed at both ends of the depth gradient. Water temperature was alike at both depths throughout the experiment ( 5 m depth : think of = 9.5°C, SD = 0.7°C, range = 4.6°C ; 11 thousand depth : mean = 9.3°C, SD = 0.7°C, rate = 5.0°C ). consequently, any effect of temperature on antipredator responses was improbable to differ along the depth gradient studied. The depth of each subject was measured with a hand-held gauge ( Tusa SCA-360 ; accuracy ±0.3 thousand ).
Laboratory mesocosm experiment
The testing ground experiment was carried out in an oscillatory roll tank [ lambert × tungsten : 6 × 1 thousand ; see cooler details in Frey and Gagnon ( 2015 ), St-Pierre and Gagnon ( 2015b ) ; Figure 2 ] that mimicked the back-and-forth menstruate caused by waves in subtidal habitats. One end of the tank contained a rotate jury that generated 15 wave cycles min−1 at a vertex longitudinal speed of 0.2 meter s−1, as measured with a Doppler current meter ( Vector Current Meter ; Nortek ) held approximately 5 cm above the center of the experimental area ( without the structures used to create the microhabitat ; see below ). These conditions approximated the frequency of waves and average water flow speeds at our study site under mince wind conditions ( Frey and Gagnon 2015 ; St-Pierre and Gagnon 2015b ). Waves propagated into a 1.5-m-long section in the center of the tank that was demarcated by nylon net and used as the “ strongly agitated ” section. Another 1.5-m-long department, located at the end of the cooler opposite the wave generating mechanism, was used as the “ weakly agitated ” section. It was separated from the other sections by a cross plywood division that prevented waves from propagating through. To simulate natural ocean floor heterogeneity in the roll cooler, rocks were placed ( diameter : 7–33 centimeter ; concentration : 27.3 rocks m−2 ) on the penetrate of both sections. Chicken wire was attached to the sides of the tank to prevent ocean cucumbers from climbing up the walls. The brandish tank was operated as a close system to hold body of water charge and flow form changeless. To help maintain a temperature close to that of the sea cucumber ’ s natural habitat, the tank was drained day by day from a depth of 37 centimeter to a depth of 20 curium ( a level that ensured that all sea cucumbers remained submerged ) and refilled immediately with seawater pumped in from Logy Bay. Water temperature in the tank was recorded hourly throughout the experiment with a temperature lumberman ( accuracy : ±0.5°C ; HOBO Pendant ; Onset Computer Corporation ). The daily variability in water temperature throughout the experiment ( 15 October to 27 November 2015 ) was 0.84 ± 0.92°C ( beggarly ±SD ).
trope 2 .
Open in new tabDownload slide apparatus for the mesocosm experiment. ( A ) Top-view schematic of the wave tank depicting the 2 sections, their dividers, and other components of the tank apparatus ( see the “ Materials and Methods ” section for details ). ( B ) Sample video recording skeleton from the strongly agitated incision. Darkly colored sea cucumbers are visible against the light tank. Small, total orange tags were attached to rocks and positioned directly adjacent to each sea cucumber to keep chase of their identities. figure 2 .Open in new tabDownload slide setup for the mesocosm experiment. ( A ) Top-view schematic of the wave tank car depicting the 2 sections, their dividers, and other components of the tank apparatus ( see the “ Materials and Methods ” section for details ). ( B ) Sample video recording frame from the strongly crusade section. Darkly colored ocean cucumbers are visible against the light tank. Small, number orange tags were attached to rocks and positioned immediately next to each ocean cucumber to keep track of their identities. The tank was illuminated by indirect, natural light through a window, and by auxiliary artificial fall. There were 2 sources of artificial ignite : ( 1 ) 2 120-cm-long, 32-W Sylvania Octron fluorescent tubes ( 4100 K, FO32/841/ECO ) and 1 120-cm-long, 34-W General Electric Cool White ( 4100 K, Hg, F34 CW WM ECO EX ) fluorescent tube suspended from the ceiling approximately 2 m above the wave tank car ; and ( 2 ) 2 500-W Globe Electric Company Inc. model 04787 and 2 150-W Sylvania model 4406156R halogen bulb ( 1300 W in entire ) on a short ( 1.75 molarity ) stand placed outside of the roll cooler approximately 1.5 meter from the 2 working sections. Fluorescent tubes were permanently turned on, as per build code, whereas halogen light bulb were turned on only during television read of subjects to provide adequate light for crisp video recording footage. illuminance from the fluorescent tube at the water surface, based on 6 measurements with a portable lux meter ( accuracy : ±10 sixty ; Hi97500 ; Hanna Instruments ), was 216.6 ± 18.6 sixty ( mean ±SD ). Before testing began, we stopped waves and move subjects into the cooler department that simulated their locate of beginning in the field : those from the deep ( > 8 meter ) end of the gradient went into the decrepit agitated section of the tank, whereas those from the shallow ( < 8 thousand ) conclusion went into the powerfully agitate incision. Each section could accommodate up to 10 sea cucumbers at a time. This concentration was like to the highest densities observed at our field locate ; anterior to testing, up to 6 extra sea cucumbers had been removed from within a 1-m radius of each subject in the field experiment. We gave subjects 60–100 min to attach to the substrate before gradually raising the flow to 15 waves min−1. Subjects were individually marked by placing alone count lead weights beside them, and by repositioning weights throughout the experiment whenever subjects moved ( motion was infrequent ). Before testing began, all subjects were acclimated to the wave tank for 3 days. During acclimatization to the powerfully agitated section, 8 of the 15 individuals that were previously tested in the field experiment moved around the tank when experimenters were not give. consequently, we could not keep track of their identities and were left with an insufficient sample from which to draw behavioral comparisons between the lab and field. pilot test was carried out on 10 sea cucumbers that were not tested in the mesocosm experiment to confirm previously reported reactions to a cocksure manipulate ( Legault and Himmelman 1993 ) ; each was observed for 30 min following 30 s of contact with an empty neoprene diving baseball glove. The sea cucumbers contracted slenderly following stimulation, but did not alternate between elongation and contraction, as seen in antipredator responses ( Francour 1997 ), and none of them detached. In the mesocosm, we tested each experimental national ’ second reception to a predatory sunstar 6 times, at 3- or 4-day intervals. After testing each subject 3 times, half of the subjects from each section of the wave tank car were selected using a random total generator ( Haahr 2018 ) and transplanted to the opposition section for their concluding 3 tests. Those that were not transplanted received a feign noise, where they were lifted out of the water system and set back down in a different placement within the same section. The test operation was like to that in the field experiment, except that the duration of each quiz was not limited by aqualung dive constraints. therefore, each test included a 180-s service line, 60-s predator exposure, and 60-min post-predator observation period. predator exposure was the lapp as in the discipline experiment, except that we used the lapp sunstar ( selected randomly ) to test all subjects in each part of the wave tank car on a given test day. Once the predator was removed from a national, we began the baseline period of the future topic. consequently, the 60-min post-predator notice periods in each section of the tank car overlapped. Subjects from a given section of the wave tank were tested in a haphazard order during their first test, and then in the same decree for tests 2 and 3. Following the transplant, subjects from a given section were tested in a fresh haphazard order for the fourthly trial, and then in the lapp club for tests 5 and 6. The 2 sections were constantly tested on the same day, but the order of testing alternated from one test day to the adjacent. Tests were video-recorded with the lapp camera used in the field experiment ( without its amphibious housing ). The television camera was mounted 1.3 m above the wave tank and pointed down such that its airfield of view captured the entire focal section of the tank.
Analyses
In the field experiment, we defined antipredator reaction as an increase in body supreme headquarters allied powers europe variability in reply to physical contact with a sunstar. Using trope analysis software ( Tracker, Douglas Brown, version 4.91 ), we measured the subject ’ randomness length and width ( 1-pixel accuracy ) at 5-s intervals throughout the baseline and post-predator observation periods. Length was the longest distance between the subject ’ south front tooth and posterior ends, while width was the length of the line perpendicular to the soundbox length vector that maximized the distance between the subject ’ s 2 sides. We calculated the ratio between length and width at each 5-s interval, arsenic well as the standard deviation of the resulting length-to-width ratios for both the baseline and post-predator observation periods. We refer to the standard deviation of the length-to-width ratios as “ body human body variability. ” entirely 1 subject detached from the ocean floor during testing, so we did not analyze this aspect of the antipredator response in the sphere experiment. The video camera moved slightly with curl carry through throughout the field experiment. This inevitable gesticulate may have changed the camera ’ s position of the subject and charm measures of length and width from one 5-s interval to the following. We therefore applied a correction operation. At each 5-s interval, we measured the length and width of a electrostatic object located immediately beside the subject, which had comparable size and orientation. such objects were either the lead weight used to identify the subject or, if the system of weights was not wholly within the field of horizon, a rock with distinctive rhodolith markings ( as seen in Figure 1C ). Changes in length or width of the object caused by any change in camera slant, relative to corresponding measurements obtained from the first 5-s interval of the test, were used to calculate correction factors for length and width during that time interval. We used linear arrested development to test whether a subject ’ randomness astuteness at the field web site influenced the forte and unevenness of the hydrodynamic forces surrounding it. We defined military capability as the median of the 660 accelerations recorded during a subject ’ second 3 tests, and unevenness as the interquartile image. We used non-parametric measures of forte and variability because histogram showed that the acceleration data were positively skewed. Before examining antipredator responses, we tested for a kinship between the ocean cucumbers ’ natural bodily process levels and their local hydrodynamic environment and prison term of day. On a given examination day, we defined natural bodily process flat as each subject ’ sulfur body form variability during the baseline observation period. We used a linear mix effects model ( LMM ) to test whether a national ’ second baseline body determine variability covaried with the force of hydrodynamic forces during its 220-s test menstruation and the time of day ( hours since midnight ), with subject identity included as a random wiretap to account for multiple measures from the lapp individual. This quiz showed that flow persuasiveness, but not clock of day, was a meaning forecaster of service line body human body unevenness ( LMM : effect of time : t39 =0.908, P = 0.369 ; effect of run military capability : t39 =2.21, P = 0.0329 ). Because natural bodily process levels varied with the military capability of hydrodynamic forces, we next determine whether a capable ’ sulfur baseline body form variability correlated with its body form unevenness during the post-predator observation period. A Pearson correlation coefficient showed that body shape unevenness during the post-predator time period was not related to body shape unevenness during the baseline period ( t13 =1.26, P = 0.229 ). therefore, we did not include baseline body form variability in analyses of behavior during the post-predator notice period. subsequently, we tested whether subjects increased their torso shape unevenness in response to the predatory sunstar. This was done by calculating each subject ’ south average body shape variability among its 3 baseline periods and, individually, among its 3 post-predator observation periods, and then comparing the average baseline and post-predator observation periods among subjects using a pair t-test. To test the hypothesis that antipredator demeanor is related to the strength of local hydrodynamic forces, we used analogue regression to compare a discipline ’ south average body determine variability in its 3 post-predator observation periods to the median persuasiveness of the hydrodynamic forces recorded during those periods. Tests were 2-tailed, and results were considered statistically meaning when P ≤ 0.05. In the lab mesocosm experiment, we defined an antipredator response as either an increase in body shape unevenness or detachment from the substrate in response to contact with a sunstar. We calculated each subject ’ second body supreme headquarters allied powers europe unevenness during the service line and post-predator notice periods following the like methods as described for the plain experiment. however, we measured each capable ’ second distance and width at 10-s intervals ( alternatively of 5-s intervals ) and we did not apply a correction routine to the measurements since the television camera did not move during tests. We noted whether subjects detached from the substrate during the quiz periods. One person, which was in the weakly agitated department of the tank throughout the experiment, climbed the slope of the tank and was out of the video recording human body during all 3 tests of the post-transplant period. Data from this subjugate were not included in analyses involving the post-transplant period. The mesocosm was operated as a closed system, so it is potential that chemicals released by the sunstar or sea cucumbers accumulated in the tank and affected antipredator responses. such collection could potentially create test ordain effects that could make the responses of unlike subjects non-independent. Before proceeding with analyses, we tested whether the order in which a subject was exposed to the sunstar on a given day ( i.e., 1–10 ) affected the lastingness of its antipredator responses. The order of testing did not affect a subject ’ sulfur beggarly body shape unevenness during its 3 tests from before the reciprocal transplant ( linear regression : t34 =0.086, P = 0.932 ) or during its 3 tests after the reciprocal transplant ( linear regression : t34 =1.00, P = 0.324 ). It besides did not affect the number of tests in which an person detached during its 3 pre-transplant tests ( linear arrested development : t36 =0.57, P = 0.574 ) or its 3 post-transplant tests ( analogue regression : t36 =0.70, P = 0.488 ). After establishing that behavior was independent of presentation order, our first motion was whether body form unevenness changed in response to marauder photograph. We performed a match t-test, fair as for the field experiment, but calculated each individual ’ second average body determine variability across all 6 service line and post-predator observation periods. A few subjects climbed the walls of the tank and partially left the television ensnare, thus preventing body supreme headquarters allied powers europe variability from being measured ( 31 baseline measures from 14 subjects and 33 post-predator measures from 17 subjects ). These tests were excluded from the calculation of average body supreme headquarters allied powers europe variability. however, this normally occurred in only some of a subjugate ’ mho 6 tests, so it was hush potential to calculate an average for that capable from its remaining tests. To evaluate whether subjects had a higher probability of detaching from the substrate in response to the sunstar, we used a Wilcoxon signed ranks trial to compare the issue of baseline periods ( 0−6 ) and the number of post-predator notice periods ( 0−6 ) in which each national detached. Our adjacent interrogate was whether antipredator responses differed between the 2 hydrodynamic environments. subject variables were the average consistency shape variability and entire count of tests in which a subject detached. The mugwump variable was “ hydrodynamic condition ” ( decrepit agitated or strongly agitated ). Each variable was tested individually during the pre-transplant and post-transplant periods because half of the individuals changed hydrodynamic conditions during the transplant. consequently, the issue of tests in which a submit detached varied from 0 to 3 in both pre-transplant and post-transplant analyses. Body shape unevenness was compared between hydrodynamic conditions with odd t-tests, and the issue of detachments was compared with Mann–Whitney tests. Because we used 4 mugwump tests to address the same question, we controlled for inflate gamble of type I error using the consecutive Bonferroni method acting ( Holm 1979 ). We present only the adjusted P-values. Our final question was whether ocean cucumbers alter antipredator behavior in answer to a sudden transfer in hydrodynamic forces. Sea cucumbers experienced 3 types of hydrodynamic shifts during the transplant experiment : strongly to weakly agitated urine, decrepit to powerfully agitated water, and no switch. Splitting the no deepen group into the 2 types of fake disturbance ( strongly to powerfully agitated and weakly to weakly agitated ) would add no extra information about environmental change but would cost statistical power due to our small sample distribution size. The dependent variable was the change in the total number of tests in which a subject detached ( i, post-transplant – pre-transplant ), and frankincense ranged from −3 to 3. The change in detachment frequency was compared among the 3 transplant conditions using a 1-way ANOVA with post hoc pairwise comparisons. We corrected for multiple military post hoc comparisons ( Holm 1979 ) and presented only the adjusted P-values. We did not analyze consistency shape unevenness for this doubt because there was no effect of hydrodynamic circumstance on torso supreme headquarters allied powers europe unevenness in the former set of analyses ( see the “ Results ” section ). effect sizes for all parametric tests were measured using Cohen ’ mho d ( Cohen 1988 ; Sawilowsky 2009 ). All analyses were conducted in R ( adaptation 3.3.1 ; R Core Team 2016 ).
Ethical note
All research practices complied with the “ Guidelines for the discussion of animals in behavioral research and teaching ” set forth by the Animal Behavior Society ( Buchanan et aluminum. 2012 ), and with the “ Guide to the care and use of experimental animals ” set forth by the Canadian Council on Animal Care ( Olfert et alabama. 1993 ). These experiments were conducted under Memorial University of Newfoundland animal care and practice protocol act IACC 15-05-PG.
Results
Field experiment
Sea cucumbers were distributed along a pronounce hydrodynamic gradient that covaried with astuteness ( Figure 3 ). Shallower individuals experienced stronger ( analogue regression : F1,13 =59.2, P < 0.001, R2 =0.82 ) and more variable ( F1,13 =66.9, P < 0.001, R2 =0.84 ) flow accelerations than deeper individuals. Long-term flow acceleration data were consistent with this form ; stronger and more variable hourly accelerations occurred at the shallow extreme, whereas faint, less variable flow accelerations occurred at the deep extreme. interestingly, the range of run accelerations observed during short tests spanned most of the roll of the long-run accelerations observed throughout the entire study ( Figure 3 ).
figure 3 .
Open in new tabDownload slide Water flow acceleration by depth for 15 orange-footed ocean cucumbers. Each open traffic circle shows the median instantaneous acceleration at a given submit ’ mho location and the thick line shows the line of best equip among these points. The 2 dilute solid lines are the lines of best meet for the 10th ( lower line ) and 90th ( upper line ) percentile values of the acceleration values calculated at each of the 15 subjects ’ locations, and the outermost dashed lines are the lines of best paroxysm for the minimum ( lower tune ) and maximum values at each of these locations. The close circles are the median of the hourly mean flow accelerations at the 2 ends of the study site from the long-run data, and the associate error bars show the inter-quartile ranges ( dense mistake bars ) and ranges ( thinly error bars ) for the long-run acceleration measurements. figure 3 .Open in new tabDownload slide Water flow acceleration by depth for 15 orange-footed ocean cucumbers. Each open traffic circle shows the medial instantaneous acceleration at a given subject ’ mho location and the thick wrinkle shows the pipeline of best fit among these points. The 2 thin solid lines are the lines of best fit for the 10th ( lower line ) and 90th ( upper line ) percentile values of the acceleration values calculated at each of the 15 subjects ’ locations, and the outermost dashed lines are the lines of best match for the minimum ( lower line ) and maximal values at each of these locations. The closed circles are the median of the hourly mean flow accelerations at the 2 ends of the study web site from the long-run data, and the consociate error bars show the inter-quartile ranges ( chummy error bars ) and ranges ( flimsy error bars ) for the long-run acceleration measurements. exposure to sunstars increased the body form unevenness of the 15 orange-footed sea cucumbers. Body condition variability was importantly greater during the post-predator observation periods ( mean ±SD : 0.20 ± 0.04 ) than during the correspond baseline periods ( mean ±SD : 0.15 ± 0.07 ; paired samples t-test : t14 =2.6, P = 0.021, five hundred = 0.7 ). Antipredator behavior was not related to the military capability of the submit ’ s local hydrodynamic forces, since average body form variability during the submit ’ south 3 post-predator observation periods ( one from each testing sidereal day ) did not covary with the median instantaneous hang acceleration recorded throughout the 3 tests ( linear regression : F1,13 =0.0, P = 0.902, R2 < 0.01 ).
Laboratory mesocosm experiment
exposure to a sunstar elicited antipredator demeanor among the 38 orange-footed sea cucumbers tested. specifically, the average torso form variability for a subject ’ second 6 post-predator observation periods ( mean ±SD : 0.39 ± 0.18 ) was importantly greater than the average consistency shape variability observed for its 6 baseline periods ( mean ±SD : 0.09 ± 0.05 ; paired samples t-test : t37 =10.7, P < 0.001, five hundred = 1.7 ). Furthermore, no sea cucumbers detached during any of their baseline periods, whereas 30 of the 38 sea cucumbers detached during at least 1 of their 6 post-predator notice periods ( medial [ IQR ] count of post-predator observation periods in which a sea cucumber detached : 1.5 [ 1–4 ] tests ; Wilcoxon signed ranks trial : V = 465, P < 0.001 ). Body form variability did not differ between the weakly agitated ( mean ±SD : 0.41 ± 0.24 ) and powerfully agitated ( mean ±SD : 0.43 ± 0.17 ) conditions during the pre-transplant period ( odd t-test : t34 =0.29, Padj = > 0.999, d = 0.10 ), or between the weakly agitated ( beggarly ±SD : 0.43 ± 0.22 ) and powerfully agitated ( think of ±SD : 0.33 ± 0.22 ) conditions during the post-transplant period ( t34 =1.4, Padj =0.526, vitamin d = 0.46 ). similarly, the total of tests in which a ocean cucumber detached did not differ between the weakly agitated ( medial [ IQR ] : 1 [ 0–1.5 ] tests ) and strongly agitated ( median [ IQR ] : 1 [ 0.5–1 ] tests ) conditions during the pre-transplant condition ( Mann–Whitney test : W = 163.5, Padj = > 0.999 ). however, sea cucumbers detached more frequently in the weakly agitated condition ( median [ IQR ] : 2 [ 1–3 ] tests ) than in the strongly agitated condition ( median [ IQR ] : 0 [ 0–1 ] tests ) during the post-transplant period ( W = 273, Padj =0.020 ). The type of environmental change experienced during the reciprocal transplant had a significant effect on the change in detachment frequency ( 1-way ANOVA : F2,35 =3.9, P = 0.030, Radj2 =0.14 ). specifically, individuals that had been moved from powerfully to weakly stir water showed a significant increase in detachment frequency proportional to individuals that moved from decrepit to powerfully agitated water ( post hoc comparison : Padj =0.030 ; Figure 4 ).
figure 4 .
Open in new tabDownload slide effect of multiplicative inverse transplants on the issue of post-predator observation periods in which a subject detached from the substrate. open squares connected by a crash credit line map subjects moved from powerfully to weakly agitated conditions. solid squares connected by a solid line represent subjects moved from weakly to powerfully agitated conditions. solid circles connected by a bleached grey tune represent command subjects moved to another location within the like environment ( feign disturbance ). change in behavior ( post-transplant – pre-transplant ) was compared among the 3 transplant treatments with a 1-way ANOVA. Treatments with different letters are statistically different, as indicated by post-hoc, pairwise comparisons corrected for type I error ( Holm 1979 ). calculate 4 .Open in new tabDownload slide effect of multiplicative inverse transplants on the count of post-predator observation periods in which a subject detached from the substrate. assailable squares connected by a dart note represent subjects moved from strongly to weakly agitate conditions. solid squares connected by a solid course typify subjects moved from weakly to strongly agitate conditions. solid circles connected by a languish grey line represent control subjects moved to another localization within the lapp environment ( feign disturbance ). deepen in behavior ( post-transplant – pre-transplant ) was compared among the 3 transplant treatments with a 1-way ANOVA. Treatments with different letters are statistically different, as indicated by post-hoc, pairwise comparisons corrected for character I error ( Holm 1979 ) .
Discussion
reverse to our beginning hypothesis, the strength of antipredator responses did not differ between orange-footed sea cucumbers in different hydrodynamic environments. however, sea cucumbers became less likely to detach from the substrate when hydrodynamic forces increased, and more likely to detach when hydrodynamic forces decreased, as per our moment hypothesis. These findings confirm that sea cucumbers alter their doorsill for detaching when environmental conditions change. While many studies report behavioral and morphologic malleability in vertebrates ( for example, tree-lizards, Urosaurus ornatus, Moore et alabama. 1998 ; trinidadian guppies, Poecilia reticulata, Kolluru et alabama. 2007 ), and morphologic malleability in marine invertebrates ( Bourdeau and Johansson 2012 ), few have demonstrated behavioral malleability in marine invertebrates ( Padilla and Savedo 2013 ). Exceptions from outside the echinodermata include soft-shell clams ( Mya areneria ), which bury deeper into the sediments when exposed to predators ( Whitlow 2010 ), mussels ( M. edulis ), which cluster together in response to a predator ( Côté and Jelnikar 1999 ), and coral polyps ( Porites compressa ), which withdraw into their protective skeletons for longer when predators are near ( Gochfeld 2004 ). There are besides examples of behavioral malleability in echinoderms. For model, sandpaper dollar Dendraster excentricus larva discontinue growing and begin cloning upon detecting mucus from predatory fish, as smaller body size affords a irregular refuge from depredation ( Vaughn and Strathmann 2008 ). These larvae besides avoid marauding fish cues by shifting their distribution in the water column ( Arellano et alabama. 2012 ). Likewise, sea urchins Psammechinus miliaris exhibit variable morphology of feeding structures and foraging behaviors in different trophic environments ( Hughes et alabama. 2012 ). In these examples, behavioral malleability is exhibited in response to the animal ’ s biotic environment. To our cognition, our study demonstrates, for the first time, malleability in the antipredator behavior of a slow-moving marine invertebrate that is induced by changes in its abiotic environment. thus, it joins a growing literature that is uncovering the ten thousand adaptations that echinoderms and other slow-moving and sessile marine organisms demonstrate in reception to environmental deepen. The force of ocean cucumbers ’ antipredator responses did not differ between the decrepit and strongly agitate conditions of the mesocosm experiment before transplants, or in relative to the hydrodynamic forces in the field experiment. It is possible that sea cucumbers in the airfield had insufficient time to produce a complete antipredator reaction. indeed, changes in torso form unevenness between the baseline and post-predator observation periods were more than 6 times greater in the mesocosm experiment, where the post-predator observation period lasted for 60 min, than in the discipline experiment, where it lasted for merely 2 min. As we and others have observed ( Legault and Himmelman 1993 ), a sea cucumber ’ s antipredator reaction can last for more than an hour after the sunstar is removed. Although the plain experiment enabled us to observe antipredator behavior in the wild, and to characterize the hydrodynamic conditions experienced by sea cucumbers, the short-change sample periods imposed by aqualung dive may have obscured a more elusive relationship between the persuasiveness of a ocean cucumber ’ mho antipredator behavior and local hydrodynamic conditions. besides, no wave tank can absolutely simulate hydrodynamic forces generated in the ocean. hydrodynamic forces in intertidal and shallow marine environments are highly varying spatially and temporally ( Denny 1988 ), which limits reproducibility in roll tanks. While beckon and flume tank car experiments are normally used to isolate effects of hydrodynamic forces on benthic organisms ( for example, Harvey et aluminum. 1995 ; Kawamata 1998 ; Gagnon et alabama. 2003 ; Peralta et alabama. 2008 ; Morse and Hunt 2013 ), test subjects in the confront sketch may have habituated more cursorily to the artificial rhythm of hydrodynamic forces in the tank. Since hydrodynamic forces were both stronger and more variable in the shallow environment, it would be valuable to assess the independent and combine effects of flow potency and variability on antipredator responses. alternatively, a relationship between antipredator responses and hydrodynamic forces may emerge only in answer to late changes in hydrodynamic conditions and may then weaken over clock time as the novelty of change disappears. Animals that show behavioral malleability in reply to sudden environmental change often respond powerfully at first, but then show diminish responses over time ( Tuomainen and Candolin 2011 ). Marmosets ( Callithrix penicillata ), for example, show increased watchfulness in fresh environments, but then show decrease watchfulness with repeat exposures to that lapp environment ( Barros et alabama. 2008 ). Some nautical invertebrates besides exhibit behavioral malleability that diminishes with drawn-out exposure to new environments. Copepods ( Centropages hamatus ) display heightened escape responses immediately following the attack of increase water turbulence, but quickly use and begin showing the same responses that are seen in non-turbulent water ( Hwang et alabama. 1994 ). therefore, differences in the antipredator behavior of orange-footed sea cucumbers may reflect short-run responses to holocene environmental change, rather than elongated responses to static differences in local hydrodynamic conditions. Sea cucumbers in the mesocosm experiment responded to changes in hydrodynamic forces, so far the degree to which this reception occurs in the wild remains strange, and far research is required to determine whether such malleability is adaptive. We suggest that individuals experiencing a chemise to less stir waters express stronger antipredator behavior in response to an attack because the consort risk of being washed aside is reduced. While a nearby predator may seem like the greater risk, the chemical cues sea cucumbers use to detect predators indicate only that a predator is nearby, and not necessarily that one is hunting ( Legault and Himmelman 1993 ). Sea cucumbers are often dumbly aggregated, and therefore even if a marauder is hunting, an individual ocean cucumber ’ randomness risk of being targeted during an attack may be quite moo ( Hamilton 1971 ; Legault and Himmelman 1993 ; So 2009 ). Furthermore, foraging efficiency of predators may be reduced under stronger hydrodynamic forces. disruptive water flows may dissipate smell plumes, making it more unmanageable for mobile predators that rely on chemosensory mechanisms to detect prey ; predators may besides experience higher mortality rates than their prey under relatively hard hydrodynamic forces ( Powers and Kittinger 2002 ; Petes et aluminum. 2008 ). Marine invertebrates often “ scale ” antipredator reactions to the degree of predation risk ( Thomas and Gruffydd 1971 ; Smee and Weissburg 2006 ; Selander et aluminum. 2011 ). A commodity exemplar is the sea penitentiary, Ptilosarcus gurneyi, which becomes more likely to burrow in the sediment when exposed to sea stars that are more specify predators, and will only burrow upon forcible contact, not in response to waterborne predatory cues ( Weightman and Arsenault 2002 ). Increasing hydrodynamic forces might thus provide sea cucumbers with a cue of belittled predation risk, causing a shift toward a lower likelihood of detaching. If insulation increases a sea cucumber ’ s likelihood of escaping a predatory attack, as previous studies suggest ( Kropp 1982 ; Legault and Himmelman 1993 ; So 2009 ), our results may indicate that a tradeoff is imposed by detaching and floating in stronger flow environments. Sea cucumbers in the raving mad experience changing hydrodynamic conditions, such as those simulated in our experiment, in at least 2 situations. First, newly settled orange-footed ocean cucumbers migrate from shallow to deeper waters over a period of respective months, beginning in fall ( Hamel and Mercier 1996 ). Although our transplants occurred over a much shorter time period, the mechanisms underlying the phenotypical malleability observed in our experiment may have evolved in the context of migration. Second, severe storms can dramatically increase body of water flow within a few hours ( Harmelin-Vivien 1994 ), which approximates the timescale of change simulated in our mesocosm experiment. The rapid switch created by storms could besides explain why sea cucumbers have evolved the capacity to quickly alter antipredator responses, since this could mitigate the risk of being washed away into inapplicable environments. Some tell suggests that when an orange-footed sea cucumber is swept onto indulgent substrata, where it is unable to attach, it becomes emaciated and finally dies ( So et alabama. 2010 ). If so, being swept ashore is not the merely hazard associated with insulation ; sea cucumbers could besides be displaced into undesirable habitats at the thick end of their distribution. thus, malleability in antipredator responses may allow orange-footed ocean cucumbers to mitigate the hazard of being displaced into unsuitable habitat. future research should assess the adaptive value of this malleability by testing whether strong antipredator responses, such as detach, tip to a higher hazard of stranding and mortality on a ocean floor with firm hydrodynamic forces.
Acknowledgments
We are grateful to D. Bélanger, A.P. St-Pierre, A. Przybysz, and J. Carberry for help with field and testing ground make. We besides thank A. Mercier, B. Gianasi, and 2 anonymous reviewers for constructive comments that improved the manuscript.
Funding
This research was funded by the Natural Sciences and Engineering Research Council of Canada ( NSERC Discovery Grants to D.R.W. [ RGPIN-2015-03769 ] and P.G. [ RGPIN-2015-05343 ] ), the Canada Foundation for Innovation ( Leaders Opportunity Fund to P.G. [ 16940 ] ), and the Research & Development Corporation of Newfoundland and Labrador ( IgniteR & D Grant to P.G. [ 5003.070.002 ] ).
References
Adler
FR
,
Harvell
CD
, 1990.
Inducible defenses, phenotypical variability and biotic environments. Trends Ecol Evol 5: 407– 410.
Angilletta
MJ
,
Huey
RB
,
Frazier
MR
, 2010.
thermodynamic effects on organismal performance : is hotter estimable ? Physiol Biochem Zool 83: 197– 206.
Arellano
SM
,
Reitzel
AM
,
Button
CA
, 2012.
variation in upright distribution of backbone dollar larvae relative to haloclines, food, and fish cues. J Exp Mar Biol Ecol 414–415: 28– 37.
Babarro
JMF
,
Carrington
E
, 2013.
attachment strength of the mussel Mytilus galloprovincialis : consequence of habitat and body size. J Exp Mar Biol Ecol 443: 188– 196.
Barkai
A
, 1991.
The effect of water motion on the distribution and interaction of three sea cucumber species on the confederacy african west seashore. J Exp Mar Biol Ecol 153: 241– 254.
Barros
M
,
Alencar
C
,
de Souza Silva
MA
,
Tomaz
C
, 2008.
Changes in experimental conditions alter anti-predator watchfulness and sequence predictability in captive marmosets. Behav Processes 77: 351– 356.
Blain
C
,
Gagnon
P
, 2014.
Canopy-forming seaweeds in urchin-dominated systems in eastern Canada : structure forces or dim-witted prey for anchor grazers ? PLoS ONE 9: e98204.
Bourdeau
PE
,
Johansson
F
, 2012.
Predator-induced geomorphologic defences as by-products of prey behavior : a review and course catalog. Oikos 121: 1175– 1190.
Buchanan
K
,
Burt de Perera
T
,
Carere
C
,
Carter
T
,
Hailey
A
et alabama., 2012.
Guidelines for the treatment of animals in behavioral inquiry and teaching. Anim Behav 83: 301– 309.
Carballo
JL
,
Ávila
E
,
Enríquez
S
,
Camacho
L
, 2006.
Phenotypic malleability in a mutualistic association between the sponge Haliclona caerulea and the calcareous macroalga Jania adherens induced by transplanting experiments. I : morphologic responses of the sponge. Mar Biol 148: 467– 478.
Caro
AU
,
Castilla
JC
, 2004.
Predator-inducible defences and local anesthetic intrapopulation variability of the intertidal mussel Semimytilus algosus in cardinal Chile. Mar Ecol Prog Ser 276: 115– 123.
Carrington
E
, 2002.
seasonal worker version in the fastening strength of blue mussels : causes and consequences. Limnol Oceanogr 47: 1723– 1733.
Cohen-Rengifo
M
,
Moureaux
C
,
Dubois
P
,
Flammang
P
, 2017.
Attachment capability of the sea urchin Paracentrotus lividus in a image of seawater velocities in relation to test morphology and tube foundation mechanical properties. Mar Biol 164: 79.
Cohen
J
, 1988. statistical Power Analysis for the Behavioral Sciences. 2nd edn.
New York:
Lawrence Erlbaum Associates.. 2nd edn .
Côté
IM
,
Jelnikar
E
, 1999.
Predator-induced clumping behavior in mussels ( Mytilus edulis Linnaeus ). J Exp Mar Biol Ecol 235: 201– 211.
Denny
MW
, 1988. Biology and the Mechanics of the Wave-Swept Environment.
princeton university:
Princeton University Press.
Denny
MW
,
Wethey
D
, 2001. Physical processes that generate patterns in marine communities. In: Bertness MD, Gaines SD, Hay ME, editors. Marine Community Ecology.
sunderland:
Sinauer Associates, 3– 37. . physical processes that generate patterns in marine communities. In : Bertness MD, Gaines SD, Hay ME, editors .
Dukas
R
, editor. 1998. cognitive ecology.
Chicago:
University of Chicago Press.
Edelaar
P
,
Wright
J
, 2006.
likely prey make excellent ornithologists : adaptive, compromising responses towards avian depredation terror by arab Babblers Turdoides squamiceps survive at a migratory hot spot. ibis 148: 664– 671.
Feder
HM
, 1972.
escape responses in marine invertebrates. Sci Am 227: 92– 101.
Figurski
JD
,
Malone
D
,
Lacy
JR
,
Denny
MW
, 2011.
An cheap instrument for measuring wave exposure and water speed. Limnol Oceanogr Methods 9: 204– 214.
Francour
P
, 1997.
predation on holothurians : a literature follow-up. Invertebr Biol 116: 52– 60.
Franz
DR
,
Worley
EK
,
Merrill
AS
, 1981.
Distribution patterns of common seastars of the Middle Atlantic Continental Shelf of the Northwest Atlantic ( Gulf of Maine to Cape Hatteras ). Biol Bull 160: 394– 418.
Freeman
AS
,
Byers
JE
, 2006.
Divergent induced responses to an invasive marauder in marine mussel populations. science 58: 831– 833.
Frey
DL
,
Gagnon
P
, 2015.
Thermal and hydrodynamic environments mediate individual and aggregate eating of a functionally important omnivore in reef communities. PLoS ONE 10: 1– 28.
Frey
DL
,
Gagnon
P
, 2016.
spatial dynamics of the green ocean urchin Strongylocentrotus droebachiensis in food-depleted habitats. Mar Ecol Prog Ser 552: 223– 240.
Gagnon
P
,
Wagner
G
,
Himmelman
JH
, 2003.
Use of a brandish tank to study the effects of water movement and algal movement on the supplanting of the sea star Asterias vulgaris towards its prey. Mar Ecol Prog Ser 258: 125– 132.
Gianasi
BL
,
Verkaik
K
,
Hamel
J-F
,
Mercier
A
, 2015.
Novel practice of PIT tags in sea cucumbers : predict results with the commercial species Cucumaria frondosa. PLoS ONE 10: 1– 22.
Gibson
RN
, 2003.
Go with the flow : tidal migrations in marine animals. Hydrobiologia 503: 153– 161.
Gochfeld
DJ
, 2004.
Predation-induced morphologic and behavioral defenses in a hard coral : implications for foraging behavior of coral-feeding butterflyfishes. Mar Ecol Prog Ser 267: 145– 158.
Haahr
M
, 2018. RANDOM.ORG : true Random Number Service.
Randomness Integr. Serv. Ltd (October 2015, date last accessed). ( October 2015, date last access ) .
Hamel
J-F
,
Mercier
A
, 1996.
early development, village, growth, and spatial distribution of the sea cucumber Cucumaria frondosa ( Echinodermata : holothuroidea ). Can J Fish Aquat Sci 53: 253– 271.
Hamilton
WD
, 1971.
geometry for the selfish herd. J Theor Biol 31: 295– 311.
Hancock
DA
, 1958.
Notes on starfish on an Essex oyster seam. J Mar Biol Assoc U K 37: 565– 589.
Harmelin-Vivien
ML
, 1994.
The effects of storms and cyclones on coral reefs : a revue. J Coast Res 12: 211– 231.
Harvell
CD
, 1984.
Predator-induced department of defense in a nautical bryozoan. skill 224: 1357– 1359.
Harvell
CD
, 1986.
The ecology and evolution of inducible defenses in a marine bryozoan—cues, costs, and consequences. Am Nat 128: 810– 823.
Harvey
M
,
Bourget
E
,
Ingram
RG
, 1995.
experimental tell of passive collection of marine bivalve larva on filamentous epibenthic structures. Limnol Oceanogr 40: 94– 104.
Hayne
KJR
,
Palmer
AR
, 2013.
Intertidal sea stars ( Pisaster ochraceus ) alter soundbox shape in reaction to wave military action. J Exp Biol 216: 1717– 1725.
Helfman
GS
, 1989.
Threat-sensitive marauder avoidance in damselfish–trumpetfish interactions. Behav Ecol Sociobiol 24: 47– 58.
Heynen
M
,
Bunnefeld
N
,
Borcherding
J
, 2017.
Facing different predators : adaptiveness of behavioral and morphologic traits under depredation. Curr Zool 63: 249– 257.
Himmelman
JH
,
Dutil
C
, 1991.
distribution, population structure and eating of subtidal seastars in the northerly Gulf of St. Lawrence. Mar Ecol Prog Ser 76: 61– 72.
Hölker
F
,
Stief
P
, 2005.
adaptive behavior of chironomid larva ( Chironomus riparius ) in response to chemical stimuli from predators and resource density. Behav Ecol Sociobiol 58: 256– 263.
Holm
S
, 1979.
A simple consecutive rejective multiple test operation. Scand J Stat 6: 65– 70.
Hughes
AD
,
Brunner
L
,
Cook
EJ
,
Kelly
MS
,
Wilson
B
, 2012.
Echinoderms display morphologic and behavioral phenotypical malleability in response to their trophic environment. PLoS ONE 7: e41243.
Hultgren
KM
,
Mittelstaedt
H
, 2015.
Color change in a marine isopod is adaptive in reducing predation. Curr Zool 61: 739– 748.
Hwang
JS
,
Costello
JH
,
Strickler
JR
, 1994.
Copepod graze in disruptive menstruate : lift forage behavior and habituation of escape responses. J Plankton Res 16: 421– 431.
Jangoux
M
,
van Impe
E
, 1977.
The annual pyloric cycle of Asterias rubens L. ( echinodermata : asteroidea ). J Exp Mar Biol Ecol 30: 165– 184.
Kawamata
S
, 1998.
effect of wave-induced oscillatory flow on browse by a subtidal sea urchin Strongylocentrotus nudus ( A. Agassiz ). J Exp Mar Biol Ecol 224: 31– 48.
Klugh
AB
, 1923.
The habits of Cucumaria frondosa. Can Field Nat 37: 76– 77.
Kolluru
GR
,
Grether
GF
,
Contreras
H
, 2007.
environmental and genetic influences on mating strategies along a replicated food handiness gradient in guppies ( Poecilia reticulata ). Behav Ecol Sociobiol 61: 689– 701.
Kropp
RK
, 1982.
Responses of five sea cucumber species to attacks by a predatory gastropod, Tonna perdix. Pacific Sci 36: 445– 452.
Kühnhold
H
,
Kamyab
E
,
Novais
S
,
Indriana
L
,
Kunzmann
A
et alabama., 2017.
Thermal stress effects on department of energy resource allocation and oxygen pulmonary tuberculosis rate in the juvenile sea cucumber, Holothuria scabra ( Jaeger, 1833 ). aquaculture 467: 109– 117.
Lawrence
JM
, 1975.
On the relationships between marine plants and sea urchins. Oceanogr Mar Biol Annu Rev 13: 213– 286.
Legault
C
,
Himmelman
JH
, 1993.
relation between escape behavior of benthic nautical invertebrates and the risk of depredation. J Exp Mar Biol Ecol 170: 55– 74.
Leonard
GH
,
Bertness
MD
,
Yund
PO
,
Jan
N
, 1999.
Crab depredation, waterborne cues, and inducible defenses in the blue mussel, Mytilus edulis. ecology 80: 1– 14.
Lima
SL
,
Dill
LM
, 1990.
behavioral decisions made under the hazard of depredation : a review and course catalog. Can J Zool 68: 619– 640.
López
RA
,
Penchaszadeh
PE
,
Marcomini
SC
, 2008.
Storm-related strandings of mollusks on the Northeast coast of Buenos Aires, Argentina. J Coast Res 244: 925– 935.
Mauzey
KP
,
Birkeland
C
,
Dayton
PK
, 1968.
Feeding behavior of Asteroids and escape responses of their prey in the Puget Sound region. ecology 49: 603– 619.
Moore
MC
,
Hews
DK
,
Knapp
R
, 1998.
Hormonal control and development of option male phenotypes : generalizations of models for sexual differentiation. Am Zool 38: 133– 151.
Morse
BL
,
Hunt
HL
, 2013.
effect of unidirectional urine currents on displacement behavior of the green sea urchin Strongylocentrous droebachiensis. J Mar Biol Assoc U K 93: 1923– 1928.
Morton
B
, 1991.
Aspects of predation by Tonna zonatum ( Prosobranchia : Tonnoidea ) feed on holothurians in Hong Kong. J Molluscan Stud 57: 11– 19.
Olfert
ED
,
Cross
BM
,
McWilliam
AA
, editors. 1993. Guide to the Care and Use of Experimental Animals. 2nd edn.
Ottawa, ON:
canadian Council on Animal Care.. 2nd edn .
Padilla
DK
,
Adolph
SC
, 1996.
Plastic inducible morphologies are not always adaptive : the importance of time delays in a stochastic environment. Evol Ecol 10: 105– 117.
Padilla
DK
,
Savedo
MM
, 2013. A systematic review of phenotypic plasticity in marine invertebrate and plant systems. In: Lesser m Advances in Marine Biology, Vol. 65, 1st edn.
San Diego, USA:
Academic Press, 67– 94. . A systematic review of phenotypical malleability in marine invertebrate and plant systems. In :, editor., Vol., 1st edn .
Peralta
G
,
Van Duren
LA
,
Morris
EP
,
Bouma
TJ
, 2008.
Consequences of shoot density and stiffness for ecosystem engineering by benthic macrophytes in flow dominated areas : a hydrodynamic gulch sketch. Mar Ecol Prog Ser 368: 103– 115.
Petes
LE
,
Mouchka
ME
,
Milston-Clements
RH
,
Momoda
TS
,
Menge
BA
, 2008.
Effects of environmental stress on intertidal mussels and their ocean asterisk predators. Oecologia 156: 671– 680.
Powers
SP
,
Kittinger
JN
, 2002.
Hydrodynamic mediation of predator–prey interactions : differential patterns of prey susceptibility and predator success explained by magnetic declination in water flow. J Exp Mar Biol Ecol 273: 171– 187.
Price
TD
,
Qvarnstrom
A
,
Irwin
DE
, 2003.
The function of phenotypical malleability in driving genetic development. Proc R Soc B Biol Sci 270: 1433– 1440. R Core Team, 2016. roentgen : A terminology and environment for statistical calculate.
Vienna, Austria:
R Foundation for Statistical Computing.
Rochette
R
,
Hamel
JF
,
Himmelman
JH
, 1994.
Foraging strategy of the asteroid Leptasterias polaris : character of prey odors, current and feed condition. Mar Ecol Prog Ser 106: 93– 100.
Saloom
ME
,
Duncan
RS
, 2005.
Low dissolved oxygen levels reduce anti-predation behavior of the fresh water clam Corbicula fluminea. Freshw Biol 50: 1233– 1238.
Sawilowsky
S
, 2009.
New effect size rules of flick. J Mod Appl Stat Methods 8: 467– 474.
Selander
E
,
Jakobsen
HH
,
Lombard
F
,
Kiorboe
T
, 2011.
Grazer cues induce stealth behavior in marine dinoflagellates. Proc Natl Acad Sci USA 108: 4030– 4034.
Shivji
M
,
Parker
D
,
Hartwick
B
,
Smith
M
,
Sloan
N
, 1983.
Feeding and distribution cogitation of the sunflower ocean star Pycnopodia helianthoides ( Brandt, 1835 ). Pacific Sci 37: 133– 140.
Sih
A
, 1986.
Antipredator responses and the perception of danger by mosquito larva. ecology 67: 434– 441.
Smee
DL
,
Weissburg
MJ
, 2006.
hard dollar ( Mercenaria mercenaria ) measure depredation risk using chemical signals from predators and hurt conspecifics. J Chem Ecol 32: 605– 619.
So
JJ
, 2009. Assessment of the biology, ecology and genetic structure of the sea cucumber Cucumaria frondosa for management of the fishery in the Newfoundland and Labrador region [MSc thesis].
Canada:
Memorial University of Newfoundland and Labrador. . assessment of the biology, ecology and familial structure of the sea cucumber Cucumaria frondosa for management of the fishery in the Newfoundland and Labrador area [ MSc thesis ] .
So
JJ
,
Hamel
J-F
,
Mercier
A
, 2010.
Habitat use, increase and depredation of Cucumaria frondosa : implications for an emerging sea cucumber fishery. fish Manag Ecol 17: 473– 484.
St-Pierre
AP
,
Gagnon
P
, 2015a.
Effects of temperature, body size, and starvation on feed in a major echinoderm predator. Mar Biol 162: 1125– 1135.
St-Pierre
AP
,
Gagnon
P
, 2015b.
Wave natural process and starvation tone intra-annual magnetic declination in displacement, microhabitat survival, and ability to contact prey in the common ocean headliner, Asterias rubens Linnaeus. J Exp Mar Biol Ecol 467: 95– 107.
Stearns
SC
, 1989.
The evolutionary significance of phenotypical malleability : phenotypical sources of variation among organisms can be described by developmental switches and reaction norms. life science 39: 436– 445.
Sun
J
,
Hamel
J-F
,
Mercier
A
, 2018.
charm of flow on locomotion, feeding behavior and spatial distribution of a suspension-feeding sea cucumber. J Exp Biol 221:pii:jeb189597. : pii : jeb189597 .
Tagliarolo
M
,
Porri
F
,
Scharler
UM
, 2018.
Temperature-induced unevenness in metabolic activity of ecologically crucial estuarine macrobenthos. Mar Biol 165: 1– 13.
Thomas
GE
,
Gruffydd
LD
, 1971.
The types of escape reactions elicited in the scallop Pecten maximus by selected sea-star species. Mar Biol 10: 87– 93.
Tuomainen
U
,
Candolin
U
, 2011.
behavioral responses to human-induced environmental transfer. Biol Rev 86: 640– 657.
Ursin
E
, 1960. A quantitative investigation of the echinoderm fauna of the central North Sea [Ph.D thesis]. Copenhagen, Denmark: Universität Kopenhagen.. A quantitative probe of the echinoderm fauna of the central North Sea [ Ph.D dissertation ]. Copenhagen, Denmark : Universität Kopenhagen .
Vaughn
D
,
Strathmann
RR
, 2008.
Predators induce cloning in echinoderm larva. science 319: 1503 .
Weightman
JO
,
Arsenault
DJ
, 2002.
Predator classification by the ocean pen Ptilosarcus gurneyi ( Cnidaria ) : function of waterborne chemical cues and physical touch with marauding sea stars. Can J Zool 80: 185– 190.
Whitlow
WL
, 2010.
Changes in survivorship, behavior, and morphology in native soft-shell clams induced by invasive green crab predators. Mar Ecol 31: 418– 430.
Winter
MA
,
Hamilton
PV
, 1985.
Factors influencing swim in bay scallops, Argopecten irradians ( Lamarck, 1819 ). J Exp Mar Biol Ecol 88: 227– 242.
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